IJE Advance Access originally published online on March 3, 2008
International Journal of Epidemiology 2008 37(3):536-546; doi:10.1093/ije/dyn033
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Smoking and human papillomavirus infection: pooled analysis of the International Agency for Research on Cancer HPV Prevalence Surveys
1 International Agency for Research on Cancer, Lyon, France.
2 Proyecto Epidemiológico Guanacaste, Fundación INCIENSA, San José, Costa Rica.
3 VU Medical Center, Amsterdam, The Netherlands.
4 College of Medicine, University of Ibadan, Ibadan, Nigeria.
5 Neonatology Department, Hung Vuong Hospital, Ho Chi Minh City, Vietnam.
6 Escuela de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile.
7 Instituto de Oncología Angel H. Roffo, Universidad de Buenos Aires, Buenos Aires, Argentina.
8 Instituto Nacional de Cancerología, Bogota, Colombia.
9 Servei d’Epidemiologia i Registre del Cancer Institut Català d’Oncologia, L’Hospitalet del Llobregat, Barcelona, Spain.
10 Research Institute, National Cancer Centre, Goyang, Korea.
11 Research Division, National Cancer Institute, Bangkok, Thailand.
12 Instituto Nacional de Salud Pública, Cuernavaca, Morelos, Mexico.
* Corresponding author. Dr Salvatore Vaccarella, International Agency for Research on Cancer, 150 cours Albert Thomas, 69372 Lyon cedex 08, France. E-mail: vaccarella{at}iarc.fr
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Abstract |
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Background Smoking increases the risk of squamous-cell carcinoma of the cervix, but it is not clear whether smoking increases the risk of acquisition or persistence of human papillomavirus (HPV) infection.
Methods Information on smoking was collected from 10 areas in four continents among population-based, age-stratified random samples of women aged 15 years or older. HPV testing was performed using PCR-based enzyme immunoassay. Unconditional logistic regression was used to estimate odds ratios (OR) and corresponding 95% confidence intervals (CI) of being HPV-positive by smoking habits, adjusted for age and lifetime number of sexual partners.
Results Ten thousand five hundred and seventy-seven women (mean age 41.4 years) were included. Among current smokers, the risk of being HPV-positive increased with smoking intensity, after allowing for lifetime number of sexual partners: ORs for <5, 5–14 and 
15 cigarettes per day were 1.21 (95% CI 0.95–1.54), 1.39 (95% CI 1.04–1.87) and 2.01 (95% CI 1.32–3.08), respectively, as compared with never-smokers. The risk among former smokers (OR = 0.95, 95% CI 0.73–1.23) was similar to that among never-smokers. Analyses stratified by lifetime number of sexual partners showed a significant trend in risk only for women with one lifetime sexual partner.
Conclusions Our study suggests that current, though not former, smoking is associated with an increased prevalence of HPV, after allowance for sexual covariates. Among current smokers, HPV prevalence increased with smoking intensity, but a clear dose–response relationship was exclusively seen among women who declared one lifetime sexual partner.
Keywords Human papillomavirus, smoking, risk factors, epidemiology, general population
Accepted 30 January 2008
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Introduction |
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Human papillomavirus (HPV)1,2 is sexually transmitted and is considered to be a necessary cause of cervical cancer.3 Other factors, however, may influence the cervical cancer process at any stage by modifying the probability of acquisition or persistence of HPV infection, or by modifying the probability of progression to cancer.4
Smoking has been found to be significantly associated with an increased risk of squamous-cell carcinoma,5,6 although not adenocarcinoma,6 of the cervix. The association with smoking, which seems to be dose-dependent and to disappear after smoking cessation, was also confirmed by studies that were able to restrict the analyses to HPV-positive women.6
Current knowledge on the relationship between smoking and prevalence or incidence of HPV infection is relatively scant, with previous studies reporting inconsistent results.7–24 Therefore, it is not clear whether smoking could increase the risk of cervical cancer by increasing the risk of acquisition, or persistence, of HPV infection. Smoking has been reported to impair immune response,25–27 and, hence, it may interfere with the clearance of HPV infection.28,29 However, women who smoke tend to report a greater number of sexual partners than women who do not, and, thus, adequate allowance for the confounding effect of sexual behaviour is of paramount importance in interpreting any association between smoking and HPV prevalence.30
To further explore these issues, we assessed the relationship between smoking and prevalence of HPV infection in the International Agency for Research on Cancer (IARC) HPV Prevalence Surveys.
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Methods |
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Contributing studies and data collection
Study protocols and questionnaires were developed by the IARC for each of 13 areas in 11 countries worldwide, and studies were carried out between 1993 and 2005. Population sampling methods of participating women have been previously described for the individual areas. Ho Chi Minh City, Vietnam,31 Lampang and Songkla, Thailand,32 Korea,33 Spain,34 Mexico,35 Argentina,36 Chile,37 Colombia38 and Nigeria39 were included in the present report. Surveys from Hanoi, Vietnam,31 China40 and India41 were not included on account of the extremely low proportion (<0.1%) of women who reported being ever-smokers.
In summary, in each area an attempt was made to obtain a random age-stratified sample of the population that included at least 100 women in each 5-year age group, from 15–19 to 65 and over. In Colombia, women were randomly selected from four low-income health districts and from an adolescent clinic for contraceptive counselling. Participation ranged from 48% in Songkla, Thailand (where most non-participants were not found at the address given by the population list), to 95% in Mexico. Exclusion criteria were pregnancy at time of recruitment, previous hysterectomy and physical or mental incompetence. The number of individuals per study area in this analysis sometimes slightly differs from that reported in the original findings due to different selection criteria or additional HPV testing after publication.
Trained interviewers questioned study participants face-to-face using a questionnaire that included information on socio-demographic characteristics, Papanicolaou (Pap) smear screening history, reproductive history, menstrual factors, oral contraceptive use and characteristics of sexual behaviour such as lifetime number of sexual partners and age at sexual debut. Women were also asked whether they thought their stable male sexual partners (referred to as ‘husbands’) had had extramarital sexual relationships with other women or with female sex-workers. Questions on smoking habits included status (never, former or current smoker), intensity (number of cigarettes smoked per day) and duration of the habit (age at starting and, for former smokers, age at cessation).
All participants signed informed consent forms according to the recommendations of the IARC and the local ethical review committees, which approved the study.
Gynaecological examination, specimen collection and cytology
Study participants underwent a pelvic examination performed by a gynaecologist or specially trained personnel. Samples of exfoliated cells from the ectocervix were collected with one or two wooden Ayre spatulas, and from the endocervix with a cytobrush (Cervibrush, CellPath, Herte, UK). After the preparation of a Pap smear, the remaining exfoliated cervical cells were placed in tubes with phosphate-buffered saline (PBS) and stored on ice. Cells were centrifuged at 3000 g and the resulting pellets were re-suspended in PBS and frozen between –20°C and –80°C until they were shipped to IARC for storage. Pap smears were stained and read locally and classified according to the Bethesda or equivalent system. Atypical squamous cells of undetermined significance or worse were found in 4.7% of study women (range between 1.6% in Ho Chi Minh City, Vietnam, and 9.4% in Nigeria). Seventy-four women (0.7%) had a diagnosis of high-grade squamous intraepithelial lesion or worse.
HPV DNA detection techniques
HPV testing was performed on exfoliated cervical cells in the Department of Pathology, VU Medical Center, Amsterdam, The Netherlands, with the exception of the Mexican study. Only women who tested positive for β-globin were included in this analysis.
A first screening was performed to determine the overall presence of HPV DNA using a general GP5+/6+ primer-mediated PCR.42 PCR products were assessed by enzyme immunoassay using oligoprobe cocktails to detect the following 36 HPV types: HPV6, 11, 16, 18, 26, 31, 33–35, 39, 40, 42–45, 51, 52–59, 61, 66, 68–73, 81–84, 89.42 In addition, PCR products were tested using a low-stringency Southern blot analysis of PCR products with a cocktail probe of HPV-specific DNA fragments. Subsequently, typing of samples positive for HPV was performed by enzyme immunoassay or reverse line blot analysis of GP5+/6+ PCR product using HPV type-specific oligoprobes for the HPV types described above.42,43 Samples that were GP5+/6+-positive by low-stringent Southern blot analyses, but were not identified by the above-mentioned typing protocols, were considered as HPVX, i.e. uncharacterized HPV types. For Chile, the oligoprobe cocktail was extended to include HPV types 30, 32, 64, 67, 69, 85, 86 and JC9710.
The determination of HPV types in the Mexican study has been previously described.35 Briefly, it was carried out on specimens from women with normal cytology at the Department of Molecular Microbiology and Immunology, Johns Hopkins University School of Public Health (Baltimore, MD, USA) and at the National Institute of Public Health (Cuernavaca, Morelos, Mexico), using biotinylated MY09/11 consensus primers and genotyping (27 HPV types: 6, 11, 16, 18, 26, 31, 33, 35, 39, 40, 42, 45, 51–59, 66, 68, 73, 82–84) by a single-hybridization, reverse line blot detection method.44 Good comparability of findings from GP5+/GP6+- and MY09/11-based PCR has been reported.45
Herpes simplex virus type-2 (HSV-2) serum antibodies
The presence of type-specific plasma IgG antibodies against HSV-2 was tested for in sera obtained in Vietnam, Thailand, Korea, Mexico, Argentina, Nigeria and Spain. Serological testing was conducted blindly, in a central laboratory in Seattle, WA, USA, using a HSV-2 ELISA assay developed by Focus Technology (formerly MRL, Cypress, CA, USA).46 All HSV-2-positive sera were re-tested to confirm results.
Statistical analysis
Smokers were defined as those women who had smoked at least one cigarette per day for a continuous period of 1 year or more. Former smokers were defined as those women who had abstained from any type of smoking for at least 12 months prior to the interview. On account of differences in the questionnaire, Mexico could not contribute to the analysis on smoking frequency and duration.
Unconditional logistic regression was used to estimate odds ratios (OR) and the corresponding 95% confidence intervals (CI) of being HPV-positive according to smoking habits. All ORs shown in the figures were adjusted for age group (<25, 25–34, 35–44, 45–54, 55 years), lifetime number of sexual partners (1, 2, 3), and, when appropriate, study area. Information on lifetime number of sexual partners in Colombia was available only in two categories, one and two partners or more; consequently, ORs for this area were adjusted on two levels only (1 and 2 partners). Ninety-eight women who declared to have never had sexual intercourse were excluded from the analyses. Analyses adjusted for lifetime number of sexual partners in four categories (1, 2, 3, 4) or husbands’ extramarital sexual relationships (no, and yes or uncertain) did not substantially modify the ORs for the smoking variables and, therefore, are not presented.
The variables were analysed categorically, and when more than two groups were compared, the graphical representation was made by using floating absolute risks.47,48 This method assigns a ‘floating’ standard error to each category, which is independent of the choice of baseline group. Conventional ORs and 95% CIs are always used in the text. Tests for linear trend of ORs were performed, giving an increasing score for each level of the categorized variable and fitting them into the model as continuous variables.
Most results are presented graphically, plotting the summary ORs as black squares, whose size is inversely proportional to the variance of the estimate. A horizontal line represents the 95% CI. Diamonds are used to plot the summary OR for all studies together. The diamonds represent the pooled OR and the extremes show the limits of the 95% CI.
Heterogeneity of the OR between areas was tested by calculating the difference between the log likelihood of the model that included the interaction term between the areas and exposure of interest and the log likelihood of the model that included the exposure only, and comparing it with the chi-squared distribution with degrees of freedom equal to the number of areas minus one.
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Results |
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A total of 10 577 women were available for the present analysis. Overall, HPV prevalence was 12.5%, and ranged from 2.5% in Spain to 26.2% in Nigeria. The mean age was 41.4 years, varying between 32.9 years in Colombia and 47.8 years in Songkla, Thailand (data not shown). Smoking and multiplicity of sexual partners were positively associated (OR for
2 vs 1 partner in ever- vs never-smokers = 2.6, 95% CI 2.3–2.9). The ORs varied by area from 0.8 (95% CI 0.4–1.9) in Korea to 7.6 (95% CI 2.8–20.0) in Vietnam (Table 1).
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Figure 1 shows the OR of HPV positivity for ever-smokers compared with never-smokers in each study area and overall. The percentage of ever-smokers ranged from 1.8% in Nigeria to 56.4% in Chile, with an overall value of 22.2%. After allowing for lifetime number of sexual partners, ever-smoking was associated with an increased risk of being HPV-positive (OR = 1.18, 95% CI 1.01–1.39), but significant differences were found between study areas, with the formal heterogeneity test giving a P-value of 0.009. The two study areas in Thailand (Lampang and Songkla) showed an inverse association between smoking and HPV positivity, and the OR was significantly lower than 1.0 in Lampang (OR = 0.45, 95% CI 0.22–0.92). Smoking was rare (6.1%) in Songkla and in Lampang it was more often reported by women older than 35 years (40.7%) than among younger women (2.3%). All other study areas showed positive associations between ever-smoking and HPV detection, with the most elevated OR found in Korea (OR = 2.32, 95% CI 1.18–4.58). After the exclusion of the two Thai areas, the heterogeneity test was no longer significant (P = 0.383) and the overall OR for ever-smoking adjusted for lifetime number of sexual partners was 1.31 (95% CI 1.11–1.56).
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2 (9 df) = 22.0; P = 0.009. aAdjusted for age and, when appropriate, for study area. bAdjusted for age, lifetime number of sexual partners and, when appropriate, for study area. L, Lampang; S, SongklaFigure 2 shows pooled results for the association between the number of cigarettes smoked per day and HPV positivity. Among current smokers, the risk of being HPV-positive increased with increasing smoking intensity: ORs for <5, 5–14 and
15 cigarettes per day were, after adjustment for lifetime number of sexual partners, 1.21 (95% CI 0.95–1.54), 1.39 (95% CI 1.04–1.87) and 2.01 (95% CI 1.32–3.08), respectively, as compared with women who had never smoked. The risk among former smokers (OR = 0.95, 95% CI 0.73–1.23) was similar to that among never-smokers (Figure 2).
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Figure 3A shows the association between the number of cigarettes smoked per day and HPV positivity by lifetime number of sexual partners. Among women who reported only one sexual partner, the risk of being HPV-positive increased steadily with increasing number of cigarettes smoked, with an OR of 3.03 (95% CI 1.58–5.82) for
15 cigarettes per day as compared with never-smokers. Among women who reported two and three or more sexual partners in their lifetime, non-significantly increased ORs were found for each category of smoking intensity, but risk trends by number of cigarettes were not statistically significant (P-trend = 0.42 for two sexual partners; P-trend = 0.30 for three or more sexual partners).
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In an attempt to further eliminate the possible confounding effect of sexual behaviour among women with one lifetime sexual partner only, we evaluated the association between smoking intensity and HPV positivity in separate strata of husbands’ extramarital sexual relationships (no, and yes or uncertain). Consistent association between HPV positivity and smoking intensity were found in the two strata (Figure 3B).
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In the six study areas for which information on HSV-2 seropositivity was available, the risk pattern for smoking intensity was evaluated in seropositive and seronegative women. Among HSV-2-seronegative women, the ORs for currently smoking <5, 5–14 and
15 cigarettes per day were 0.79 (95% CI 0.41–1.52), 0.80 (95% CI 0.37–1.73) and 2.64 (95% CI 1.25–5.56), respectively, as compared with never-smokers, while among HSV-2-seropositive women the ORs for currently smoking <5, 5–14 and 15 cigarettes per day were 1.41 (95% CI 0.81–2.46), 1.43 (95% CI 0.83–2.46) and 1.49 (95% CI 0.66–3.32), respectively, as compared with never-smokers. No significant association emerged between smoking duration and HPV positivity. Among current smokers, the OR adjusted for lifetime number of sexual partners for HPV positivity was 1.38 (95% CI 1.03–1.86) for women who had smoked for 10–19 years and 0.97 (95% CI 0.71–1.33) for those who had smoked for 20 years or more as compared with never-smokers.
Findings on smoking and HPV positivity were similar when high-risk and low-risk HPV types (as defined in Muñoz et al.,49 data not shown) and women <35 years and 35 years of age were considered separately. ORs among smokers of 15 cigarettes per day, for instance, were 2.38 (95% CI 1.28–4.45) for women below the age of 35, and 1.90 (95% CI 1.04–3.45) for women aged 35 years or more.
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Discussion |
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The present pooled analysis of the IARC HPV Prevalence Surveys showed that current tobacco smoking was associated with a significant, although moderate, increased risk of prevalent HPV infection. Among current smokers, the risk of being HPV-positive increased with increasing number of cigarettes smoked per day, and women who reported to smoke 15 or more cigarettes daily had a
2-fold risk of HPV positivity as compared with never-smokers. Conversely, former smokers did not show a different risk of HPV positivity compared with never-smokers. The present findings on tobacco smoking contrast with the lack of association, in the same IARC surveys, between HPV prevalence and certain characteristics that are associated with cervical cancer, i.e. parity, age at first full-term pregnancy and oral contraceptive use.50
Tobacco smoking is suspected to facilitate the acquisition or persistence of an HPV infection through a reduced number of Langerhans cells and CD4 lymphocytes,25–27 which are markers of local immune response in the cervix. In addition, smoking can decrease the activity of the natural killer cells51 and therefore it may affect the innate immune system.
Previous studies on the relationship of smoking with HPV infection were generally much smaller than our present pooled analysis and showed inconsistent results. In respect to HPV prevalence, a large study in women from Costa Rica11 found a positive association of smoking with HPV16 only. Two other prevalence studies in Canada12 and Denmark17 reported respectively positive, and no association between smoking and HPV infection. Studies on incident HPV infection that allowed for sexual covariates were few and among them two cohort studies of female university students7 and adolescents16 from the USA showed increased HPV incidence among smokers. Two studies that were carried out in Colombia,14 whose baseline findings are part of our present report, and Canada15 did not report any significant association between tobacco smoking and the incidence of HPV infection. None of the studies on incidence or prevalence of HPV infection provided the information by number of cigarettes smoked daily.
Few studies of relatively small size have analysed the effect of smoking on HPV persistence: a study in young women from the USA showed a lower probability of HPV clearance among ever-smokers as compared with never-smokers, and a significant dose–response relationship of HPV persistence with increasing duration of years of the habit, but not with smoking intensity.21 Other authors, however, reported an inverse,19,20 or a complete lack of association22 between smoking and HPV persistence.23,24 Finally, some authors evaluated the relationship of smoking with HPV infection in HIV-positive women from the USA: a prospective study found that smoking was associated with a significantly higher incidence and prevalence of HPV infection.52 Two other studies found that smoking was not associated with HPV clearance53 among HIV-positive women.54
A study in Danish soldiers analysed the relationship between smoking and penile HPV infection, finding an association with persistence, but not with acquisition, of the infection.55
In our study, we found significant between-study area heterogeneity in the apparent effect of smoking on HPV positivity. Heterogeneity, however, chiefly derived from one country, Thailand, where an inverse association between smoking and HPV positivity emerged. Smoking was, however, extremely rare among young women in Thailand.
When we performed a sensitivity analysis after the exclusion of the two Thai areas, the heterogeneity test was no longer significant (P = 0.383). The exclusion of these two areas increased the magnitude of the association between smoking and HPV-positivity.
A relationship between smoking and HPV infection is difficult to prove mainly because of the strong confounding effect of sexual behaviour. In our population, the lifetime number of sexual partners was positively associated with both HPV positivity2 and the number of cigarettes smoked per day. The association between multiplicity of sexual partners and smoking varied, however, by study area. Interestingly, the excess of HPV-positivity among smokers was found also in areas where smoking and multiplicity of sexual partners were not correlated (e.g. Korea and Nigeria).
If tobacco smoking increases HPV acquisition or persistence, then we would expect to see an effect of smoking in each category of women with a similar level of exposure to HPV. Thus, we assessed the relationship between smoking intensity and HPV positivity across strata of categories of lifetime number of sexual partners. A clear dose–response relationship was seen only among women who reported one sexual partner, but not among women who reported multiple sexual partners.
The increase in HPV positivity with increasing smoking intensity observed for women who reported one sexual partner may be due, however, to residual confounding by sexual behaviour. It is conceivable that women who under-reported their lifetime number of sexual partners and have, therefore, increased HPV prevalence are also likelier to smoke and, if they do so, to smoke a greater number of cigarettes than women who truly had one sexual partner only. This would spuriously produce a trend in risk by number of cigarettes in the one-partner only stratum.
Smoking intensity was also examined by strata of seropositivity for HSV-2, which, besides being a risk factors for HPV positivity in our study populations2, is an objective marker of sexual behaviour. The OR for 15 or more cigarettes smoked per day reached the level of significance only among HSV-2-seronegative women.
Finally, husbands’ sexual behaviour is known to affect a woman's probability of HPV infection.2 To take into account for the ‘male factor’, women who reported one sexual partner only were further stratified by husbands’ extramarital sexual relationships. A dose–response association of HPV positivity with smoking intensity was found among both women who reported that their only sexual partner had, or might have had, extramarital sexual relationships and women who reported that their only sexual partner did not have extramarital sexual relationships.
A limitation of this cross-sectional study is that it includes information on HPV prevalence, not allowing the distinction between the factors associated with acquisition or persistence of HPV infection. In addition, information on recent number of sexual partners, which was found to be the strongest risk factor for acquisition of new HPV infection,7,14,18 was not available in our study.
A recently published reanalysis of 23 epidemiological studies, which included the majority of the published data on smoking and cervical cancer, showed that smokers are at an increased risk of squamous cell carcinoma of the cervix.6 The OR for current smokers of 15 or more cigarettes per day was 1.98 (95% CI 1.78–2.21) as compared with never-smokers, after adjustment for study area, age, lifetime number of sexual partners, duration of oral contraceptive use, age at sexual debut and number of full-term pregnancies. Former smokers did not show a significant association with cervical cancer. The association between smoking and cervical cancer was confirmed when the analyses were restricted to HPV-positive women.6
Tobacco smoking could thus increase the risk of cervical cancer in more than one way, i.e. by increasing the probability of an HPV infection to become chronic, as well as its probability to become malignant.
Duration of smoking was not associated with HPV positivity in our study and this result is consistent with that found in the collaborative re-analysis on smoking and cervical cancer.6 The detection of a possible association between duration of smoking and HPV positivity is difficult mainly because women who have smoked for a long period of time are generally older and less sexually active than women who have smoked for a short period of time.
Interestingly, the effect of smoking seemed to be only temporary, as suggested also by the fact that in former smokers no association with cervical cancer risk was reported.6,27 Smoking cessation was also found to reduce early cervical abnormalities,56 thus further supporting the beneficial effect of smoking cessation on cervical cancer prevention.
In conclusion, this study showed that current, though not former, smoking was associated with an increased prevalence of HPV infection. This could be explained by the local immunosuppressive effect of smoking that could facilitate the establishment or persistence of HPV infections. However, our present results should be interpreted with caution, mainly because residual confounding by sexual behaviour is difficult to rule out and the dose–response relationship between smoking and HPV prevalence was clearly seen only among women who reported one lifetime sexual partner.
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Financial support was received from: the United Nations Development Programme/United Nations Population Fund/World Health Organization/World Bank Special Program of Research, Development and Research Training in Human Reproduction, Department of Reproductive Health and Research, World Health Organization, Switzerland (grant 94053A); the World Health Organization (Technical Services Agreement A15312 [GenBank] ); the Bill & Melinda Gates Foundation (grant number 35537); European Commission grant QLRT-1999-31238; the Swiss Bridge 2001 award; Piemonte Region, Italy; and the Spanish Ministry of Health (ISCIII, RCSP-09). The authors would like to thank Dr Keerti Shah (Department of Molecular Microbiology and Immunology, John Hopkins University School of Public Health, Baltimore, MD, USA) for HPV testing in the study from Mexico, and Ms Trudy Perdrix-Thoma for technical assistance.
Conflict of interest: None declared.
KEY MESSAGES
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In addition to the aforementioned, collaborators of the IARC HPV Prevalence Surveys (IHPS) Study Group include, in alphabetical order by country: Argentina (L Herrera, D Loria, M A Prince); Chile (A Luzoro, J M Ojeda, R Prado); Colombia (M Molano, M Ronderos); France (A Arslan, G M Clifford, M Plummer); Korea (D-H Lee); Mexico (M Hernández); Nigeria (A Omigbodun, K Ojemakinde, I Ajayi); Spain (X F Bosch, R Font); Thailand (V Kesararat, S Kongchuchuy, S Tunsakul); The Netherlands (M Jacobs); Vietnam (P T H Anh). 
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References |
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