Keywords: human papillomavirus, cervical cancer, cervical precancerous lesion, genotype, meta-analysis

Summary of eligible studies

We retrieved 1274 citations from the search strategy (Appendix S1), and 190 potentially relevant articles were identified for full-text review. Data were abstracted from 45 eligible studies that met the eligibility criteria [10–54]. The study flow diagram is shown in Figure1.

Study characteristics

Forty-five eligible studies published between 1996 and 2016, including forty-one single-center [10–50] and four multi-center studies [51–54], were documented in this review. Among these studies, 12 were conducted in East China [10–21], 3 in South China [22–24], 4 in West China [25–28], 14 in North China [29–42], 3 in Taiwan [43–45], 4 in Hong Kong [46–49], and 1 in Macao [50].

A total of 49,997 eligible women from 32 provinces and municipalities were recruited to participate in these studies (Figure2). Out of 49,997 women tested for overall HPV prevalence, 19,361 (38.7%) had normal cervices, 4877 (9.8%) CIN1, 11,967 (23.9%) CIN2/3, and 13,792 (27.6%) ICCs. The overall HPV distribution stratified by cervical disease grade and geographical region is shown in Table1. Eastern China contributed the largest number of samples (20,292, 40.6%), followed by Northern China (13,390, 26.8%), Taiwan (6521, 13.0%), Hong Kong (3297, 6.6%), and Western China (2428, 4.9%). Of the 49,997 women, 1496 (3.0%) were non-Han Chinese women including 1431 Uyghur [28] and 65 Mongolian [38].

Overall HPV prevalence and meta-analysis

A total of 30,165 women were HPV-positive. Overall HPV prevalence increased with the degree of cervical disease severity from 24.8% in normal cervices to 87.7% in ICC (P < 0.001) (Table1). The pooled prevalence of overall HPV types among women with ICC was 91.1% (95% CI 88.7–93.1%) and displayed significant heterogeneity, I² = 93.2%,P < 0.0001 (Figure3). Differences in the HPV positivity rate by geographical region varied obviously among pathological categories. In normal cervices, the overall HPV prevalence varied substantially by region, ranging from approximately 10% in Taiwan/Hong Kong to more than 20% in mainland China. For ICC, the overall HPV prevalence was consistent (more than 95%) in Taiwan, Hong Kong, and Macao but ranged from 77.5% to 92.9% and yielded an average of 83.7% (95% CI 82.9–88.2%) in mainland China. The overall HPV prevalence rates in SCC, ADC and unspecified ICC were 86.9% (5840/6721), 71.5% (459/642) and 90.1% (5795/6429), respectively.

After stratified by HPV DNA source, we found that the prevalence rates of overall HPV types in cervical cancer from tissues were consistently significantly higher than that from exfoliated cells in all geographical regions (P < 0.05). With regard to PCR primers, HPV prevalence was higher in samples that were tested using SPF1/GP6+ (99.3%, 95% CI 99.0–99.7%) and/or SP10 (95.1%, 95% CI 93.6–96.7%) primers when compared with MY09/11 (86.1%, 95% CI 84.9–87.3%) and/or PGMY09/11 (83.6%, 95% CI 82.6–84.5%) primers (P < 0.001). Meanwhile, the meta-analysis of the HPV prevalence in women with cervical cancer based on HPV DNA source, different region, publication calendar period, and PCR primers is shown in Table2.

Type-specific HPV prevalence and risk of cervical cancer

Type-specific HPV prevalence in HPV-positive women stratified by cervical disease grade is shown inSupplementary Table 3. HPV16 was the most frequently detected hrHPV type in every grade. HPV16 positivity rate varied little between cervicitis and normal tissues (22.7%, 95% CI 21.5–24.0%) and CIN1 (23.6%, 95% CI 22.0–25.3%) but increased through CIN2 (37.6%, 95% CI 35.5–39.7%) and CIN3 (51.9%, 95% CI 50.1–53.7%) to reach 65.6% (95% CI 64.7–66.4%) in ICC. HPV18 positivity varied very little between cervicitis and normal tissues and CIN3 (5.6–7.9%) but increased to 12.6% (95% CI 12.0–13.2%) in ICC. HPV58 was the second most common type in ICC (12.6%, 95% CI 12.0–13.2%). Notably, HPV52 was the second most common type in cervicitis/CIN1/CIN2 (16.3–22.0%), but the prevalence rate decreased remarkably through CIN3 (15.7%, ranked third) and reduce to 6.5% in ICC (ranked fourth). For the next five most common hrHPV types in ICC, including HPV33, 31, 59, 45, and 39, the positivity rate ranged from 2.1% to 5.5%. For the next five least common hrHPV types in ICC, including HPV51, 56, 68, 35, and 66, the positivity rate ranged from 0.7% to 1.4%. HPV16, 18 and 45 were the only hrHPV types found more frequently in ICC than in cervicitis/normal samples, with the ICC:cervicitis/normal ratios of 2.9, 2.2 and 1.4, respectively. HPV31, 33, 52, and 58 were more frequent in CIN3 in comparison with cervicitis/normal samples, but less common in ICC compared with CIN3 (ICC:CIN3 ratios ranging from 0.6 for HPV58 and down to 0.4 for HPV52). HPV16, 18, 35, 39, 45, and 59 were more frequent in ICC than CIN3, with ICC:CIN3 ratios ranging from 2.3 for HPV18 to 1.1 for HPV35/45.

When stratified by geographical region, we found increased HPV16 positivity with lesion severity to be similar in all regions, with ICC:cervicitis/normal ratios ranging from 2.4 in North China to 4.2 in East China (Figure4 andSupplementary Table 1). The increased HPV18 positivity between normal and ICC cases was observed across all regions, with ICC:cervicitis/normal ratios between 1.8 and 4.1. For HPV58 and HPV52, a relatively elevated in ICC:cervicitis/normal ratio (2.9 and 3.9, respectively) was observed in West China and not apparent in other regions. With regard to HPV DNA source, we found that the prevalence of type-specific HPV in HPV-positive women with cervical cancer based on exfoliated cells were universally higher than that in tissues. HPV58 was the second most common type in exfoliated cells but ranked third in tissues (Table3).

Study quality and publication bias

The quality assessment of all eligible studies was based on the Agency for Healthcare Research and Quality (AHRQ) scale, which is shown inSupplementary Table 2, and the assessment results provided reasonable confidence in the reliability of the meta-analysis. The methodological quality assessment was considered high in thirty-four studies [10–15,17,19–23,25–32,39–45,47–53] and moderate in eleven studies [16,18,24,33–38,46,54]. Five studies had full scores for the representativeness of the cross-sectional study [10,17,20,23,43], but most of them lacked scores because subjects were not consecutive. Other studies lacked scores for incomplete follow-up data. Egger's and Begg's tests were performed to assess the publication bias and proved to be insignificant (bothP = 0.33).

Consent statement

As this study was a systematic review and meta-analysis, we did not include any humans and/or animals. This study was approved by the Institutional Medical Ethics Review Board of Taizhou Hospital in Zhejiang Province.

Search strategy

This meta-analysis was performed in adherence with the guidelines outlined in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [70] (Supplementary Table 5, PRISMA Checklist). We used PubMed/MEDLINE (NCBI), the Cochrane Central Register of Controlled Trials (Wiley), China National Knowledge Infrastructure (CNKI), and the VIP database for Chinese Technical Periodicals (VIP) to search for relevant articles published from the earliest date available to November 15, 2016. The search strategy is described in Appendix S1. Furthermore, we reviewed the references cited in the retrieved articles to search for additional relevant studies.

Eligibility criteria

The participants were females from China who were included in studies of cervical disease associated with HPV. Eligible studies met the following inclusion criteria: 1) using consensus PCR primers, 2) overall and type-specific HPV elicitation, and 3) confirmed by cervical pathological diagnosis. The exclusion criteria were as follows: 1) duplicated data, 2) reviews, letters, conference reports or degree thesis, 3) studies on HIV patients or other sexually transmitted pathogens, 4) studies on gestational or vaccinated women, 5) HPV genotypes not stratified by lesion grade or fewer than 10 cases, and 6) HPV DNA types fewer than 3 high-risk genotypes identified.

Data extraction

Two investigators (SS. Dong and XJ. Feng) independently extracted data from eligible studies. Disagreements were resolved by discussion or involvement of a third investigator (HH. Xu). For each eligible study, the following items were extracted: first author, publication year, region of China, study design, HPV DNA source, PCR primers, pathological diagnosis, sample size, and the number of overall or type-specific HPV-positive samples. For a subset of studies reporting such data, the overall prevalence of multiple infections (which may also include low-risk HPV types) was also extracted. Detail information on all included studies is presented inSupplementary Table 4. Each study was classified according to the following criteria: 1) four macro-geographical regions of mainland China (East, West, South, and North, respectively), Taiwan, Hong Kong, and Macao, 2) HPV DNA source (exfoliated cells, fresh biopsies, fixed biopsies), and 3) histological diagnosis (CIN1, CIN2, CIN3, ICC, squamous cell carcinoma (SCC), or adeno/adenosquamous carcinoma (ADC)).

Quality assessment

Two investigators (LZ. Zheng and A. Lin) independently assessed the quality/risk of bias for each eligible study according the quality assessment forms from the AHRQ (https://www.ncbi.nlm.nih.gov/books/NBK35156/) [71]. A third investigator (K. Wang) resolved the disagreements. In this meta-analysis, the methodological quality of all eligible studies was assessed by AHRQ and included an 11-item yes/no/unclear response option: the “Yes” was scored as “1”, and “No” or “Unclear” was scored “0”. Study quality was assessed as follows: high quality = 8–11; moderate quality = 4–7; low quality = 0–3.

Statistical analysis

We calculated the prevalence of the overall HPV and type-specific HPV (14 high-risk HPV types: HPV 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66 and 68; 2 low-risk HPV types: HPV 6 and 11) among Chinese women with cervical precancerous lesions and ICCs. Type-specific HPV prevalence was defined as the proportion of HPV-positive women in which a particular HPV type was detected, so sample sizes differed among the type-specific analyses. Odds ratios (ORs) and relative 95% confidence intervals (95% CI) were calculated using SPSS version 15.0 (SPSS Inc., Chicago, IL).P values were two-sided, and statistical significance was accepted if theP value was 0.05 or less.

Meta-analysis was conducted using a random effects model. The I² statistic quantified the heterogeneity among the studies, andP < 0.10 was considered indicative of significant heterogeneity. Forest plots were used to display the results graphically. To examine the potential publication bias, we used the Egger's and Begg's tests, whereP < 0.05 was considered to be statistically significant. All analyses were performed using the R statistical software, and the Metaprop command was used as it provides appropriate methods for dealing with proportions with 100% [72].

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