The Asian Cervical Cancer Prevention Advisory Board (ACCPAB) members include Jeffrey Tan (Australia), Jihong Liu (China), Hextan Yuen Sheung Ngan (Hong Kong), Annie Nga Yin Cheung (Hong Kong), Neerja Bhatla (India), Andi Darama Putra (Indonesia), Jong-Sup Park (Korea), Young-Tak Kim (Korea), Soon Ruey (Malaysia), Genera Limson (Philippines), Song-Nan Chow (Taiwan), Kung-Liahng Wang (Taiwan), Wichai Termrungruanglert (Thailand), and Chitsanu Pancharoen (Thailand), et al.
Human papillomavirus type distribution in women from Asia: a meta-analysis
Article first published online: 26 APR 2007
2007, IGCS and ESGO
International Journal of Gynecological Cancer
Volume 18, Issue 1, pages 71–79, January/February 2008
How to Cite
BAO, Y.-P., LI, N., SMITH, J.S., QIAO, Y.-L. and ACCPAB members (2008), Human papillomavirus type distribution in women from Asia: a meta-analysis. International Journal of Gynecological Cancer, 18: 71–79. doi: 10.1111/j.1525-1438.2007.00959.x
- Issue published online: 14 DEC 2007
- Article first published online: 26 APR 2007
- Accepted for publication February 7, 2007
- human papillomavirus;
- type distribution
The aim of this study was to determine human papillomavirus (HPV) type distribution in women with and without cervical neoplasia from Asia and to estimate the potential future impact of an HPV 16/18 prophylactic vaccine in this region. A meta-analysis was conducted including 79 studies using polymerase chain reaction to detect HPV types. A total of 5954, 1653, 958, and 16,803 women with invasive cervical cancer (ICC), high-grade squamous intraepithelial lesions (HSIL), low-grade squamous intraepithelial lesions (LSIL), and normal cytology or histology were included, respectively. Type-specific prevalence of HPV types 6, 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66, 68, 70, 73, and 82 were estimated and stratified by cervical lesion grade. Overall HPV prevalence was 85.9%, 81.0%, 72.9%, and 14.4%, respectively, in women with ICC, HSIL, LSIL, and normal cytology/histology. In ICC, HPV 16 was the predominant type (52.4%), followed by HPV 18, 58, 33, 52, 45, 31, and 35. The estimated HPV 16/18–positive fraction was 66.9%, 40.4%, 26.7%, and 3.3% in women with ICC, HSIL, LSIL, and normal cytology or histology, respectively. In ICC, the estimated HPV 16/18–positive fraction was about 70% in all Asian geographic regions, with the exception of Japan (51.3%). HPV 16/18 vaccines are estimated to provide about 67% protection against ICC in Asia. HPV 58 and 52 were among the five most common types in ICC in eastern and southeastern Asia but not in south central Asia. After HPV 16 and 18, the next most six common HPV types were 58, 33, 52, 45, 31, and 35 that accounted for additional 20% of cervical cancer cases in Asia. For optimal population coverage, these HPV carcinogenic types should be considered for second-generation HPV prophylactic vaccines.
Invasive cervical cancer (ICC) is the second most common cancer among women worldwide. According to estimates from the International Agency for Research on Cancer (GLOBOCAN 2002), an estimated 493,000 new cases and 274,000 deaths of cervical cancer occur among women worldwide each year(1). Approximately 265,885 (54%) cases occur in Asia(2), where cervical cancer remains a significant public health problem threatening women.
Human papillomavirus (HPV) has been established as a necessary cause of cervical cancer and its precursors, including cervical intraepithelial neoplasias grades 2 and 3 (CIN 2–3)(3–6). The utility of high-risk HPV DNA testing is being evaluated as a future cervical cancer screening methods(7). In contrast, HPV prophylactic vaccines hold great promise to reduce the global burden of cervical cancer(8). Thus, the detection and control of carcinogenic HPV types have become the focus of both primary and secondary cervical cancer prevention strategies(9). The determination of the most common HPV types in cervical cancer is instructive for the development of new HPV screening methods and HPV vaccines. Although previous publications of multicenter and meta-analyses provided total information about HPV type distribution in Asia(10–13), data from the Asian region have been limited in terms geographic coverage and cervical status.
HPV prophylactic vaccine has been successfully developed and will be available on the market of some Asian countries. To provide information for the public health and governmental decision makers and government, it is important to determine the detailed pattern of HPV type distribution and to estimate the potential protection of the current HPV 16/18 prophylactic vaccine candidates. The development of new second-generation HPV prophylactic vaccines will likely include additional priority carcinogenic types in addition to HPV types 16/18.
The purposes of this meta-analysis are to estimate the potential protection of an HPV 16/18 vaccine in different geographic regions of Asia and to determine the priority HPV types for the development of new HPV vaccines for the Asian region.
Materials and methods
Source material was obtained from citations listed in Medline. References included in previous studies of Clifford on HPV type distribution in ICC(11), high-grade squamous intraepithelial lesions (HSIL)(12), and low-grade squamous intraepithelial lesions (LSIL)(13) in Asia were updated using the following key search terms: “cervical cancer/cervical neoplasms,”“human papillomavirus (HPV),”“human,”“female,” and “polymerase chain reaction (PCR)”. This analysis included peer-reviewed published literature in the Medline database up to October 2006 and was limited to studies fulfilling the following inclusion criteria: (1) the cervical specimen was from the Asian women, (2) clear description of pathology or cytology determined classification as follows: ICC, HSIL, LSIL, and normal cytology/histology, (3) sample sizes were more than 20 cases for each classification group. Studies at least included one category from four groups (ICC, HSIL, LSIL, and normal cytology/histology), (4) clearly described HPV DNA detection methods by PCR, (5) in addition to HPV 16, 18, 6, and 11, the detection of at least one additional HPV type, and (6) HPV type–specific prevalence stratified by cervical lesion grade (ICC, HSIL, LSIL, or normal). Where available, ICC was independently divided into squamous cell carcinoma (SCC) and adenocarcinoma and adenosquamous carcinoma (ADC). If histology-specific HPV prevalence was not reported or cases included other histology types, cases were classified as unspecific ICC. HSIL refers either to lesions cytologically equivalent to HSIL according to the Bethesda system or to lesions histologically confirmed as CIN 2–3. Cases of carcinoma in situ were included in the classification CIN 3. LSIL refers to lesions cytologically equivalent to LSIL according to the Bethesda system as well as to lesions histologically confirmed as CIN 1. For normal group, women were included with confirmed histology or cytology diagnosis from either population-based or hospital-based studies. Furthermore, if data or data subsets were published in more than one article, only the publication with the largest sample size was included.
For each study, the following key information was extracted: (1) data of publication, (2) country or area of sample, (3) the classification of pathology or cytology (ICC [SCC/ADC], HSIL [CIN 3/CIN 2], LSIL [CIN 1], and normal), (4) type of cervical specimen (fresh or fixed biopsy tissue; exfoliated cell or combination), (5) the PCR primers used to detect HPV-positive samples, (6) diagnosis cervical outcome confirmed by: histology and cytology, and (7) type-specific and overall prevalence of HPV infection, which stratified by pathologic/cytologic classification. The countries were divided into four subregions in Asia according to geographic settings, sample size, and ethnicity includes: eastern Asia-1(14–38) (including China, Hong Kong, and Taiwan, where the majority are Chinese women), eastern Asia-2(39–71) (including Japan and Korea), southeastern Asia(72–79) (including Indonesia, Philippines, Malaysia, and Thailand), and south central Asia(3,80–90) (India and Iran). For studies comparing HPV prevalence across two countries, data were separated into regional components, respectively(21).
Estimation of type-specific prevalence
HPV prevalence data were expressed as proportion of the number of HPV-positive cases among all cases tested for HPV. Type-specific HPV prevalence was defined according to the specific publication and was presented for the most 18 common HPV types identified by the previous ICC meta-analysis(11), including HPV types 6, 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66, 68, 70, 73, and 82(11). Multiple HPV infections were separated into constituent types and thus type-specific prevalence included that in both single and multiple infections. Similarly, HPV type–specific prevalence was presented in descending order for individual HPV types in ICC for each histologic/cytologic classification, and only studies testing for a particular HPV type contribute to the analysis for that specific type. Therefore, sample size varied among the type-specific analyses.
For each histologic/cytologic classification of ICC, HSIL, LSIL, and normal cytology/histology, following sources of variation (publication year, geographic area, histologic determined type for ICC [only for ICC], diagnosis cervical outcome, type of specimen for HPV DNA testing, and type of PCR primers used) were introduced into a unconditional multiple logistic regression analysis. Final logistic models were conducted based on statistically significant variables. Overall adjusted HPV prevalence and 95% confidence intervals for stage of cervical lesion were estimated by adjustment for variables found to be significant in final model. P values comparing type-specific HPV prevalence were calculated using Chi-square tests.
Type-specific HPV prevalence was compared between HSIL /LSIL/normal, with ICC by prevalence ratios (PRs) with 95% confidence intervals. All statistical analyses were done in SAS version 8.0.
A total of 25,368 women from 79 studies(3,14–90) were included in analyses. Among them, a total of 5954, 1653, 958, and 16,803 women with ICC, HSIL, LSIL, and normal cytology/histology were included in 55, 27, 10, and 25 studies, respectively (Table 1). For ICC cases, the majority were SCC (n = 3231) in comparison with ADC (n = 533). Among women with normal cytology/histology, 12,670 women from population-based studies and 4133 women from hospital-based studies were included.
|Number of cases||Crude/adjusted HPV %||Number of cases||Crude/adjusted HPV %||Number of cases||Crude/adjusted HPV %||Number of cases||Crude/adjusted HPV %||Number of cases|
|South central Asiae(72–79)||492||91.9/90.5||—||—||—||—||1983||15.2/14.4||2475|
|Totalg(3,14–90)||5954, 5905/49||85.9/89.5||1653, 1227/426||81.0/70.9||958, 640/318||72.9/41.3,||16,803, 1688/15,115||14.4/15.9||25,368|
Overall HPV prevalence
The overall crude HPV prevalence was 85.9%, 81.0%, 72.9%, and 14.4% in ICC, HSIL, LSIL, and normal cytology/histology, respectively. Some geographic variation in overall HPV prevalence was noted among women with all cervical lesion grades. In ICC, overall adjusted HPV prevalence ranged from 82.5% to 91.1%, being lowest in China/Hong Kong/Taiwan (82.5%), higher in Japan/Korea (86.6%) and south central Asia (90.5%), and the highest in southeastern area (91.1%). In HSIL, overall adjusted HPV prevalence ranged from 75.1% in China/Hong Kong/Taiwan to 85.1% in Korea and Japan. For LSIL, HPV prevalence ranged from 33.3% in India to 74.6% in Korea and Japan. For women with normal cytology/histology, HPV prevalence had a smaller range of 14.0% in southeastern Asia to 14.4% in south central Asia.
In ICC, adjusted HPV prevalence was slightly lower in ADC (84.5%) than in SCC (86.1%), and this difference was not statistically significant. HPV DNA was significantly less frequently detected in biopsies tissue (83.4%) than either in cervical exfoliated cells (89.9%) or in both cells and biopsies (91.0%) (P < 0.0001). For PCR primers, the highest HPV prevalence was detected using short PCR fragment 10 (94.2%) and the lowest in specimens using type-specific PCR (82.8%). HPV prevalence increased with dates of study publication, from 82.8% in specimens included in publications before the year 2000 to 90.5% after the year 2004 (trend test P < 0.0001).
In normal women with cytology/histology, HPV prevalence was lower in the 12,670 women included from population-based studies (10.9%) than in the 4133 women included from hospital-based studies (25.0%) (P < 0.0001).
Summary of type-specific HPV prevalence
In decreasing order of HPV prevalence in ICC cases from Asia, the ten most common HPV types were 16, 18, 58, 33, 52, 45, 31, 35, 59, and 51 (Fig. 1). The HPV 16/18–positive fraction among women with ICC in Asia was 67% overall with geographic variation in subregion of Asia. After HPV 16 and 18, HPV types 58, 33, 52, 45, 31, and 35 accounted for additional 20% of ICC cases in this region. The proportion of ICC cases attributed to HPV 16/18 appeared to differ somewhat by geographic region, being the highest in south central Asia (77.6%), in the order of southeastern Asia (72.0%), Korea (70.3%), China/Hong Kong/Taiwan (69.5%), and being the lowest in Japan (50.3%) (P < 0.0001).
In ICC, HPV 16 type–specific prevalence in SCC was 53.8%, significantly higher than that in ADC (32.3%) (P < 0.0001). Similar results were found for the HPV 16 phylogenetically related types 58, 52, and 35 (P < 0.05) but not for HPV 33 and 31. In contract, the HPV 18 was statistically more common in ADC (34.4%) than SCC (11.1%) (P < 0.0001) (Fig. 2).
Among all ICC cases, there appeared to be some variation in the prevalence of the third, forth, and fifth most common HPV types after HPV 16 and 18 in different subregions of Asia. HPV 16 and 18 were followed by HPV 58, 52, and 33 in eastern Asia (including China/Hong Kong/Taiwan and Korea and Japan), by HPV 45, 52, and 58 in southeastern Asia, but HPV 45, 33, and 35 in south central Asia (Fig. 3). Overall, HPV 58 and 52 were among the five most common HPV types in ICC in all regions of Asia except in south central Asia (India and Iran).
A similar sequence pattern of HPV type–specific prevalence was found in women with HSIL, LSIL, and normal cytology/histology. The ten most common HPV types were 16, 58, 52, 18, 33, 51, 31, 56, 35, and 45 in HSIL;16, 58, 52, 18, 51, 56, 39, 31, 68, and 35 in LSIL; and 16, 52, 58, 51, 18, 56, 35, 33, 39, and 31 in normal histology/cytology, respectively. For HSIL, LSIL, and normal group, HPV 16/18–positive fractions were 40.4%, 26.7%, and 3.3%, respectively.
The PRs are presented in Table 2 for comparisons of ICC to HSIL cases (ICC/HSIL) and ICC to LSIL cases (ICC/LSIL). PRs for HPV types 16, 18, and 45 were 1.6, 2.0, and 1.6 for ICC/HSIL comparisons and 2.6, 2.2, and 2.2 for ICC/LSIL comparisons, respectively. PRs for all other HPV types were less than 1 for ICC/HSIL, although HPV 33 also showed a PR notably higher than 1 for ICC/LSIL comparisons.
|Number of case (%)||Number of case (%)||Number of case (%)||Number of case (%)||ICC/HSIL PR||Number of case (%)||ICC/LSIL PR||Number of case (%)|
|HPV 16a||5954 (52.4)||3231 (53.8)||533 (32.3)||1653 (33.1)||1.6||958 (20.0)||2.6||16,803 (2.6)|
|HPV 18b||5853 (14.5)||3139 (11.1)||524 (34.4)||1587 (7.3)||2.0||790 (6.7)||2.2||15,048 (0.7)|
|HPV 58a||4922 (5.5)||2708 (5.5)||473 (1.3)||1275 (11.8)||0.5||931 (7.9)||0.7||16,470 (0.9)|
|HPV 33||5823 (3.8)||3187 (3.7)||527 (2.7)||1162 (6.6)||0.6||590 (1.2)||3.2||15,194 (0.5)|
|HPV 52a||4585 (3.8)||2556 (4.2)||467 (1.9)||1066 (10.6)||0.4||731 (7.3)||0.5||12,320 (1.5)|
|HPV 45||3857 (2.8)||2297 (2.8)||302 (3.3)||585 (1.7)||1.6||387 (1.3)||2.2||10,204 (0.3)|
|HPV 31||4774 (2.3)||2623 (2.2)||332 (0.6)||941 (5.2)||0.4||563 (3.4)||0.7||15,048 (0.4)|
|HPV 35a||4307 (1.3)||2602 (1.5)||310 (0)||835 (3.1)||0.4||677 (2.5)||0.5||14,731 (0.6)|
|HPV 59||3880 (1.2)||2297 (1)||238 (2.1)||640 (1.4)||0.9||563 (0.9)||1.3||10,481 (0.3)|
|HPV 51||3712 (0.7)||2256 (0.9)||238 (0)||737 (5.7)||0.1||931 (5.7)||0.1||12,090 (0.9)|
|HPV 56||3974 (0.6)||2256 (0.7)||373 (0.5)||640 (3.4)||0.2||563 (5.3)||0.1||10,481 (0.7)|
|HPV 68||4049 (0.6)||2300 (0.4)||379 (1.3)||640 (0.8)||0.8||563 (3)||0.2||10,481 (0.3)|
|HPV 6||4907 (0.4)||2850 (0.4)||387 (0)||714 (0.6)||0.7||483 (0.8)||0.5||10,307 (0.2)|
|HPV 82||2180 (0.4)||1341 (0.1)||106 (0)||162 (0.6)||0.7||51 (0)||—||8182 (0.1)|
|HPV 39||3766 (0.3)||2256 (0.3)||238 (0)||568 (1.4)||0.2||477 (3.8)||0.1||10,351 (0.4)|
|HPV 66||3597 (0.2)||2256 (0.4)||238 (0)||412 (1)||0.2||405 (2.2)||0.1||10,044 (0.3)|
|HPV 70||3344 (0.2)||2189 (0.2)||225 (0)||282 (0.4)||0.5||231 (1.7)||0.1||9221 (0.3)|
|HPV 73||2982 (0.2)||2172 (0.2)||200 (0)||246 (0)||—||196 (0.5)||0.4||9177 (0)|
Overall HPV prevalence
This meta-analysis presents data on HPV type–specific prevalence in over 25,368 women in Asia. Overall HPV prevalence in 5954 ICC cases (85.9%) was lower than the almost 100% prevalence detected using most sensitive PCR HPV detection methods(4). This lower HPV prevalence may be due to the inclusion of studies using PCR detection techniques of lower sensitivity or ascertaining a relatively smaller number of HPV types. Of the 5954 ICC cases included, 76% cases were from eastern Asia, with slightly lower HPV prevalence of 83–86%. A quarter (24%) of ICC cases came from south central and southeastern Asia, with a higher HPV prevalence of 90–91%. The more proportional cases from eastern Asia degraded the average overall HPV prevalence. Adjusted HPV prevalence found in SCC and in ADC cases from Asia were not different statistically, confirming previous conclusions that HPV infection is the primary causal agent for both SCC and ADC consistently worldwide(6,91).
This analysis includes data from 1653 HSIL and 958 LSIL cases, notably increasing the number of cervical neoplasia cases included in previous reviews. With the inclusion of these new cases, overall HPV prevalence of HSIL (80.8%) and LSIL (72.8%) in Asian women were similar to that previously reported (84.2% and 67.1%, respectively)(12,13). In 16,803 women with normal histology/cytology, overall HPV prevalence appeared to be similar within all of the subregions of Asia (eastern, south central, and southeastern) and was slightly higher (∼14%) than that found in 6100 Asian women with normal cytology (8.2%) in population-based samples using General Primer 5, +/6+ HPV DNA detection assays(92). The 12,670 normal women were from population-based study (10.9%), which was similar to that in previous study(92), and 4133 women were from hospital-based study (25.0%). The histologic normal group possibly included the case with abnormal cytology that could heighten the overall HPV prevalence in normal group of Asia.
The overall adjusted HPV prevalence was similar between four geographic subregions within Asia for women with ICC, HSIL, and normal cytology/histology in our study. However, HPV prevalence appeared to differ among LSIL cases within geographic regions of Asia. The possible reason was that the overall sample sizes for LSIL were limited in stratified analyses by geographic region, with one study from Thailand showing a notably low HPV prevalence (33.3%, n = 20)(80). Additional studies with a larger number of women are required to reliably estimate HPV type distribution in LSIL from Asia.
HPV type–specific prevalence
HPV 16 was clearly the predominant type in Asian women with and without cervical neoplasia. In ICC, the attributable fraction of HPV 16 was 52.4%, slightly higher than the figure of 45.9% in 3091 women with ICC from Asia in Clifford’s previous systematic review(11). HPV 16 was more common than HPV 18 in SCC cases, and HPV 18 was the most common type in ADC, consistent with results of previous studies(11,93).
The potential impact of an HPV 16/18 prophylactic vaccine for the future prevention of cervical neoplasia can be estimated from the HPV 16/18–positive fraction in women with cervical neoplasia, under the assumption of wide vaccination coverage. Our data suggest that an HPV 16/18 prophylactic vaccine has the potential to prevent an estimated 67% of ICC cases in Asia. The HPV 16/18–positive fraction was about 70% of ICC cases in all Asia but not in Japan (50.3%). One interesting finding was that the proportion of ICC cases attributable to HPV types 16 and 18 appeared to be slightly lower in Japan (∼50%). This lower fraction of HPV 16/18 cases in Japan may be due to a potential lower detection of HPV 16 and/or 18 by the “L1C1/C2” PCR primer, which is widely used in Japan(41,50,62), and it need furthermore investigation.
After HPV 16 and 18, HPV types 58, 33, 52, 31, 33 35, and 45 were the most six common HPV types in ICC. Figure 1 showed the possible cumulative protection fraction of vaccine with the priority HPV types, according to the descending order of HPV type–specific prevalence in ICC. Our analysis indicated that the prevention of HPV 16, 18, 58, 33, and 52 could potentially provide ∼80% protection of ICC. The prevention of HPV types 16, 18, 58, 33, 52, 31, 35, and 45 could potential provide ∼87% protection of ICC cases in the Asian area, which was similar to other geographic regions(10,11,93). Figure 3 showed that HPV types 58 and 52 were among the five most common types in ICC in all geographic regions of Asia, except south central Asia (India and Iran), confirming results of previous reviews(11,13,37,38,93).
The PR values of HPV 16, 18, and 45 in ICC/HSIL and ICC/LSIL were greater than 1, indicating that HPV 16, 18, and 45 are more likely to progress to cervical cancer from LSIL and HSIL than the other HPV types, supporting results from previous similar study(13,94,95). Although HPV 33 also appeared to have a higher progression potential from LSIL to ICC based on these PR data, further data are needed with larger samples sizes to confirm findings.
The HPV 16/18–positive fractions were 41.3% in HSIL, 26.8% in LSIL, and 3.3% in normal histology/cytology, and ranged 36–50%, 11–33%, and 0.9–8%, respectively. The findings are largely consistent with those from a previous review including fewer cervical neoplasia cases, which showed that the fractions were about 41% in HSIL and 32% in LSIL, ranging from 41% to 67% and from 16% to 32% in HSIL and LSIL, respectively(93).
Our findings provide a detailed description of overall and type-specific HPV prevalence in Asia, stratified by geographic region. With a large sample size and systematic review of the literature, these findings notably improve our understanding of HPV infection prevalence in women having different grades of cervical neoplasia in Asia. Our review, however, was limited as some studies used relatively insensitive assays or only detected a subset of HPV types. Thus, we expect that our estimated figures on the proportion of HPV 16- or HPV 18-positive ICC cases would have been higher if most sensitive PCR assays had been systematically used in all included studies, and if HPV-negative ICC cases have been typed using more sensitive assays(10).
Among 265,885 new cases of cervical cancer occurring in the Asian region, the contributions of eastern Asia, southeastern Asia, and south central Asia were 61,132 (23%), 42,538 (16%), and 157,759 (60%), respectively(2). Although approximately 50% new cases of Asia occur in India and 3% are estimated to occur in Japan(2), the proportion of cases with HPV-typing data from India was notably low (4%), in comparison to Japan, which accounted for 30% of included cases. The inclusion of a relatively greater number of ICC cases typed from Japan may have slightly reduced the proportion of HPV 16– and/or HPV 18–positive ICC cases in Asia. Moreover, the cases were not obtained from every Asian subregion, as some countries had no published HPV DNA–typing data (eg, Myanmar, Singapore, and Vietnam) and were thus not included in this systematic review.
In summary, the estimated HPV 16/18–positive fraction was 66.9% for ICC, 40.4% for HSIL, 26.7% for LSIL, and 3.3% for women with normal cytology/histology from Asia. Thus, first-generation HPV 16/18 vaccines have the potential to provide ∼67% protection against ICC in Asia. HPV 58 and 52 were among the five most common types in ICC in all Asia but not in south central Asia. After HPV 16 and 18, HPV types 58, 33, 52, 45, 31, and 35 accounted for additional about 20% cervical cancer of Asia and should be considered for inclusion in second-generation HPV vaccines.
We are grateful to all of authors who made detailed data available from their published studies, and we express our gratitude to GlaxoSmithKline for its technical support during the identification of published studies for this work.
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