Background: Few population-based studies have investigated premalignant and malignant cervical abnormalities in Beijing.

Methods: A total of 6,385 randomly selected sexually active women were interviewed and examined. Cervical lesion was diagnosed using cytology and histology. High-risk human papillomavirus (HPV) was detected by the second-generation hybrid capture test and typed by gene chip of DNA from paraffin-embedded tissue.

Results: The cervical lesion prevalence diagnosed by histology was 5.8%. High-risk HPV overall prevalence was 9.9%, 50.5% with cervical lesion and 7.4% without cervical lesion. High-risk HPV DNA load increased with increasing degree of lesions. HPV 16 was the most common type (26.5%) among women with cervical lesion, followed by HPV 58 (8.8%), HPV 33 (7.8%), and HPV 56 (5.3%). Women under 50 years of age, married status, pregnancy and delivery status, couple's sexual behavior, contraceptive history, columnar ectopy, and bacterial vaginosis or trichomonas vaginitis history were more risk factors for HPV infection. Factors for cervical lesion were similar, but in comparison with HPV infection, all associations were weakened. Only middle-aged women, husband's sexual partners, oral contraceptives, columnar ectopy, and history of trichomonas vaginitis remained associated with cervical lesion.

Conclusion: In Beijing, the prevalence of cervical lesion and high-risk HPV is higher than estimated in previous reports. HPV 16, 58, and 33 were the most prevalent types. This is relevant for work related to cervical cancer vaccination.

Impact: The study was conducted to understand the current status and epidemiologic characteristics of women with cervical lesion and HPV infection in Beijing. Cancer Epidemiol Biomarkers Prev; 19(10); 2655–64. ©2010 AACR.

Cervical cancer is one of the leading cancers among women worldwide (1). Developed countries have experienced important reductions in the incidence of and mortality associated with cervical cancer with effective and extensive screening with Pap smears (2). However, it remains the most common cancer among women in many developing countries, where 80% of instances are diagnosed only at advanced stages (3-5).

Cervical intraepithelial neoplasia (CIN) reflects a continuous and progressive process of cervical cancer, and is thus considered as a cervical precancerous lesion (6). An important factor is the status of high-risk human papillomavirus (HPV) infection that affects the development of CIN (7-9). With the virus infection, high-grade squamous intraepithelial lesions can develop and progress to cancer over a period of 8 to 12 years (10, 11). This relatively long and reversible development process means it is possible to carry out an intervention and treatment of the precancerous cervical lesion to effectively prevent invasive cervical cancer.

The population of the People's Republic of China is 1.3 billion. Cervical cancer incidence in China is high, with about 132,300 new cases each year, yielding a rate of above 27 per 100,000 women (12). However, data from China surveys show heterogeneous patterns of different areas, and provide widely varying estimates of prevalence. Few population-based studies have investigated the prevalence of cervical abnormalities and HPV (12, 13). Beijing is the capital city of China with a population of 16.9 million. The population comprises 56 ethnic groups in the country. The floating or migrant-worker population in Beijing is estimated to be more than 4 million. This study aimed to understand the current status and characteristics of the women with cervical lesion and HPV in Beijing.

Study population

We carried out the present survey from August 2006 to December 2009 in Beijing, which has 18 districts (4 urban, 4 suburban, and 10 outer suburbs). On the basis of data from the 2005 census published by the National Bureau of Statistics of China, our representative sample of the adult female population of Beijing was stratified by age and regional distribution using a multistage cluster sampling method. First, according to the proportion of each district's population, five to eight communities were randomly selected from each district. Second, one neighborhood was randomly chosen from each community. Finally, from the lists provided by local neighborhoods, a final random sample of 50 women per neighborhood was derived. After randomized samples of the population were selected, door-to-door visits were made to recruit these women to their local maternal and child health hospitals. If the recruited number was bigger than the sample required, another random sampling was done on this basis. If the recruited number was smaller than the sample required, the number from each neighborhood was further increased through random sampling. On the basis of the age ratios of the 2005 census, the study strove to enroll approximately 10 women age 25 to 34 years, 14 women age 35 to 44 years, 13 women age 45 to 54 years, and 13 migrant-worker women age 25 to 54 years from each neighborhood.

According to the inclusion criteria, invited participants were those women who (a) were 25 to 54 years old in reproductive age, and were physically and mentally able to undergo an interview and a pelvic examination; (b) were living in Beijing for more than half a year, including both those with household registration in Beijing and those without (migrant-worker population); (c) had no history of cervical surgery; (d) were not pregnant; and (d) had no history of pelvic radiation therapy. In the end, a total of 6,385 individuals from 25 to 54 years of age were randomly recruited from 137 communities. Written consent was obtained from all participants in accordance with the regulations of the Beijing Obstetric and Gynecology Hospital and various districts' maternal and child health hospitals, which approved the study.

Interviews were administered by two to four experienced gynecologists. Questionnaires contained a total of 197 questions about sociodemographic information and obstetric and gynecologic history, which included profile information, menstruation and marital status, as well as pregnancy, sexual behavior, and contraceptive history. Past medical history, family history of tumors, and history of gynecologic examinations were also included. Participants then had a gynecologic examination, and a cervical sample was taken.

Cytology and histology diagnosis

During the gynecologic examination, samples of exfoliated cervical cells for liquid-based thin-layer cytology (Thinprep CytycCorp.) were collected with a brush by placing the tip of the brush at squamo-columnar junction and rotating it five times in one direction. The contents were sent to the Beijing Obstetrics and Gynecology Hospital for analysis. All smears were reported by two cytologists separately, and the abnormal/indeterminate ones were reviewed by a senior cytologist for final diagnosis. Results were classified according to the Bethesda System. All abnormal smears and 10% of normal smears chosen at random were sent for review by an experienced cytopathologist.

Study subjects who showed a positive cytology result, atypical squamous cells of undetermined significance (ASC-US) or more severe, were referred to the study colposcopist. After comprehensive observation to the transformation zone, punch biopsies were taken from any suspicious region. The median period between enrollment visit and colposcopy visit was 2.6 weeks (range, 2-6 weeks). The results of pathology were classified into negative (normal or inflammation), CINI, and CIN II+ (including CIN II, CIN III, and early-stage squamous cervical carcinoma). Histologic specimens were reviewed by two independent expert pathologists. The results of histology used in the analysis were based on joint expert efforts. In addition, a random sample of 1 in 50 women in the negative cytologic group was referred for colposcopy as a control group. All confirmed or highly suspicious high-grade or invasive cervical lesions were treated at the collaborating hospitals with loop excision, cold knife conization, hysterectomy, or radiotherapy, according to the protocols.

HPV detection and typing

Additional cells were obtained with a dacron swab inside the endocervical canal and from the entire circumference of the ectocervix for HPV testing. The second-generation hybrid capture (HC-II) test (Digen Corporation) using the high-risk probe cocktail was done for all subjects in the study. Quantitative detection of HPV DNA was evaluated at the molecular level by detections of gene hybridization-chemiluminescence-signal amplification technology. The high-risk probe cocktail, which detects HPV types 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, and 68 was used based on the manufacturer's instructions. A positive result referred to a patient who was positive for ≥1 of the 13 high-risk HPV types included. Samples were considered positive if they attained or exceeded the Food and Drug Administration–approved threshold of HPV DNA of 1.0 pg/mL, which corresponded to 1.0 relative light unit. Infection with low-risk HPV types was not evaluated.

DNA was extracted from the paraffin-embedded tissue of cervical biopsies and amplified by PCR using HPV DNA primers. The overall presence of HPV DNA positivity was determined by PCR using 5′-biotinylated MY09/11 consensus primers, as described previously (14). The PCR products were then reversely hybridized with gene chip technology. The mixed primer MY11/GP6+ was labeled with biotin to do PCR, then the product was hybridized with the gene chip that blotted 23 kinds of specific oligonucleotide probes. Finally, the streptavidin-conjugated alkaline phosphatase and NBT/BCIP (5-bromo-4-chloro-3-indoly-phosphate/nitroblu tetrazolium) was used to work with the chip and read the HPV type of each tissue (15, 16). The presence of 23 subtypes, including HPV 16, 18, 31, 33, 35, 39, 45, 51, 52, 53, 56, 58, 59, 66, 68, 73, 83, and MM4, 6, 11, 42, 43 and 44, was determined.

Statistical analysis

Statistical analysis was done using SPSS version 13.0 software. Descriptive analysis was made of the demographic data. The various characteristics of the cervical lesion prevalence, positive with high-risk HPV, were determined using the prevalence rate. Odds ratio (OR) with 95% confidence interval (95% CI) was used to estimate relative risk using unconditional, logistic regression, adjusted for age groups (25-29, 30-34, 35-39, 40-44, 45-49, and 50-54 years). Multivariate logistic regression analysis was carried out to estimate the main determinant risk factors for cervical lesion in the population. The statistical significance of trends for OR (P for trend) was assessed by treating ordinal variables as continuous.

Characteristics of study subjects

A total of 6,385 women in reproductive age from 25 to 54 years old were recruited. With 46 cases lost, the final effective sample size was 6,339. The average age was 39.6 ± 8.1 years. In terms of household registration, 76.6% had theirs in Beijing. The average age at first sexual intercourse was 24.0 ± 2.3; 96.9% reported having only one lifetime sexual partner, 2.9% having two sexual partners, and only 0.2% having more than two sexual partners. Of the 6,339 women, 6,034 (95.2%) had a delivery history. A total of 5,240 (82.7%) women reported having used contraception; 2,362 had used intrauterine contraceptive devices (IUD), 2,366 had used condoms, 206 had used oral contraceptives, 282 had undergone a sterilization operation, 10 had male partners who had undergone sterilization operations, and 14 reported other methods of contraception. Only 0.4% of the women (16 of 6,339) had gone through HPV detection before. A total of 1,219 of the 6,339 (19.2%) women had experienced cervical cytology detection.

Cytology results

All of the study subjects underwent cervical cytology tests. The results below ASC-US (including normal and inflammatory cells) were defined as negative in cytology; the results of ASC-US or more severe, including atypical squamous cells cannot exclude HSIL (ASC-H), low-grade squamous intraepithelial lesion (LSIL), high-grade squamous intraepithelial lesion (HSIL), squamous cell carcinoma (SCC), and atypical glandular cells (AGC), were defined as positive in cytology. Among the women in our study, 9.6% (607 of 6,339) were positive. According to categories of positive cytology, ASC-US accounted for 6.45% (409 of 6,339), ASC-H for 0.17% (11 of 6,339), LSIL for 1.56% (99 of 6,339), HSIL for 0.50% (32 of 6,339), SCC for 0.03% (2 of 6,339), and AGC for 0.85% (54 of 6,339).

Cervical lesion prevalence

Women with pathology results CIN I and CIN II+ were collectively referred to as positive pathology and diagnosed as having cervical lesions. A total of 607 positive cytology cases underwent cervical biopsy and were pathologically diagnosed with 374 positive pathology cases. One hundred fifteen randomly sampled negative cytology women had pathologic diagnosis as control, and no cases suffered cervical lesion. The prevalence was 5.9% for cervical lesion, 4.7% for CIN I, and 1.2% for CIN II+. Adjusted for age, the estimated overall prevalence of cervical lesion in the population of Beijing was 5.8%. Table 1 presents the cervical lesion distribution of the subjects, the overall prevalence, and age-adjusted OR and 95% CI of each cytologic category.

Table 1.

Cervical lesion distribution comparing cytology and histology (OR and corresponding 95% CI; n = 6,339)

Cervical cytologyTotal no.Cervical lesion
Negative (%)CIN ICIN II+
No. (%)OR* (95%CI)No. (%)OR* (95%CI)
ASC-US 409 172 (42.0) 208 (50.9) 29 (7.1) 
ASC-H 11 5 (45.4) 4 (36.4) 0.55 (0.16-1.91) 2 (18.2) 2.91 (0.60-13.17) 
AGC 54 29 (53.7) 21 (38.9) 0.61 (0.34-1.10) 4 (7.4) 1.05 (0.35-3.11) 
LSIL 99 21 (21.2) 60 (60.6) 1.45 (0.95-2.33) 18 (18.2) 2.91 (1.54-5.38) 
HSIL 32 6 (18.7) 2 (6.3) 0.06 (0.02-0.27) 24 (75.0) 39.31 (16.23-74.00) 
SCC 0 (0) 0 (0) — 2 (100) — 
Cervical cytologyTotal no.Cervical lesion
Negative (%)CIN ICIN II+
No. (%)OR* (95%CI)No. (%)OR* (95%CI)
ASC-US 409 172 (42.0) 208 (50.9) 29 (7.1) 
ASC-H 11 5 (45.4) 4 (36.4) 0.55 (0.16-1.91) 2 (18.2) 2.91 (0.60-13.17) 
AGC 54 29 (53.7) 21 (38.9) 0.61 (0.34-1.10) 4 (7.4) 1.05 (0.35-3.11) 
LSIL 99 21 (21.2) 60 (60.6) 1.45 (0.95-2.33) 18 (18.2) 2.91 (1.54-5.38) 
HSIL 32 6 (18.7) 2 (6.3) 0.06 (0.02-0.27) 24 (75.0) 39.31 (16.23-74.00) 
SCC 0 (0) 0 (0) — 2 (100) — 

*Adjusted for age.

Reference category.

High-risk HPV and HPV subtype

Of the cervical cell samples provided by 6,339 women, 154 cases' specimens for HC-II test were not eligible, leaving 6,185 valid high-risk HPV results (with 615 positive cases). High-risk HPV was 41.2% in the cytology-positive group, 6.6% in the cytology-negative group, 50.5% in the cervical lesion group, and 7.4% in the no-lesion group. Adjusted for age, the estimated overall prevalence of high-risk HPV was 9.9% among the population of Beijing.

Higher-grade cervical lesions were associated with greater high-risk HPV infection rates and a higher HPV DNA load. The high-risk HPV infection rate of the CIN I group was 39.9%, whereas the rate of the CIN II+ group was 88.6%. HPV DNA load above 100 pg/mL was 62.0% in the CIN II+ group and 21.2% in the CIN I group (Table 2), with a significant difference (χ2 = 27.507, P < 0.01).

Table 2.

Detection of cervical lesion according to high-risk HPV infection and DNA load (OR and corresponding 95% CI; n = 6,185)

Total no.CIN ICIN II+
No. (%)OR* (95% CI)No. (%)OR* (95% CI)
High-risk HPV infection 
    Negative 5,570 176 (3.2) 9 (0.2) 
    Positive 615 117 (19.0) 8.36 (6.72-10.78) 70 (11.4) 97.86 (69.07-197.26) 
Load of high-risk HPV DNA 
    0-1 5,570 176 (3.2) 9 (0.2) 
    1-100 420 55 (13.0) 4.89 (3.65-6.75) 21 (5.0) 36.53 (22.34-80.36) 
    101-500 109 26 (23.9) 12.63 (8.65-20.42) 20 (18.3) 189.95 (134.53-433.43) 
    >500 86 36 (41.9) 52.45 (37.78-91.70) 29 (33.8) 826.27 (631.22-1956.42) 
Total no.CIN ICIN II+
No. (%)OR* (95% CI)No. (%)OR* (95% CI)
High-risk HPV infection 
    Negative 5,570 176 (3.2) 9 (0.2) 
    Positive 615 117 (19.0) 8.36 (6.72-10.78) 70 (11.4) 97.86 (69.07-197.26) 
Load of high-risk HPV DNA 
    0-1 5,570 176 (3.2) 9 (0.2) 
    1-100 420 55 (13.0) 4.89 (3.65-6.75) 21 (5.0) 36.53 (22.34-80.36) 
    101-500 109 26 (23.9) 12.63 (8.65-20.42) 20 (18.3) 189.95 (134.53-433.43) 
    >500 86 36 (41.9) 52.45 (37.78-91.70) 29 (33.8) 826.27 (631.22-1956.42) 

*Adjusted for age.

Reference category.

HPV was typed by gene chip of DNA, which was extracted from the paraffin-embedded tissue of 607 cytology-positive cases (Table 3). Among the women with cervical lesions, the prevalence of any subtype of HPV was 62.6% (50.5% for high-risk type and 10.2% for low-risk type). Among the women with no cervical lesion, the prevalence of any subtype of HPV was 36.1% (26.2% for high-risk type and 9.9% for low-risk type). A total of 193 women had single-type and 125 had multiple-type infections. In all, 21 individual HPV types were identified. The most commonly found high-risk HPV types in women with cervical lesions were HPV 16 (26.5%), HPV 58(8.8%), HPV 33 (7.8%), and HPV 56 (5.3%).

Table 3.

Prevalence of various HPV types in cytology-positive cases (n = 607)

HPV type*No cervical lesion (n = 233)CIN I (n = 295)CIN II+ (n = 79)
SingleMultipleTotal (%)SingleMultipleTotal (%)SingleMultipleTotal (%)
Negative   149 (63.9)   138 (46.8)   2 (2.54) 
Positive 
    Any 57 27 84 (36.1) 93 64 157 (53.2) 43 34 77 (97.5) 
    High risk 43 18 61 (26.2) 72 47 119 (40.3) 39 31 70 (88.6) 
    Low risk 14 23 (9.9) 21 17 38 (12.9) 7 (8.9) 
    High risk 
        16 17 10 27 (11.6) 28 34 62 (20.0) 15 22 37 (46.8) 
        58 14 (6.0) 11 20 (6.8) 13 (16.5) 
        33 10 (4.3) 13 18 (6.1) 11 (13.9) 
        56 8 (3.4) 13 (4.4) 7 (8.9) 
        31 4 (1.7) 10 (3.4) 8 (10.1) 
        35 6 (2.6) 9 (3.1) 7 (8.9) 
        18 5 (2.1) 10 (3.4) 5 (6.3) 
        59 2 (0.9) 7 (2.4) 3 (3.8) 
        68 3 (1.3) 5 (1.7) 3 (3.8) 
        51 2 (0.9) 4 (1.4) 3 (3.8) 
        39 1 (0.4) 4 (1.4) 3 (3.8) 
        73 1 (0.4) 2 (0.7) 2 (2.5) 
        45 1 (0.3) 
        52 1 (0.4) 
    Low risk 
        43 8 (3.4) 10 16 (5.4) 2 (2.5) 
        66 4 (1.7) 12 (4.1) 3 (3.8) 
        53 2 (0.9) 6 (2.0) 1 (1.3) 
        42 3 (1.3) 5 (1.7) 
        6 2 (0.9) 1 (0.3) 1 (1.3) 
        11 2 (0.9) 2 (0.7) 
        83 1 (0.4) 
HPV type*No cervical lesion (n = 233)CIN I (n = 295)CIN II+ (n = 79)
SingleMultipleTotal (%)SingleMultipleTotal (%)SingleMultipleTotal (%)
Negative   149 (63.9)   138 (46.8)   2 (2.54) 
Positive 
    Any 57 27 84 (36.1) 93 64 157 (53.2) 43 34 77 (97.5) 
    High risk 43 18 61 (26.2) 72 47 119 (40.3) 39 31 70 (88.6) 
    Low risk 14 23 (9.9) 21 17 38 (12.9) 7 (8.9) 
    High risk 
        16 17 10 27 (11.6) 28 34 62 (20.0) 15 22 37 (46.8) 
        58 14 (6.0) 11 20 (6.8) 13 (16.5) 
        33 10 (4.3) 13 18 (6.1) 11 (13.9) 
        56 8 (3.4) 13 (4.4) 7 (8.9) 
        31 4 (1.7) 10 (3.4) 8 (10.1) 
        35 6 (2.6) 9 (3.1) 7 (8.9) 
        18 5 (2.1) 10 (3.4) 5 (6.3) 
        59 2 (0.9) 7 (2.4) 3 (3.8) 
        68 3 (1.3) 5 (1.7) 3 (3.8) 
        51 2 (0.9) 4 (1.4) 3 (3.8) 
        39 1 (0.4) 4 (1.4) 3 (3.8) 
        73 1 (0.4) 2 (0.7) 2 (2.5) 
        45 1 (0.3) 
        52 1 (0.4) 
    Low risk 
        43 8 (3.4) 10 16 (5.4) 2 (2.5) 
        66 4 (1.7) 12 (4.1) 3 (3.8) 
        53 2 (0.9) 6 (2.0) 1 (1.3) 
        42 3 (1.3) 5 (1.7) 
        6 2 (0.9) 1 (0.3) 1 (1.3) 
        11 2 (0.9) 2 (0.7) 
        83 1 (0.4) 

NOTE: The table includes all cytology-positive cases, divided into two groups according histology diagnosis.

*The same woman can be counted more than once for multiple infection.

Age-specific cervical lesions and high-risk HPV prevalence

Figure 1 shows the estimated age-specific prevalence and the corresponding 95% CI of cervical lesions and high-risk HPV in Beijing. A total of 6,339 women were grouped in six age groups: 25-29, 30-34, 35-39, 40-44, 45-49, and 50-54 years. CIN I was highest in women younger than age 35, with a median age of 34 years, among whom it reached 5.7%. It was lowest at 3.3% among women 45 to 49 years of age, and then increased again to 4.4% in women 50 to 54 years of age. The median age of women with CIN II+ was 36 years. An initial peak of 2.2% at age 30 to 34 years was observed, and it decreased consistently with increase in age. However, among women 40 to 44 years of age, the rate was 1.4% higher than the rate among those 35 to 39 years of age. The difference between the prevalence of CIN II+ in different age groups of women was marginally statistically significant (P < 0.05). The age-specific prevalence of high-risk HPV increased from 10.0% in women age 25 to 29 years then peaked at 11.0% in women age 30 to 34 years, and then decreased to 9.9% in women 35 to 39 years of age, and to 10.2% in women 40 to 44 years of age. The prevalence decreased progressively to 9.2% and 7.5% in women age 45 to 49 and 50 to 54 years, respectively.

Figure 1.

Age-specific prevalence of cervical lesion and high-risk HPV in Beijing (with corresponding 95% CI).

Figure 1.

Age-specific prevalence of cervical lesion and high-risk HPV in Beijing (with corresponding 95% CI).

Close modal

The prevalence of cervical lesions in different age groups among high-risk HPV-positive populations was significantly higher than that in high-risk HPV-negative populations. In the positive populations, the cervical lesion prevalence in 30- to 34-year-old women was the highest (39.5%). It decreased as age increased until the lowest point for women at 45 to 49 years of age (21.0%), and then it went slightly higher at 50 to 54 years of age (27.0%).

Risk factors of high-risk HPV infection and cervical lesion

Age-adjusted associations between various factors and the detection of high-risk HPV and cervical lesions are shown in Table 4.

Table 4.

Associations between various factors and detection of high-risk HPV and cervical lesion (OR and corresponding 95% CI; n = 6,339)

Total no.High riskCervical lesion
No. (%)OR* (95% CI)No. (%)OR* (95% CI)
Age (years) 
    25-29 824 82 (9.9) 1.36 (0.97-1.93) 37 (4.5) 0.85 (0.55-1.34) 
    30-34 1,132 124 (11.0) 1.52 (1.11-2.09) 83 (7.3) 1.44 (0.99-2.09) 
    35-39 1,203 119 (9.9) 1.36 (0.99-1.87) 81 (6.7) 1.31 (0.90-1.92) 
    40-44 1,250 127 (10.2) 1.40 (1.02-1.92) 82 (6.6) 1.28 (0.88-1.86) 
    45-49 1,086 100 (9.2) 1.26 (0.90-1.75) 47 (4.3) 0.82 (0.54-1.25) 
    50-54 844 63 (7.5) 44 (5.2) 
Educational level 
    High school and below 2,649 220 (8.3) 142 (5.4) 
    University and above 3,690 395 (10.7) 1.32 (1.11-1.57) 232 (6.3) 1.18 (0.96-1.47) 
Monthly family income per capita 
    ≤CNY 2,000 Yuan 1,194 78 (6.5) 72 (6.0) 
    >CNY 2,000 Yuan  5,145 537 (10.4) 1.67 (1.30-2.13) 302 (5.9) 0.97 (0.75-1.27) 
Smoking 
    Never 6,110 591 (9.7) 359 (5.9) 
    Ever 229 24 (10.5) 0.79 (0.54-1.18) 15 (6.6) 1.02 (0.61-1.54) 
Drinking 
    Never 5,063 469 (9.3) 283 (5.5) 
    Ever 1,276 146 (11.4) 0.93 (0.66-1.17) 91 (7.1) 0.96 (0.89-1.20) 
Married status 
    Married 6,142 585 (9.5) 358 
    Unmarried§ 197 30 (15.2) 1.71 (1.15-2.54) 16 1.43 (0.85-2.40) 
Lifetime sexual partners 
    1 6,144 593 (9.7) 364 (6.0) 
    >1 195 22 (11.3) 1.19 (0. 76-1.87) 10 (5.1) 0.86 (0.45-1.63) 
Husband's sex partners 
    1 6,014 563 (9.4) 342 (5.7) 
    2 263 37 (14.1) 1.59 (1.11-2.27) 22 (8.4) 1.51 (0.97-2.37) 
    ≥3 62 15 (24.2) 3.09 (1.76-5.56) 10 (16.1) 3.19 (1.66-6.33) 
Age at first intercourse 
    ≤20 444 60 (13.5) 2.15 (1.35-3.44) 37 1.54 (0.90-2.64) 
    21-27 5,482 527 (9.6) 1.46 (0.99-2.17) 314 1.03 (0.67-1.59) 
    ≥28 413 28 (6.8) 23 
Pregnant 
    Never 156 23 (14.7) 1.63 (1.04-2.56) 13 (8.3) 1.47 (0.83-2.61) 
    Ever 6,183 592 (9.6) 361 (5.8) 
Age at first pregnancy 
    ≤24 2,936 290 (9.9) 4.05 (1.27-4.11) 176 (6.0) 1.32 (0.73-2.41) 
    25-29 2,986 290 (9.7) 2.23 (1.25-3.97) 173 (5.8) 1.28 (0.70-2.32) 
    ≥30 261 12 (4.6) 12 (4.6) 
Delivery 
    Never 305 51 (16.7) 1.95 (1.43-2.66) 23 (7.5) 1.32 (0.85-2.05) 
    Ever 6,034 564 (9.3) 351 (5.8) 
Oral contraceptives 
    Never  6,133 601 355 (5.8) 
    Ever 206 14 0.67 (0.39-1.16) 19 (9.2) 1.63 (1.02-2.56) 
Condom use 
    Never 3,973 395 (9.9) 248 (6.2) 
    Ever 2,366 220 (9.3) 0.93 (0.78-1.10) 126 (5.3) 0.84 (0.68-1.05) 
IUD contraceptives 
    Never 3,977 378 (9.5) 231 (5.8) 
    Ever 2,362 237 (10.0) 0.58 (0.48-0.97) 143 (6.1) 0.95 (0.81-1.23) 
Columnar ectopy 
    No 4,941 417 (8.4) 247 (5.0) 
    Yes  1,398 198 (14.2) 1.79 (1.49-2.15) 127 (9.1) 1.90 (1.52-2.37) 
Bacterial vaginosis 
    Never 5,786 511 (8.8) 329 (5.7) 
    Ever 553 104 (18.8) 2.39 (1.90-3.01) 45 (8.1) 1.47 (1.06-2.03) 
Trichomonas vaginitis 
    Never 5,792 543 (9.4) 323 (5.6) 
    Ever 547 71 (13.0) 1.44 (1.11-1.88) 51 (9.3) 1.74 (1.28-2.37) 
Total no.High riskCervical lesion
No. (%)OR* (95% CI)No. (%)OR* (95% CI)
Age (years) 
    25-29 824 82 (9.9) 1.36 (0.97-1.93) 37 (4.5) 0.85 (0.55-1.34) 
    30-34 1,132 124 (11.0) 1.52 (1.11-2.09) 83 (7.3) 1.44 (0.99-2.09) 
    35-39 1,203 119 (9.9) 1.36 (0.99-1.87) 81 (6.7) 1.31 (0.90-1.92) 
    40-44 1,250 127 (10.2) 1.40 (1.02-1.92) 82 (6.6) 1.28 (0.88-1.86) 
    45-49 1,086 100 (9.2) 1.26 (0.90-1.75) 47 (4.3) 0.82 (0.54-1.25) 
    50-54 844 63 (7.5) 44 (5.2) 
Educational level 
    High school and below 2,649 220 (8.3) 142 (5.4) 
    University and above 3,690 395 (10.7) 1.32 (1.11-1.57) 232 (6.3) 1.18 (0.96-1.47) 
Monthly family income per capita 
    ≤CNY 2,000 Yuan 1,194 78 (6.5) 72 (6.0) 
    >CNY 2,000 Yuan  5,145 537 (10.4) 1.67 (1.30-2.13) 302 (5.9) 0.97 (0.75-1.27) 
Smoking 
    Never 6,110 591 (9.7) 359 (5.9) 
    Ever 229 24 (10.5) 0.79 (0.54-1.18) 15 (6.6) 1.02 (0.61-1.54) 
Drinking 
    Never 5,063 469 (9.3) 283 (5.5) 
    Ever 1,276 146 (11.4) 0.93 (0.66-1.17) 91 (7.1) 0.96 (0.89-1.20) 
Married status 
    Married 6,142 585 (9.5) 358 
    Unmarried§ 197 30 (15.2) 1.71 (1.15-2.54) 16 1.43 (0.85-2.40) 
Lifetime sexual partners 
    1 6,144 593 (9.7) 364 (6.0) 
    >1 195 22 (11.3) 1.19 (0. 76-1.87) 10 (5.1) 0.86 (0.45-1.63) 
Husband's sex partners 
    1 6,014 563 (9.4) 342 (5.7) 
    2 263 37 (14.1) 1.59 (1.11-2.27) 22 (8.4) 1.51 (0.97-2.37) 
    ≥3 62 15 (24.2) 3.09 (1.76-5.56) 10 (16.1) 3.19 (1.66-6.33) 
Age at first intercourse 
    ≤20 444 60 (13.5) 2.15 (1.35-3.44) 37 1.54 (0.90-2.64) 
    21-27 5,482 527 (9.6) 1.46 (0.99-2.17) 314 1.03 (0.67-1.59) 
    ≥28 413 28 (6.8) 23 
Pregnant 
    Never 156 23 (14.7) 1.63 (1.04-2.56) 13 (8.3) 1.47 (0.83-2.61) 
    Ever 6,183 592 (9.6) 361 (5.8) 
Age at first pregnancy 
    ≤24 2,936 290 (9.9) 4.05 (1.27-4.11) 176 (6.0) 1.32 (0.73-2.41) 
    25-29 2,986 290 (9.7) 2.23 (1.25-3.97) 173 (5.8) 1.28 (0.70-2.32) 
    ≥30 261 12 (4.6) 12 (4.6) 
Delivery 
    Never 305 51 (16.7) 1.95 (1.43-2.66) 23 (7.5) 1.32 (0.85-2.05) 
    Ever 6,034 564 (9.3) 351 (5.8) 
Oral contraceptives 
    Never  6,133 601 355 (5.8) 
    Ever 206 14 0.67 (0.39-1.16) 19 (9.2) 1.63 (1.02-2.56) 
Condom use 
    Never 3,973 395 (9.9) 248 (6.2) 
    Ever 2,366 220 (9.3) 0.93 (0.78-1.10) 126 (5.3) 0.84 (0.68-1.05) 
IUD contraceptives 
    Never 3,977 378 (9.5) 231 (5.8) 
    Ever 2,362 237 (10.0) 0.58 (0.48-0.97) 143 (6.1) 0.95 (0.81-1.23) 
Columnar ectopy 
    No 4,941 417 (8.4) 247 (5.0) 
    Yes  1,398 198 (14.2) 1.79 (1.49-2.15) 127 (9.1) 1.90 (1.52-2.37) 
Bacterial vaginosis 
    Never 5,786 511 (8.8) 329 (5.7) 
    Ever 553 104 (18.8) 2.39 (1.90-3.01) 45 (8.1) 1.47 (1.06-2.03) 
Trichomonas vaginitis 
    Never 5,792 543 (9.4) 323 (5.6) 
    Ever 547 71 (13.0) 1.44 (1.11-1.88) 51 (9.3) 1.74 (1.28-2.37) 

*Adjusted for age.

Reference category.

Adjusted for sexual factors (marital status, lifetime sexual partners, husband's sexual partners).

§Unmarried includes separated, divorced, and widowed.

Differences between age groups were statistically significant for high-risk HPV. Women under 50 years of age were more at risk of infection (OR for <50 versus ≥50 years, 1.38). Women who drank alcoholic beverages one to two times per week or smoked had an increased risk of detection of HPV (OR, 1.27 and 1.09, respectively) compared with nondrinkers and nonsmokers. Women with high education levels and high income levels were more likely to be infected with HPV (OR, 1.32 and 1.67, respectively). Single women (including unmarried, divorced, and widowed) were more likely to be infected with HPV (OR, 1.71) compared with married women. The prevalence of HPV increased with a woman's lifetime number of sexual partners (OR for two or more partners, 1.19). Furthermore, HPV positivity was significantly associated with the number of the husband's sexual partners (OR for two partners versus one, 1.59; OR for more than three partners versus one, 3.09). The age of first sexual intercourse was inversely associated with HPV positivity (OR for ≤20 versus ≥28 years, 2.15; OR for 21-27 versus ≥28 years, 1.46). The detection of HPV was lower among ever-pregnant than never-pregnant women, and lower among parous than nulliparous women (OR for never pregnant versus ever, 1.63; OR for never delivery versus ever, 1.95). Age at first pregnancy was related to HPV infection (OR for ≤24 versus ≥30 years, 4.05; OR for 25-29 versus ≥30 years, 2.23), but induced or spontaneous abortion number and delivery number were unrelated. Condom use had some protective effect on HPV infection (OR, 0.93), whereas IUD use had increased risk (OR, 1.06). Oral contraceptive use was not associated with HPV infection (OR, 0.67). Cervical or vaginal status also related to HPV infection; columnar ectopy, and history of bacterial vaginosis or trichomonas vaginitis increased the risk (OR, 1.79, 2.39, and 1.44, respectively). No significant association was found between HPV positivity and household registration, ethnic group, occupation, or menstruation status.

To adjust for any confounding effects, the effects of lifestyle (alcohol drinking, smoking, age at first sex, parity, contraception) on HPV infection were adjusted for sexual factors (marital status, lifetime sexual partners, husband's sexual partners). By each sexual factor, the same lifestyle's cases belonged to different groups. Stratification analysis was used to determine the relationship. If the sexual factor was related to the lifestyle, it was included in the multilevel regression model to estimate the OR of HPV infection and the corresponding 95% CI using the MLwiN software. Adjusted for marital status and lifetime sexual partners, alcohol drinking (OR, 0.93; 95% CI, 0.66-1.17) and smoking (OR, 0.79; 95% CI, 0.54-1.18) had no association. Adjusted for lifetime sexual partners and husband's sexual partners, IUD contraceptives (OR, 0.58; 95% CI, 0.48-0.97) had no association.

The risk factors for cervical lesion, similar to high-risk HPV infection, included high education levels (OR, 1.18), single women (OR, 1.43), the number of husband's sexual partners (OR for two partners versus one, 1.51; OR for more than three partners versus one, 3.19), age at first intercourse (OR for ≤20 versus ≥28 years, 1.54; OR for 21-27 versus ≥28 years, 1.03), pregnancy and delivery status (OR for never pregnant versus ever, 1.47; OR for never delivery versus ever, 1.32), age at first pregnancy (OR for ≤24 versus ≥30 years, 1.32; OR for 25-29 versus ≥30 years, 1.28), no condom use (OR for use versus no use, 0.93), columnar ectopy (OR, 1.90), bacterial vaginosis history (OR, 1.47), and trichomonas vaginitis history (OR, 1.74). Unlike high-risk HPV infection, middle-aged women were more likely to suffer from cervical lesion (OR for 30-44 versus ≥50 years, 1.34; OR for 30-44 versus <30 years, 1.57); oral contraceptive use was associated with cervical lesion (OR, 1.63); and high income and the number of a woman's lifetime sexual partners were not associated with cervical lesion.

When the variables that were related to cervical lesion were entered in the same multiple logistic models, all associations weakened, most notably those with lifestyle and with a woman's sexual habits. However, high-risk HPV infection (OR, 12.54; 95% CI, 9.95-15.81), middle-aged women (OR, 1.53; 95% CI, 1.17-2.49), the number of husband's sexual partners (OR, 2.07; 95% CI, 1.12-3.85), oral contraceptive use (OR, 1.40; 95% CI, 1.09-1.81), columnar ectopy (OR, 1.39; 95% CI, 1.04-1.63), and trichomonas vaginitis (OR, 1.48; 95% CI, 1.05-2.10) remained significantly associated with cervical lesion.

National-level cancer mortality data are sparse in China. Both the incidence rate of cervical cancer in different geographic areas and the age-specific curves of the incidence rate seem to vary (13, 17-19). Beijing has a complex multilevel population structure. Thus, the investigation was a representative epidemiologic survey. The guideline by the Chinese government in 2004 recommended that the initial screening time should be between the ages of 20 and 30 years in economically developed areas, between 35 and 40 years in economically underdeveloped areas, and for high-risk groups appropriately early enough to exanimate. We considered economic and demographic characteristics overall and determined sexually active women 25 to 54 years of age among the healthy women in Beijing as the study subjects.

This is the first population-based study to investigate the prevalence rate of cervical lesion and high-risk HPV infection in a large sample in Beijing or even in China. With the support of the government, Chinese women have attached greater importance to cervical cancer. More than 99% participation in all components of the study was attained, assuring the representativeness of the study population and allowing for population-wide estimates. In Beijing, the age-adjusted prevalence rate of cervical lesions is 5.8%, which is higher than the known cervical lesion prevalence in developed countries (2, 20, 21). More severe cervical cytology abnormality was associated with higher prevalence of cervical lesions. The increasingly severe diagnostic categories were strongly associated with increasing overall detection of high-risk HPV in the lesion, and increasing OR. The HPV DNA load <100 pg/mL was considered low load whereas ≥100 pg/mL was considered high load; the HPV DNA load had obvious relevance with cervical lesion in accordance with other results (22). High viral loads are likely to increase the risk for events initiating dysplasia such as viral integration (23). Our results indicate that increasing the viral load of high-risk HPV in cervical smears increases the risk of cervical lesions, which is similar to what was previously described for carcinoma in situ (22).

Using the HC-II assay, we found that among Beijing women the level of HPV infection (9.9%) is lower than that found in China (24). Twenty-one HPV types were found in cytology-positive women; most of the HPV types were associated with invasive cervical cancer worldwide (25). In our study, the most prominent HPV type in both single and multiple infections was HPV 16 in women with or without cervical lesion, followed by HPV 58 and HPV 33. Surveys have reported relatively high HPV 58 and HPV 33 prevalence in Asia (25). HPV 16, 18, 58, 33, 52, and 45 were more common in Asia than in other areas (26). The predominance of HPV 58 and HPV 33 in Beijing is in accordance with the results of certain surveys in other regions of China (17, 18, 27). However, HPV 18 is not the main infection type.

The age pattern of HPV prevalence also differs somewhat from one country to another. The predominant pattern features an early peak soon after the start of sexual intercourse (28), followed by lower levels of HPV positivity in middle age (28, 29). In studies from sub-Saharan Africa (30), the prevalence of HPV declined with age. In our survey, high-risk HPV prevalence was highest in women age 30 to 34 years and declined thereafter, which is similar to some previous studies in China (17, 24). In China, late marriage and late childbirth are encouraged. The relatively late age at first intercourse may explain the higher HPV prevalence in relatively older women in Beijing than in other countries.

High-risk HPV prevalence is mainly related to the age of populations, lifestyles, and the habits of sexual life. As in previous studies on HPV risk factors, we found consistent associations with the number of sexual partners, number of husband's sexual partners, married status (being single), and age at first intercourse. It is well known that in many populations, the husbands' sexual habits are more important than the woman's sexual habits as a risk factor for sexually transmitted infections (31). The number of husband's sexual partners was the main risk factor for high-risk HPV infection, indicating the important role of males in HPV transmission to female partners. The majority (96.9%) of women in Beijing have only one sexual partner in their life. Although we thought the data may be relatively conservative, the results are very significant. In agreement with previous work (31-33), HPV infection was inversely related to the age of first pregnancy, but there was no association with the number of pregnancies. Perhaps associated with evidence of fewer pregnancies, women in Beijing do not get pregnant multiple times except for a small minority, with an average of two pregnancies only. Similar direct associations were also found with alcohol drinking and smoking, but when adjusted for sexual factors no associations remained. In our survey, higher educational levels and higher income were the risk factors for high-risk HPV infection. At present the reason is unclear for the lack of details on sexual habit. We analyzed different methods of contraception for subjects and found that women took oral contraceptives without HPV infection risk, which was not consistent with reports published overseas (34). We also found an association between columnar ectopy, the most common sexually transmitted infection (history of bacterial vaginosis or trichomonas vaginitis), and HPV prevalence.

Cervical lesion incidence in the 25- to 29-years-old group of Beijing women has a low prevalence rate. However, for middle-aged women (30-44 years) who are sexually active, cervical lesion incidence (7.3%) is significantly higher than that of other age groups. Between 45 and 49 years of age, the incidence of cervical lesion is declining, but for those 50 to 54 years of age, the incidence rate has risen. The results of this study are similar to international reports (4), and also conform with the incidence age and natural development process of cervical cancer (6).

The risk factors for cervical lesion are similar to high-risk HPV infection. Cervical lesion was inversely related to age of first pregnancy, but there was no correlation with the number of pregnancies. Smoking is considered as a risk factor for cervical lesion and cervical cancer, but the effects of alcohol on cervical lesions have not been made clear (35). This study shows no effects of smoking and alcohol drinking on cervical lesion prevalence, after results were adjusted for sexual factors. Differences from using of condoms or IUD would increase the risk of cervical lesion (36). In our study, using oral contraceptives did not increase the risk of HPV infection, but increased the risk of cervical lesion, consistent with international reports (34). Women who have been sexually active since adolescence and whose husbands have several sexual partners form a higher risk cohort of cervical lesion, perhaps related to the increased opportunities for HPV infection (37).

Indicators were introduced into multiple logistic regression equations for analysis, and associations with cervical lesion were weakened. This may be compared with HPV infection; the number of sexual partners and age of first sexual intercourse had minor effects on cervical cancer (8). Long-term use of oral contraceptives could increase the risk of cervical lesion and may be related to progesterone, which could activate E6, E7 fragments of HPV (34). Higher frequency of sexual activity, transmission by husband, and columnar ectopy with less resistance all increase the probability of infection of HPV. The causal relationship between HPV infections and history of trichomonas vaginitis could not be established.

No potential conflicts of interest were disclosed.

Grant Support: Beijing Municipal Science and Technology Commission (No. D0906008040491). This study was a collaborative project jointly undertaken by the Beijing Obstetrics and Gynecology Hospital (Beijing O&G Hospital), Haidian Maternal and Child Health Care Hospital, Chaoyang Maternal and Child Health Care Hospital, Tongzhou Maternal and Child Health Care Hospital, Dongcheng Maternal and Child Health Care Hospital, Fengtai Maternal and Child Health Care Hospital, Huairou Maternal and Child Health Care Hospital, Yanqing Maternal and Child Health Care Hospital, Daxing Maternal and Child Health Care Hospital, Xicheng Maternal and Child Health Care Hospital, Shijingshan Maternal and Child Health Care Hospital, Chongwen Maternal and Child Health Care Hospital, and Xuanwu Maternal and Child Health Care Hospital.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

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