Abstract
Background:
We sought to identify the prevalence of and risk factors associated with cervical abnormalities among Chinese women in Hong Kong.
Methods:
A community-based cervical screening program was offered free of charge in Hong Kong. Information on the demographics, sexual experience, and obstetrical history of women who attended the Cervical Screening Clinic were collected and tabulated with their Pap smear results to establish the risk factors associated with cervical abnormalities among Hong Kong Chinese women.
Results:
A total of 44,219 women attended the Cervical Screening Clinic for their first Pap smear tests over an 8-year period, with the prevalence of cervical abnormality at 4.51%. Adjusted for all associating factors, the significant risk factors of cervical abnormalities identified among Hong Kong Chinese women are being aged 40–49 (odds ratio [OR] 1.53), being single (OR 1.52) or cohabiting (OR 1.52), having received primary school education only (OR 1.53), having had three or more sexual partners (OR 1.52), onset of sexual activity at age ≤18 (OR 1.53), having reported bleeding after intercourse (OR 1.44), and having had more than three pregnancies (OR 1.47). Condom use was identified as the single most significant protective factor reducing the risk of cervical abnormalities among these women (OR 0.76).
Conclusions:
This first population study in Hong Kong provides a better understanding of the risk factors associated with cervical abnormalities among Hong Kong Chinese women. A primary preventive strategy to reduce cervical cancer incidence should focus on modifying these preventable risk factors, complemented by population-based cervical screening programs to increase the coverage rate to 80% in the long term, together with human papillomavirus (HPV) vaccination.
Introduction
According to the World Health Organization (WHO), 1 it is estimated that there are about 500,000 newly diagnosed cases and that 260,000 women die of cervical cancer worldwide annually. Cervical cancer is also the fifth most common cancer to affect women in Hong Kong, with 439 new cases diagnosed yearly, representing 4.3% of all female cancers in 2004. 2 Cervical cancer is one of the few malignancies in which precancerous lesions are both detectable and treatable. Cervical cytology (the Pap smear) is universally accepted as the gold standard for screening. It is reported that cervical screening can prevent around 75% of cancer cases in women who attend regularly. 3 A reduction in both the incidence and mortality of cervical cancer has been noted after the introduction of nationwide cervical screening programs, especially when used in concert with public health measures to increase disease awareness.
In Hong Kong, it was reported that as many as 60%–70% of women had never had a Pap test. 4 A later study shows similar results, with Pap smear coverage in Hong Kong rather low, at only 43% of women having had the test. 5 This low uptake rate of Pap smear screening is unacceptable for a community that is considered economically well off and has a modern healthcare system and a relatively well-educated population.
Demographic characteristics and risk for cervical cancer
Invasive cancer of the cervix seldom appears before the age of 30, rising sharply thereafter and reaching a peak at around age 45–49 years in the European population. 6 In the United States, the incidence rate of abnormal smears is highest among women aged 25–29 years, 7 whereas in India, the age peak incidence of atypical squamous cells is 40–49 years. 8 In Hong Kong, it has been reported that both low-grade and higher-grade lesions were more likely to be exhibited among women aged 35–50 years. 9
A study of the risk factors for high-grade lesions found that the odds ratios (OR) of married women, separated/divorced women, and widows with reference to single women are 2.35, 2.36, and 2.06 respectively, 10 which showed single women as having the lowest risk of developing high-grade lesions compared with other groups of women. However, another study demonstrated the contrary, that women who have never married (OR 1.78) or are divorced (OR 1.76) or widowed (OR 1.27) have a higher risk of developing cervical cancer than those who are married. 11 Another study showed that women with less than a high school education had a 1.5 times higher risk than those with a postgraduate education of developing preinvasive cervical intraepithelial neoplasia (CIN). 12
Relationship between sexual behavior and obstetric risk for cervical cancer
The development of invasive cervical cancer is correlated with sexual behavior. It is estimated that the risk of developing CIN for women aged ≤16 years at first intercourse is 1.9 times the risk of those who are ≥21 years at first intercourse. 12 The risk of developing both squamous cell carcinoma and adenocarcinoma is also related to the lifetime number of sexual partners. 13 Comparing human papillomavirus (HPV)-positive subjects against HPV-negative controls, the risk for infection of those with six or more sexual partners was four times that of those who had had only one partner (OR 3.89). Studies also have shown that long-term use of oral contraceptives (OCs) could be a cofactor of cervical cancer, 14,15 although the association of OC use with cervical cancer is not consistent. 16 Unsurprisingly, regular condom use by sexual partners has been shown to reduce the risk of cervical and vulvovaginal HPV infection of women. 17
There is an association between the number of full-term pregnancies and squamous cell cancer risk. 18 A study has shown that the OR for women who have had one or two full-term pregnancies was 2.3 compared with nulliparous women. 19 Although it is not known if hormones intervene in cervical carcinogenesis, estradiol has been reported to cause immortalization of HPV-induced cells. 20 Comparing the HPV-positive women to the HPV-negative controls, the risk for infection was higher for those with a history of miscarriage, with an OR of 2.59. 21 The risk of carcinoma in situ (CIS) was elevated in women who had had an abortion.
Smoking and alcohol consumption and risk for cervical cancer
The effect of smoking has been investigated extensively in many studies, showing a moderate and statistically significant association with cervical cancer. Although cigarette smoking has been postulated as a cofactor in the etiology of cervical cancer, the effect of cessation of smoking on cervical lesions remained unknown until the study by Szarewski et al. 22 The constituents of cigarettes, including nicotine and tobacco-specific carcinogens, have been detected in the cervical mucus of female smokers. 23
Between May 1995 and June 2003, a Cervical Screening Clinic (CSC) was established in a regional tertiary care hospital. This clinic provided free screening in the form of cervical smears for the public, funded by the Hong Kong Cancer Fund. Public announcement was made in the territory of this free screening service, including advertisements in local newspapers, announcement on the website of the funding organization, and posters at various nongovernmental organizations (NGOs) (particular those that especially served women) and the management offices of government housing estates. Posters and banners were also posted near the clinic. Some women learned about the service through word of mouth, and all women came to the screening voluntarily.
A total of 63,532 cervical smears were collected. All women who attended the clinic for Pap smear tests completed a questionnaire at the time of their clinic visits that solicited information on their demographic characteristics, sexual experiences, obstetrical history, and substance/medicine intake.
Materials and Methods
This was a retrospective study, designed to analyze the information collected during the 8-year period of the CSC. The completed questionnaires and the results of the Pap tests were retrieved from the clinic's records. Information was analyzed to identify the prevalence of abnormal cervical smear among these women, the major reasons for women deciding to have a Pap smear, and the associated risk factors for cervical abnormalities among Hong Kong Chinese women.
The Pap test was done to examine if there were abnormal changes in the cells of the cervix. A small sample of cells from the surface of the cervix was collected using a spatula, was smeared onto a glass slide, and then was immersed into 95% ethanol liquid fixative. The fixed smears were sent to the cytology laboratory and then examined under a microscope. The smears were stained with a Pap stain and screened by cytologists. All abnormal smears were examined by a pathologist.
Data analysis
The women were grouped for analysis according to the presence or absence of cervical abnormality. The Statistical Package for the Social Sciences (SPSS, Chicago, IL) version 13.0 was used for statistical analysis of the data. Descriptive analyses and chi-square tests were performed to determine associations between the demographics and possible risk factors and Pap test results. The significance level was set at p < 0.05. Univariate and multivariate analyses were performed using logistic regression to identify significant risk factors of cervical abnormalities.
Results
During the operation period of the CSC from May 1995 to June 2003, a total of 63,532 Pap smears were tested. Of all the specimens collected, 94.7% (n = 60,168) were adequate for cytology diagnosis determined based on the Bethesda System 2001, whereas 5.3% (n = 3,364) were inadequate for cytology diagnosis. For obvious reasons, inadequate specimens without cytology diagnosis were excluded from this report. Of these, 44,219 (73.5%) were first-time ever visits, and 15,949 (26.5%) were repeat visits. Only the 44,219 first-time cervical smears with adequate specimens are reported in this study, giving overall normal cytological Pap smear results of 42,223 (95.5%) and abnormal cytological smears of 1,996 (4.5%) for the first-time visits.
Demographic characteristics and Pap test results
Table 1 compares the demographic characteristics of women with normal and those with abnormal Pap test results. Women aged 40–49 were the group of women with the highest percentage of abnormal Pap test results (4.9%) compared with other age groups and the overall rate of 4.5% in this population. There are statistically significant differences between women with normal and abnormal Pap test results in different age groups (p ≤ 0.001).
Significant at p < 0.05; **significant at p < 0.005.
Cohabiting women (6.1%) and separated women/widows (5.4%) were more likely to have abnormal Pap test results compared with married and single women and the overall rate of 4.5%. There was also a significant difference of Pap test results in terms of marital status (p ≤ 0.025). Women with primary school and lower educational level were more likely to have abnormal Pap test results (4.9%) than other women with higher education. There were significant differences between women with normal and abnormal Pap test results in terms of educational level (p ≤ 0.001). Current smokers and those who drank alcohol daily were more likely to have abnormal Pap test results (6.7% and 5.9%, respectively) than those who did not smoke or drink (4.4%). There were significant differences in Pap test results for women who smoked (p ≤ 0.0001) or drank (p ≤ 0.0009).
Relationship between sexual experiences, obstetrical history, and Pap test results
Table 2 compares the sexual experiences of women with normal and abnormal Pap test results. Women who started sexual activity at a younger age (<18) had a higher percentage of abnormal Pap test results than those who started sexual activity between the ages of 18–29 and ≥30 years (6.4% vs. 4.5% and 2.9%). There is a statistically significant relationship between the onset of sexual activity and abnormal Pap results (p ≤ 0.001). The rates of abnormal Pap test results increase as women increase their number of sexual partners. The rates of abnormal Pap results are 4.1%, 5.8%, and 7.1% for women with one, two, and three or more sexual partners, respectively. Results show a significant relationship between the number of sexual partners and abnormal Pap test results (p ≤ 0.001).
Significant at p < 0.05; **significant at p < 0.005.
IUCD, intrauterine contraceptive device.
Women who had had a sexually transmitted disease (STD) were more likely to have abnormal Pap test results than women who had never had an STD (5.6% vs. 4.5%), but without a statistically significant difference (p ≤ 0.23). Women who had bled after intercourse had a statistically significantly higher percentage of abnormal Pap test results than those who had not bled after intercourse (6.7% vs. 4.4%) (p ≤ 0.001). Women who reported using condoms had the lowest rate of abnormal Pap test results (3.5%) compared with those using other methods of contraception, with a significant difference at p ≤ 0.001.
Table 2 also shows the relationship between obstetrical history and Pap test results. The rates of abnormal Pap test results increased for women with increased numbers of pregnancies. The rates were 3.1%, 3.2%, 4.1%, 4.5%, and 5.6% for women with zero, one, two, three, and four pregnancies, respectively. The rates of abnormal Pap test were 4.4%, 4.7%, and 5.8% for women who had had zero, one, and two or more miscarriages, respectively. Women with more children were more likely to have abnormal Pap test results. The percentages of abnormal Pap test results were 3.6%, 4.1%, 4.4%, and 5.3% for women with no children, one, two, or three or more children, respectively. Women who had had an abortion were found to have a higher rate of abnormal Pap test results than those who had never had an abortion (5.2% vs. 4.0%). There was a statistically significant relationship between abnormal Pap test results and increasing number of pregnancies (p ≤ 0.001), miscarriages (p ≤ 0.025), number of children (p ≤ 0.001), and having had an abortion (p ≤ 0.001).
Risks for cervical epithelial abnormalities
Logistic regression was used to identify the adjusted OR of possible risk factors for abnormal Pap test results. All 13 variables, except history of STD, that had been identified as significant factors in previous analyses were entered. Results show that 8 of the 13 variables entered were identified as risk factors in the final model (Table 3). Demographic risk factors were women in the age groups 30–39 (OR 1.361), 40–49 (OR 1.53), ≥50 (OR 1.388) compared with younger women (<30); those who were single (OR 1.517), cohabiting (OR 1.519), or separated/widowed (OR 1.319) compared with married women; those who had attained a primary school or less (OR 1.527) or secondary school education (OR 1.457) compared with those with a tertiary level education.
OR adjusted for all other variables.
Reference group.
Significant at p < 0.05; **significant at p < 0.005.
CI, confidence interval; OR, odds ratio.
Behavioral risk factors were women who had had two sexual partners (OR 1.372) or three or more sexual partners (OR 1.522) compared with those who had had none or only one; women who had reported bleeding after intercourse (OR 1.439) compared with those who had not; women who had started sexual activity <18 years of age (OR 1.528) or between 18 and 29 years (OR 1.306) compared with those who started at ≥30 years; those whose contraceptive practices were using injection (OR 0.909), condom (OR 0.758), pill (OR 1.137), intrauterine contraceptive device (IUCD) (OR 1.115), or tubal ligation (OR 1.001) compared with those who used no contraceptives; and women who had had one (OR 0.888), two (OR 1.125), three (OR 1.203), or four or more pregnancies (OR 1.468) compared with those who had never been pregnant.
Discussion
Demographic risk factors for cervical epithelial abnormality
The risk factors associated with cervical epithelial abnormality among Hong Kong Chinese women are consistent with those found in similar studies in the West. According to the results of this study, the risk of developing epithelial abnormality of the cervix for women aged 40–49 was 1.5 times the risk of those <30. These results are supported in another study in Hong Kong, in which both low-grade and higher-grade lesions were more likely to be exhibited among women aged 35–50 years. 9
The results of this study showed that women with a lower educational level had a higher risk of developing cervical epithelial abnormality. The risks of progressive cervical epithelial abnormality for women with primary level or less and secondary level education were 1.5 and 1.4 times that of women with tertiary level education. It has been reported that the risks of developing high-grade lesions for women without education in Spain and Colombia were 1.3 and 1.7 times, respectively, compared with those who had received higher education. 24
Marital status, sexual partners, and age at onset of sexual activity
We found that the risk of cervical epithelial abnormality for single and cohabiting women was 1.5 times the risk and that for separated women/widows was 1.3 times the risk of those who were married. Patil et al. 25 also found that risk factors of cervical cancer were being widowed, separated, or divorced. Analysis shows that women with a greater number of sexual partners had higher rates of cervical abnormalities, from 4.1% for no or one sexual partner to 7.1% for three or more sexual partners. The risks of advancing cervical epithelial abnormality for two and three or more sexual partners were 1.3 and 1.5 times, respectively, compared with those with no or one sexual partner. This finding was supported by Zhao et al., 26 who found that the risk of HPV infection in women with multiple sexual partners was 1.4 times that of those with no sexual partner.
The results show that women who were younger at the onset of sexual activity were at a higher risk of developing cervical epithelial abnormality. The risk of developing cervical epithelial abnormality for women <18 years at the onset of sexual activity was 1.5 times the risk of those who had started sexual activity at ≥30 years. Another study reported similar results; that is, the risk of cervical cancer for women at 15–16 years and at <15 at the time of first intercourse was 1.9 and 2.2 times, respectively, compared with those who first had intercourse at ≥21. 27 Results suggested that marital status, number of sexual partners, and age at onset of sexual activity are possibly interrelated; thus, those who are married, are older at the onset of sexual activity, and have fewer sexual partners had lower rates of cervical abnormalities.
Bleeding after intercourse
Our results show that women who bled after intercourse had a higher risk of developing cervical epithelial abnormality. The risk of progressing cervical epithelial abnormality for women with bleeding after intercourse was 1.4 times the risk of those without bleeding. This is unsurprising, as bleeding after intercourse is an indication of possible vaginal infections, STDs, cervical dysplasia, or uterine fibroid, possibly leading to development of a cervical abnormality.
Contraceptive use
Use of condoms by women's partners demonstrated a reduced risk of progressing cervical epithelial abnormality. The risk of developing a cervical epithelial abnormality for women whose partners used condoms was 75.8% of the risk for those whose partners did not. This finding is supported by a previous study, 17 which showed that among newly sexually active women, consistent condom use by their partners reduces the risk of cervical and vulvovaginal HPV infection.
Number of pregnancies
Women with two or more pregnancies had a higher risk of progressive cervical epithelial abnormality. The risks of developing cervical epithelial abnormality for women with two, three, and four or more pregnancies were, respectively, 1.1, 1.2, and 1.5 times greater than those of women who had never been pregnant. This finding was supported by the findings of Kjellberg et al. 28 The risk of developing CIN II–III for women who had been pregnant was 1.1 times the risk of those who had never been pregnant.
To summarize, the significant risk factors of cervical abnormalities identified among Hong Kong Chinese women are age (40–49), cohabiting and being separated, having attained a lower educational level, younger age at onset of sexual activity, having multiple sexual partners, bleeding after intercourse, nonuse of condoms, and multiple pregnancies.
Limitations
This was the first population study (>44,000 participants) exploring the various risk factors associated with cervical abnormalities among Chinese women in Hong Kong. The study is limited because of its retrospective nature, in which women's self-reported information was retrieved from the CSC's medical records.
Conclusions
This population-based study shows that the prevalence of cervical abnormality among Hong Kong women is 4.51%. Sexual behavior is identified as the key preventable risk factor of cervical abnormalities among Hong Kong Chinese women. Primary prevention of cervical cancer and promotion programs should target people at risk, focusing on modifying the avoidable risks of getting cervical cancer. The main strategies should be organized screening and the promotion of safer sex.
After operation of the CSC, a territory-wide cervical screening program was launched in Hong Kong by the Department of Health (DH) in early 2004. 2 The DH provides cervical smear tests to women aged 25–64 years who have ever had sexual relations. All women are recommended to have regular triennial screening followed by two consecutive annual smears, with letter reminders and government broadcasts on public television. The coverage rate of the screening program, as a way to measure the effectiveness of Pap screening program is being monitored. From 2004 to 2008, 59.2%–64.1% of women aged 25–64 had screening within the last 3 years, in comparison to the estimated 44% ever screening coverage rate for women in Hong Kong. 5 It is the aim of the CSC to increase the coverage rate to 80%–85% in the long term.
A call-recall system has been instituted to inform and remind eligible women to have cervical cancer screening. Once a woman is registered with the Cervical Screening Information System, the DH will send letters to remind her when she is due for her next smear. Private doctors also send reminder letters to their clients to have cervical smears taken.
The first generation of HPV vaccines has been available in Hong Kong since 2006, and it will be interesting to see how public and private funding of HPV vaccination will affect changes in the epidemiology of HPV infections and cervical abnormalities in Hong Kong. To examine how HPV vaccination will modify the landscape of cervical abnormalities among Chinese women in Hong Kong, further studies should be carried out in Hong Kong in the postvaccination era. The results of this study provide data as a baseline for comparison with incidents of cervical abnormalities in the post-HPV vaccine era in Hong Kong. For cervical cancer prevention, combined protocols of HPV vaccination together with mass screening by cytologic study are recommendations adopted by public health professionals.
Studies have shown that certain demographic characteristics of women, such as age, marital status, and education level, are related to the incidence of cervical cancer. Studies have shown that the age of initial sexual activity, the number of sexual partners, the use of oral contraceptives, as well as sexually transmitted diseases are related to cervical cancer. Obstetrical history, including the number of pregnancies, parity, miscarriages, and abortions, has also been shown to be associated with cervical cancer. Most of these studies were done in the West, and the risks for cervical cancer among Chinese are not known.
This population‐based study reveals that the prevalence of cervical abnormality among Chinese women in Hong Kong is 4.51%. The cost of a Pap test could have been a barrier to many women, and 80% of women were attracted to this free screening service offered. The significant risk factors of cervical abnormalities identified among Hong Kong Chinese women are age (40–49), cohabiting and being separated, having attained a lower educational level, younger age at onset of sexual activity, having multiple sexual partners, bleeding after intercourse, and multiple pregnancies. Condom use can significantly reduce the risk of cervical abnormalities among Chinese women in Hong Kong.
Footnotes
Acknowledgments
This study was supported by the Cervical Screening Clinic of the Department of Anatomical and Cellular Pathology, Faculty of Medicine, The Chinese University of Hong Kong, with funding provided by the Hong Kong Cancer Fund.
Disclosure Statement
The authors have no conflicts of interest to report.
