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Coverage of Cervical Cancer Screening in 57 Countries: Low Average Levels and Large Inequalities

Coverage of Cervical Cancer Screening in 57 Countries: Low Average Levels and Large Inequalities

  • Emmanuela Gakidou, 
  • Stella Nordhagen, 
  • Ziad Obermeyer
PLOS
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Cervical cancer is the second most common cancer in women and a leading cause of mortality worldwide, with 273,000 deaths estimated in 2002 [1]. Eighty-three percent of cases occur in the developing world, where cervical cancer accounts for 15% of female cancers, as compared to just 3.6% in developed countries [1].

In the 1960s and 1970s, incidence rates in high-income countries were similar to those seen in the developing world today; the subsequent decline in cervical cancer incidence and mortality in high-income countries is largely credited to effective screening programs [2–11]. Considerable debate has arisen about whether such strategies are feasible and cost-effective in the developing world, where most cervical cancer now occurs [12–16].

Country-level data on current levels of screening provide important input into the debate on global cervical cancer policy planning. While there has been extensive research on rates of screening in the United States and other industrialized nations [17–22], data from the developing world are limited to a few countries and sub-national surveys [14,23–27]. In addition, the magnitude of inequalities in screening is virtually unknown in all but a few countries [28–30]. Differences in current levels of access to screening may have implications for designing screening and prevention strategies, particularly given novel approaches for screening and treatment in low-income settings [31–38], as well as for the development and delivery of a vaccine against the strains of human papillomavirus (HPV) that cause cervical cancer [39–52]. While cervical cancer programs also require human resources and laboratory infrastructure, the World Health Organization has identified screening coverage as a crucial component of providing effective prevention [53]. It is also the component of programs least amenable to purely financial solutions, unlike purchasing equipment, training employees, or ensuring laboratory quality control.

Summary Points

  • The large declines in cervical cancer mortality in developed countries have been attributed to widespread screening, but it is unclear whether this success can be replicated in the developing world.
  • It is generally assumed that screening coverage in the developing world is low; in this paper we substantiate this claim with evidence from 57 countries, thus contributing to the evidence base for formulation of effective policies.
  • Our analysis of population-based surveys indicates that coverage of cervical cancer screening in developing countries is on average 19%, compared to 63% in developed countries, and ranges from 1% in Bangladesh to 73% in Brazil.
  • Older and poor women, who are at the highest risk of developing cervical cancer, are least likely to be screened.
  • Strategies for improving cervical cancer prevention must be adapted to meet the specific needs of individual countries: expanded screening may be a viable option where sufficient infrastructure and health system access exists, but novel strategies need to be considered in other settings.

In this paper we present estimates of the average level and inequalities in cervical cancer screening from 57 countries across all levels of economic development included in the World Health Surveys (WHS), a set of household surveys implemented by the World Health Organization in 2002 [54]. More details on the surveys are provided in Table S1. We define the population eligible for screening as women aged 25 to 64, although Figure S1 shows that our results are robust across definitions of the eligible population. We show results for two measures: (1) crude coverage, which we define as the proportion of eligible women who report that they have had a pelvic exam (regardless of when the exam occurred), and (2) effective coverage, which we define as the proportion of eligible women who report that they have had a pelvic exam and Pap smear in the past three years. We calculate coverage by global wealth deciles, which are comparable across countries, as well as by a relative wealth index specific to each individual country. More specific details of the parameters and methods used for this analysis are provided in Text S1.

For the majority of these countries, these data represent the only information available on coverage of cervical cancer screening. This analysis points to an acute shortage of cervical cancer prevention services across much of the developing world and striking inequalities in access to these services, highlighting the need for new prevention and treatment strategies.

Our Findings

Figure 1 shows levels of coverage of cervical cancer screening for the 57 countries, and Table 1 summarizes these results. The population-weighted means of crude coverage and effective coverage of cervical cancer screening across all included countries are 68% and 40%, respectively. In the 30 developing countries surveyed, these rates are much lower: 45% and 19%, respectively. (Former communist countries are considered developed for purposes of this analysis.) There is wide variation in the level of effective coverage across countries, from over 80% in Austria and Luxembourg to 1% or less in Bangladesh, Ethiopia, and Myanmar. In many countries, a large proportion of women have had pelvic examinations, but the exam was not accompanied by laboratory tests or was not done in the three years preceding the survey. In Georgia, for example, 67% of women have had a pelvic exam, but only 11% had had one in the preceding three years and accompanied by a Pap smear; likewise in China, crude coverage is 70%, but effective screening coverage is only 23%. (Estimates of coverage by age group and wealth quintile for all included countries are provided in Table S2.)

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Figure 1. Crude and Effective Cervical Cancer Screening Coverage for Women Ages 25–64

https://doi.org/10.1371/journal.pmed.0050132.g001

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Table 1. Crude and Effective Cervical Cancer Screening Coverage across Development Groups for Women Ages 25–64 (With 95% Confidence Intervals)

https://doi.org/10.1371/journal.pmed.0050132.t001

In a large number of countries the majority of women have never had a pelvic exam. This proportion is largest in Malawi, Ethiopia, and Bangladesh, where more than 90% of women report that they have never had a pelvic exam. In 16 of the 57 countries analyzed, more than half of eligible women had never had a pelvic exam. Figure 1 also demonstrates that the relationship between the proportion of women ever having a pelvic exam and the proportion effectively screened is not uniform. Even among high-income countries, which have crude coverage rates at or above 90%, the proportion of women who are effectively screened varies widely.

Figure 2 shows crude and effective coverage of cervical cancer screening across age groups for developed and developing countries. While the age pattern of crude and effective coverage is similar across level of development, coverage is markedly lower in developing countries. Crude and effective coverage rates begin to decline for women over 45 years of age in developing countries and over 55 years of age in developed countries. The age group at which the declines in effective coverage are observed corresponds with the age at which incidence rates and mortality from cervical cancer have been shown to rise sharply [53].

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Figure 2. Coverage of Cervical Cancer Screening, By Age Group, Across Two Development Groups

https://doi.org/10.1371/journal.pmed.0050132.g002

Figure 3 shows that considerable inequalities in crude and effective coverage of cervical cancer screening exist across global wealth deciles. While the average crude screening rate across the set of countries in the analysis was 68%, only 31% of women in the poorest global wealth decile have ever had a pelvic exam, compared to 91% of women in the richest global wealth decile. The inequalities are even more pronounced for effective coverage of cervical cancer screening, with the poorest women being nearly seven times less likely to have been screened effectively compared to their rich counterparts (9% and 64%, respectively). Even though crude coverage rates are high for women in the richest wealth deciles, effective coverage rates are overall very low: all wealth deciles except the wealthiest have effective coverage rates of lower than 60%, and effective coverage of cervical cancer screening is at or below 10% in the poorest three deciles.

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Figure 3. Cervical Cancer Screening Coverage, By Global Wealth Decile, Across All Countries

https://doi.org/10.1371/journal.pmed.0050132.g003

In addition to inequalities across countries, significant wealth-related inequalities also exist within countries. Figure 4 demonstrates inequalities between the poorest and richest quintiles in crude and effective screening coverage for Brazil, China, Germany, and India, four of the most populous countries included in the WHS. We present results using a within-country relative wealth index; while not directly comparable across countries, it is more relevant for within-country inequalities. In India, the rates of coverage are very low for rich and poor women alike. While crude coverage for rich women is higher (36% compared to 22% for poor women), effective coverage for cervical cancer screening is uniformly low, 6% and 4% respectively. By contrast, wealth-related inequalities are very pronounced for both crude and effective coverage in China and Brazil. In Germany, as in several other high-income countries, crude coverage rates are uniformly high, and therefore wealth-related inequalities are mainly observed for effective coverage of cervical cancer screening.

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Figure 4. Cervical Cancer Screening Coverage in Top and Bottom Within-Country Wealth Quintiles, Across Four Selected Countries

https://doi.org/10.1371/journal.pmed.0050132.g004

Policy Implications

The results of this study illustrate that a wide range of current screening practices exists across countries; this makes it unlikely that any one strategy will prove to be effective globally. Choices regarding cervical cancer prevention strategies must be adapted to the current situation and the constraints of individual countries—indeed, multiple strategies may need to be pursued within the same country. In this regard, it may be useful to consider countries in three broad groups, based on current screening coverage rates, each facing different policy choices with regard to cervical cancer prevention.

In developed countries, where high rates of effective coverage have been achieved, focusing on the subgroups of women who are not effectively screened may be a reasonable and cost-effective strategy. It is likely that HPV vaccination would lead to some health gains in these countries; however, the benefits of this strategy should be weighed against its substantial costs.

In some middle-income and former communist countries, a majority of women have had pelvic exams in their lifetime; however, rates of effective screening (i.e., a recent exam accompanied by laboratory tests) are low. This indicates that a large proportion of women in these countries have contact with obstetric or gynecologic health services, and that the health system may have the capacity to provide effective screening to a larger number of women. In these countries, it may be possible to build on “missed opportunities”—pelvic exams without laboratory tests or of insufficient frequency—to increase coverage without significant investment in health infrastructure. “Organized” programs, with systematic call, recall, follow-up, and surveillance, hold promise in this regard [13] and could be implemented in the context of existing health services.

This study also identifies a number of countries where the vast majority of women have never had a pelvic exam. In such settings, where the health system is unable to provide even low levels of crude coverage of this basic intervention, improved screening is clearly urgent, especially for women aged over 35 years. Visual inspection with acetic acid has recently shown promise as an appealing alternative to cytological examination in low-income settings: overall cost is lower, and women in need of further intervention can be identified immediately rather than after laboratory results are obtained [55]. It is also clear that improving women's access to the health system should be a high priority, as contact with the health system is a prerequisite for any screening program to succeed.

More radical solutions, however, may be needed, particularly for this latter group of countries. The availability of a vaccine for HPV offers one such solution. Vaccination places considerably fewer logistical demands on a health system than repeated screening, testing, and treatment of precursor lesions. In addition, it may be easier to reach younger women than to systematically screen older women, who are at the highest risk of developing cervical cancer. In some of these countries, for example the Philippines, where school enrolment rates are relatively high, vaccination programs could be implemented in the context of the education system. Such an approach would be substantially less expensive and easier to implement than delivering the vaccine through door-to-door approaches or through primary health care, where population coverage levels are likely to be low. Donors may also be more prepared to pay for targeted interventions like vaccines, which can easily be implemented through vertical programs. Finally, it is possible that vaccination may be more culturally acceptable than vaginal examination in some cultures with the lowest rates of coverage.

However, the benefits of the vaccine must be weighed against its limitations as a prevention strategy as well as its considerable cost. Vaccination will not have an impact for many years, as it has to be directed to adolescents before the onset of sexual activity. The immediate need for cervical cancer screening and control in many developing countries suggests that there should be greater emphasis on strategies to reach women aged 35 or over, while alternatives are being considered and explored. The current version of the HPV vaccine protects against the two strains most commonly implicated in cervical cancer. Since the vaccine is projected to prevent the majority of, but not all, cervical cancer cases, screening will likely still need to be recommended for vaccinated women. There is also the possibility that a new emphasis on a vaccine would divert resources and attention—at the policy level as well as for individual women—from screening [38].

In addition, the cost of purchasing the vaccine may be significant. A recent study showed that vaccination and three screening visits would be very cost-effective, assuming a total cost of vaccination of US$25 per woman.[56]. However, the current cost of the vaccine is very far from this projection: while there may be opportunities for international programs to negotiate discounts through mass purchasing [57,58], the current price of US$300–US$400 per course [59,60] may be prohibitive. Indeed, the real cost may be higher, since women would need to be reached multiple times in order to deliver each dose of a multiple-dose course [56] and since cold-chain infrastructure is currently required. Since vaccination does not obviate the need for screening, the financial burden of both strategies may be too high for already strained health systems to bear. An addition consideration to keep in mind, highlighted by the recent controversy over the vaccine in the US [61], is that vaccinating women against a sexually transmitted infection is by no means universally culturally accepted.

Finally, this study also highlights the urgent need for better monitoring of cervical cancer screening and control and for in-depth evaluations of current strategies implemented in various countries, so that the evidence base of what works and what does not can be strengthened. Questions on preventive services, including cervical cancer and breast cancer screening, are often not included in national health surveys in developing countries, thus resulting in a weak global evidence base for cervical cancer screening and control. The World Health Surveys, which were used in this analysis, have several limitations. First, among the limitations of self-reported data is the fact that, for questions on cervical cancer screening, it is difficult to know with certainty whether we are measuring the coverage of a pelvic exam in the context of obstetric or gynecologic care or a screening test for cancer. Also, while it is likely that women would remember a pelvic exam, our estimates of effective coverage are limited by the ability of women to report whether a laboratory test (i.e., a Pap smear) was performed in the context of the pelvic exam. Since it is possible that a number of women were not informed, did not understand, or did not report this test, our numbers may represent a low estimate of effective coverage. It is also possible that women do not report accurately on the timing of the vaginal exam and that our estimates of crude coverage are underestimates, if women do not report vaginal exams that were performed several years before the survey.

We have attempted to correct for bias from missing data by applying a multiple imputation method; however, this technique may not adequately address all the bias in the WHS data. Despite these limitations, the WHS provide the first opportunity to estimate cervical cancer screening rates and inequalities across a large set of developing and developed countries. The findings presented in this paper provide a solid starting point, while highlighting the need to improve the quality and the frequency of monitoring of cervical cancer screening and control efforts worldwide.

Conclusion

Effective coverage rates for cervical cancer screening services are very low outside of developed countries, and women at the highest risk of developing cervical cancer are among the least likely to be screened. Coverage rates decline with advancing age, when cervical cancer incidence rates are the highest. Poor women, who likely have higher exposure to known cervical cancer biological risk factors such as smoking and unsafe sex [62], also show much lower coverage rates. Improving the effective coverage of cervical cancer screening or developing alternative ways to decrease cervical cancer mortality worldwide would have a considerable impact on decreasing the disease's burden as well as overall health inequalities. No one strategy will work everywhere, making it important to consider multiple strategies across—and likely within—countries.

Supporting Information

Figure S1. Comparison of proportion of women who have never had a pelvic examination and effective screening coverage between two age-based definitions of the screening-eligible population

https://doi.org/10.1371/journal.pmed.0050132.sg001

(13 KB PDF).

Table S1. Sample sizes and percentage of observations missing for eligible women ages 25–64 by WHS country

https://doi.org/10.1371/journal.pmed.0050132.st001

(7 KB PDF).

Table S2. Effective coverage and fraction of women who never had pelvic exam by age and wealth group for eligible women ages 25–64, by WHS country

https://doi.org/10.1371/journal.pmed.0050132.st002

(12 KB PDF).

Text S1. Description of the analytical methods used

https://doi.org/10.1371/journal.pmed.0050132.sd001

(43 KB DOC).

Author Contributions

EG, SN, and ZO designed the analytical framework. SN performed statistical analyses. EG, SN, and ZO drafted the manuscript. EG accepts full responsibility for the work and the conduct of the study, had access to the data, and controlled the decision to publish.

References

  1. 1. Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55: 74–108.DM ParkinF. BrayJ. FerlayP. Pisani2005Global cancer statistics, 2002.CA Cancer J Clin5574108
  2. 2. US Centers for Disease Control and Prevention (2006) 2006/2007 National Breast and Cervical Cancer Early Detection Program fact sheet. US Centers for Disease Control and Prevention20062006/2007 National Breast and Cervical Cancer Early Detection Program fact sheet.Available: http://www.cdc.gov/cancer/nbccedp/about.htm. Accessed 7 May 2008. Available: http://www.cdc.gov/cancer/nbccedp/about.htm. Accessed 7 May 2008.
  3. 3. Gustafsson L, Ponten J, Zack M, Adami HO (1997) International incidence rates of invasive cervical cancer after introduction of cytological screening. Cancer Causes Control 8: 755–763.L. GustafssonJ. PontenM. ZackHO Adami1997International incidence rates of invasive cervical cancer after introduction of cytological screening.Cancer Causes Control8755763
  4. 4. Gustafsson L, Ponten J, Bergstrom R, Adami HO (1997) International incidence rates of invasive cervical cancer before cytological screening. Int J Cancer 71: 159–165.L. GustafssonJ. PontenR. BergstromHO Adami1997International incidence rates of invasive cervical cancer before cytological screening.Int J Cancer71159165
  5. 5. Breen N, Wagener DK, Brown ML, Davis WW, Ballard-Barbash R (2001) Progress in cancer screening over a decade: Results of cancer screening from the 1987, 1992, and 1998 National Health Interview Surveys. J Natl Cancer Inst 93: 1704–1713.N. BreenDK WagenerML BrownWW DavisR. Ballard-Barbash2001Progress in cancer screening over a decade: Results of cancer screening from the 1987, 1992, and 1998 National Health Interview Surveys.J Natl Cancer Inst9317041713
  6. 6. Koong SL, Yen AM, Chen TH (2006) Efficacy and cost-effectiveness of nationwide cervical cancer screening in Taiwan. J Med Screen 13(Suppl 1): 44–47.SL KoongAM YenTH Chen2006Efficacy and cost-effectiveness of nationwide cervical cancer screening in Taiwan.J Med Screen13Suppl 14447
  7. 7. Herbert A, Smith JH (2007) Women under 25 should be offered screening. BMJ 334: 273.A. HerbertJH Smith2007Women under 25 should be offered screening.BMJ334273
  8. 8. Nygard JF, Skare GB, Thoresen SO (2002) The cervical cancer screening programme in Norway, 1992–2000: Changes in Pap smear coverage and incidence of cervical cancer. J Med Screen 9: 86–91.JF NygardGB SkareSO Thoresen2002The cervical cancer screening programme in Norway, 1992–2000: Changes in Pap smear coverage and incidence of cervical cancer.J Med Screen98691
  9. 9. Peto J, Gilham C, Fletcher O, Matthews FE (2004) The cervical cancer epidemic that screening has prevented in the UK. Lancet 364: 249–256.J. PetoC. GilhamO. FletcherFE Matthews2004The cervical cancer epidemic that screening has prevented in the UK.Lancet364249256
  10. 10. Symonds RP (2001) Is screening for cervical cancer effective. Clin Oncol (R Coll Radiol) 13: 473–475.RP Symonds2001Is screening for cervical cancer effective.Clin Oncol (R Coll Radiol)13473475
  11. 11. Farnsworth A, Mitchell HS (2003) Prevention of cervical cancer. Med J Aust 178: 653–654.A. FarnsworthHS Mitchell2003Prevention of cervical cancer.Med J Aust178653654
  12. 12. Bermudez A (2005) Can we do the same in the developing world. Gynecol Oncol 99: S192–S196.A. Bermudez2005Can we do the same in the developing world.Gynecol Oncol99S192S196
  13. 13. Sankaranarayanan R, Buldukh AM, Rajkumar R (2001) Effective screening programmes for cervical cancer in low- and middle-income developing countries. Bull World Health Organ 79: 954–962.R. SankaranarayananAM BuldukhR. Rajkumar2001Effective screening programmes for cervical cancer in low- and middle-income developing countries.Bull World Health Organ79954962
  14. 14. Bradley J, Barone M, Mahe C, Lewis R, Luciani S (2005) Delivering cervical cancer prevention services in low-resource settings. Int J Gynaecol Obstet 89: S21–S29.J. BradleyM. BaroneC. MaheR. LewisS. Luciani2005Delivering cervical cancer prevention services in low-resource settings.Int J Gynaecol Obstet89S21S29
  15. 15. Denny L (2005) The prevention of cervical cancer in developing countries. BJOG 112: 1204–1212.L. Denny2005The prevention of cervical cancer in developing countries.BJOG11212041212
  16. 16. Pollack AE, Tsu VD (2005) Preventing cervical cancer in low-resource settings: Building a case for the possible. Int J Gynaecol Obstet 89: S1–S3.AE PollackVD Tsu2005Preventing cervical cancer in low-resource settings: Building a case for the possible.Int J Gynaecol Obstet89S1S3
  17. 17. Garner EI (2003) Cervical cancer: Disparities in screening, treatment, and survival. Cancer Epidemiol Biomarkers Prev 12: 242s–247s.EI Garner2003Cervical cancer: Disparities in screening, treatment, and survival.Cancer Epidemiol Biomarkers Prev12242s247s
  18. 18. DeAlba I, Ngo-Metzger Q, Sweningson JM, Hubbell FA (2005) Pap smear use in California: Are we closing the racial/ethnic gap. Prev Med 40: 747–755.I. DeAlbaQ. Ngo-MetzgerJM SweningsonFA Hubbell2005Pap smear use in California: Are we closing the racial/ethnic gap.Prev Med40747755
  19. 19. McDonald JT, Kennedy S (2007) Cervical cancer screening by immigrant and minority women in Canada. J Immigr Minor Health 9: 323–334.JT McDonaldS. Kennedy2007Cervical cancer screening by immigrant and minority women in Canada.J Immigr Minor Health9323334
  20. 20. Newmann SJ, Garner EO (2005) Social inequities along the cervical cancer continuum: A structured review. Cancer Causes Control 16: 63–70.SJ NewmannEO Garner2005Social inequities along the cervical cancer continuum: A structured review.Cancer Causes Control166370
  21. 21. Yabroff KR, Lawrence WF, King JC, Mangan P, Washington KS, et al. (2005) Geographic disparities in cervical cancer mortality: What are the roles of risk factor prevalence, screening, and use of recommended treatment. J Rural Health 21: 149–157.KR YabroffWF LawrenceJC KingP. ManganKS Washington2005Geographic disparities in cervical cancer mortality: What are the roles of risk factor prevalence, screening, and use of recommended treatment.J Rural Health21149157
  22. 22. Hou SI, Lessick M (2002) Cervical cancer screening among Chinese women. AWHONN Lifelines 6: 349–354.SI HouM. Lessick2002Cervical cancer screening among Chinese women.AWHONN Lifelines6349354
  23. 23. Castro-Jimenez MA, Londono-Cuellar PA, Vera-Cala LM (2006) [Use and determinants of Pap smear in a rural Colombian municipality 1998–1999]. [Article in Spanish]. Rev Salud Publica (Bogota) 8: 248–257.MA Castro-JimenezPA Londono-CuellarLM Vera-Cala2006[Use and determinants of Pap smear in a rural Colombian municipality 1998–1999]. [Article in Spanish].Rev Salud Publica (Bogota)8248257
  24. 24. Kritpetcharat O, Suwanrungruang K, Sriamporn S, Kamsaard S, Kritpetcharat P, et al. (2003) The coverage of cervical cancer screening in Khon Kaen, northeast Thailand. Asian Pac J Cancer Prev 4: 103–105.O. KritpetcharatK. SuwanrungruangS. SriampornS. KamsaardP. Kritpetcharat2003The coverage of cervical cancer screening in Khon Kaen, northeast Thailand.Asian Pac J Cancer Prev4103105
  25. 25. Lin HH, Chen SH, Jeng SY, Chen HM (2007) [A project to improve the screening rate of pap smear for cervical cancer]. [Article in Chinese]. Hu Li Za Zhi 54: 62–69.HH LinSH ChenSY JengHM Chen2007[A project to improve the screening rate of pap smear for cervical cancer]. [Article in Chinese].Hu Li Za Zhi546269
  26. 26. Sriamporn S, Khuhaprema T, Parkin M (2006) Cervical cancer screening in Thailand: An overview. J Med Screen 13(Suppl 1): 39–43.S. SriampornT. KhuhapremaM. Parkin2006Cervical cancer screening in Thailand: An overview.J Med Screen13Suppl 13943
  27. 27. Winkler J, Bingham A, Coffey P, Handwerker WP (2007) Women's participation in a cervical cancer screening program in northern Peru. Health Educ Res 23: 10–24.J. WinklerA. BinghamP. CoffeyWP Handwerker2007Women's participation in a cervical cancer screening program in northern Peru.Health Educ Res231024
  28. 28. Baker D, Middleton E (2003) Cervical screening and health inequality in England in the 1990s. J Epidemiol Community Health 57: 417–423.D. BakerE. Middleton2003Cervical screening and health inequality in England in the 1990s.J Epidemiol Community Health57417423
  29. 29. Coughlin SS, King J, Richards TB, Ekwueme DU (2006) Cervical cancer screening among women in metropolitan areas of the United States by individual-level and area-based measures of socioeconomic status, 2000 to 2002. Cancer Epidemiol Biomarkers Prev 15: 2154–2159.SS CoughlinJ. KingTB RichardsDU Ekwueme2006Cervical cancer screening among women in metropolitan areas of the United States by individual-level and area-based measures of socioeconomic status, 2000 to 2002.Cancer Epidemiol Biomarkers Prev1521542159
  30. 30. Parikh S, Brennan P, Boffetta P (2003) Meta-analysis of social inequality and the risk of cervical cancer. Int J Cancer 105: 687–691.S. ParikhP. BrennanP. Boffetta2003Meta-analysis of social inequality and the risk of cervical cancer.Int J Cancer105687691
  31. 31. Tsu VD, Pollack AE (2005) Preventing cervical cancer in low-resource settings: How far have we come and what does the future hold. Int J Gynaecol Obstet 89: S55–S59.VD TsuAE Pollack2005Preventing cervical cancer in low-resource settings: How far have we come and what does the future hold.Int J Gynaecol Obstet89S55S59
  32. 32. Mandelblatt JS, Lawrence WF, Gaffikin L, Limpahayom KK, Lumbiganon P, et al. (2002) Costs and benefits of different strategies to screen for cervical cancer in less-developed countries. J Natl Cancer Inst 94: 1469–1483.JS MandelblattWF LawrenceL. GaffikinKK LimpahayomP. Lumbiganon2002Costs and benefits of different strategies to screen for cervical cancer in less-developed countries.J Natl Cancer Inst9414691483
  33. 33. Goldie SJ, Kuhn L, Denny L, Pollack A, Wright TC (2001) Policy analysis of cervical cancer screening strategies in low-resource settings: Clinical benefits and cost-effectiveness. JAMA 285: 3107–3115.SJ GoldieL. KuhnL. DennyA. PollackTC Wright2001Policy analysis of cervical cancer screening strategies in low-resource settings: Clinical benefits and cost-effectiveness.JAMA28531073115
  34. 34. Goldie SJ (2003) Chapter 15: Public health policy and cost-effectiveness analysis. J Natl Cancer Inst Monogr 31: 102–110.SJ Goldie2003Chapter 15: Public health policy and cost-effectiveness analysis.J Natl Cancer Inst Monogr31102110
  35. 35. Miller AB, Sankaranarayanan R, Bosch FX, Sepulveda C (2003) Can screening for cervical cancer be improved, especially in developing countries. Int J Cancer 107: 337–340.AB MillerR. SankaranarayananFX BoschC. Sepulveda2003Can screening for cervical cancer be improved, especially in developing countries.Int J Cancer107337340
  36. 36. Schiffman M, Castle PE (2005) The promise of global cervical-cancer prevention. N Engl J Med 353: 2101–2104.M. SchiffmanPE Castle2005The promise of global cervical-cancer prevention.N Engl J Med35321012104
  37. 37. Goldie SJ, Gaffikin L, Goldhaber-Fiebert JD, Gordillo-Tobar A, Levin C, et al. (2005) Cost-effectiveness of cervical-cancer screening in five developing countries. N Engl J Med 353: 2158–2168.SJ GoldieL. GaffikinJD Goldhaber-FiebertA. Gordillo-TobarC. Levin2005Cost-effectiveness of cervical-cancer screening in five developing countries.N Engl J Med35321582168
  38. 38. Katz IT, Wright AA (2006) Preventing cervical cancer in the developing world. N Engl J Med 354: 1110.IT KatzAA Wright2006Preventing cervical cancer in the developing world.N Engl J Med3541110
  39. 39. Steinbrook R (2006) The potential of human papillomavirus vaccines. N Engl J Med 354: 1109–1112.R. Steinbrook2006The potential of human papillomavirus vaccines.N Engl J Med35411091112
  40. 40. Adams M, Jasani B, Fiander A (2007) Human papilloma virus (HPV) prophylactic vaccination: Challenges for public health and implications for screening. Vaccine 25: 3007–3013.M. AdamsB. JasaniA. Fiander2007Human papilloma virus (HPV) prophylactic vaccination: Challenges for public health and implications for screening.Vaccine2530073013
  41. 41. Brinkman JA, Caffrey AS, Muderspach LI, Roman LD, Kast WM (2005) The impact of anti HPV vaccination on cervical cancer incidence and HPV induced cervical lesions: Consequences for clinical management. Eur J Gynaecol Oncol 26: 129–142.JA BrinkmanAS CaffreyLI MuderspachLD RomanWM Kast2005The impact of anti HPV vaccination on cervical cancer incidence and HPV induced cervical lesions: Consequences for clinical management.Eur J Gynaecol Oncol26129142
  42. 42. Crosbie EJ, Kitchener HC (2006) Human papillomavirus in cervical screening and vaccination. Clin Sci (Lond) 110: 543–552.EJ CrosbieHC Kitchener2006Human papillomavirus in cervical screening and vaccination.Clin Sci (Lond)110543552
  43. 43. Feeley C (2006) Advances in cervical cancer screening and human papillomavirus vaccines. J Br Menopause Soc 12: 19–23.C. Feeley2006Advances in cervical cancer screening and human papillomavirus vaccines.J Br Menopause Soc121923
  44. 44. Goldie SJ, Kohli M, Grima D, Weinstein MC, Wright TC, et al. (2004) Projected clinical benefits and cost-effectiveness of a human papillomavirus 16/18 vaccine. J Natl Cancer Inst 96: 604–615.SJ GoldieM. KohliD. GrimaMC WeinsteinTC Wright2004Projected clinical benefits and cost-effectiveness of a human papillomavirus 16/18 vaccine.J Natl Cancer Inst96604615
  45. 45. Gross G (2007) HPV-vaccination against cervical carcinoma: Will it really work. Med Microbiol Immunol 196: 121–125.G. Gross2007HPV-vaccination against cervical carcinoma: Will it really work.Med Microbiol Immunol196121125
  46. 46. Mahdavi A, Monk BJ (2005) Vaccines against human papillomavirus and cervical cancer: Promises and challenges. Oncologist 10: 528–538.A. MahdaviBJ Monk2005Vaccines against human papillomavirus and cervical cancer: Promises and challenges.Oncologist10528538
  47. 47. Monk BJ, Mahdavi A (2007) Human papillomavirus vaccine: A new chance to prevent cervical cancer. Recent Results Cancer Res 174: 81–90.BJ MonkA. Mahdavi2007Human papillomavirus vaccine: A new chance to prevent cervical cancer.Recent Results Cancer Res1748190
  48. 48. Monsonego J (2007) [Prevention of cervical cancer: Screening, progress and perspectives]. [Article in French]. Presse Med 36: 92–111.J. Monsonego2007[Prevention of cervical cancer: Screening, progress and perspectives]. [Article in French].Presse Med3692111
  49. 49. Raffle AE (1999) How long will screening myths survive. Lancet 354: 431–432.AE Raffle1999How long will screening myths survive.Lancet354431432
  50. 50. Raffle AE (2007) Human papillomavirus vaccine policy. Lancet 369: 367–368.AE Raffle2007Human papillomavirus vaccine policy.Lancet369367368
  51. 51. Roden R, Monie A, Wu TC (2006) The impact of preventive HPV vaccination. Discov Med 6: 175–181.R. RodenA. MonieTC Wu2006The impact of preventive HPV vaccination.Discov Med6175181
  52. 52. Roden R, Wu TC (2006) How will HPV vaccines affect cervical cancer. Nat Rev Cancer 6: 753–763.R. RodenTC Wu2006How will HPV vaccines affect cervical cancer.Nat Rev Cancer6753763
  53. 53. World Health Organization (2006) Comprehensive cervical cancer control: A guide to essential practice. World Health Organization2006Comprehensive cervical cancer control: A guide to essential practice.Available: http://www.who.int/reproductive-health/publications/cervical_cancer_gep/index.htm. Accessed 7 May 2008. Available: http://www.who.int/reproductive-health/publications/cervical_cancer_gep/index.htm. Accessed 7 May 2008.
  54. 54. World Health Organization (2007) World Health Surveys. World Health Organization2007World Health Surveys.Available: http://surveydata.who.int/index.html. Accessed 7 May 2008. Available: http://surveydata.who.int/index.html. Accessed 7 May 2008.
  55. 55. Sankaranarayanan R, Esmy PO, Rajkumar R, Muwonge R, Swaminathan R, et al. (2007) Effect of visual screening on cervical cancer incidence and mortality in Tamil Nadu, India: A cluster-randomised trial. Lancet 370: 398–406.R. SankaranarayananPO EsmyR. RajkumarR. MuwongeR. Swaminathan2007Effect of visual screening on cervical cancer incidence and mortality in Tamil Nadu, India: A cluster-randomised trial.Lancet370398406
  56. 56. Goldie SJ, Kim JJ, Kobus K, Goldhaber-Fiebert JD, Salomon J, O'Shea MKH, Bosch FX, de Sanjose S, Franco EL (2007) Cost-effectiveness of HPV 16, 18 vaccination in Brazil. Vaccine 25: 6257–6270.SJ GoldieJJ KimK. KobusJD Goldhaber-FiebertJ. SalomonMKH O'SheaFX BoschS. de SanjoseEL Franco2007Cost-effectiveness of HPV 16, 18 vaccination in Brazil.Vaccine2562576270
  57. 57. Levine R, England S, Mitchell V (2007) Immunization financing options: A resource for policymakers. GAVI Financing Task Force. R. LevineS. EnglandV. Mitchell2007Immunization financing options: A resource for policymakers. GAVI Financing Task Force.Available: http://www.who.int/immunization_delivery/new_vaccines/15.briefcase_web.pdf. Accessed 7 May 2008. Available: http://www.who.int/immunization_delivery/new_vaccines/15.briefcase_web.pdf. Accessed 7 May 2008.
  58. 58. Matiru R, Ryan T (2007) The Global Drug Facility: A unique, holistic and pioneering approach to drug procurement and management. Bull World Health Organ 85: 348–353.R. MatiruT. Ryan2007The Global Drug Facility: A unique, holistic and pioneering approach to drug procurement and management.Bull World Health Organ85348353
  59. 59. Brisson M, Van de Velde N, De Wals P, Boily MC (2007) The potential cost-effectiveness of prophylactic human papillomavirus vaccines in Canada. Vaccine 25: 5399–5408.M. BrissonN. Van de VeldeP. De WalsMC Boily2007The potential cost-effectiveness of prophylactic human papillomavirus vaccines in Canada.Vaccine2553995408
  60. 60. Kulasingam S, Connelly L, Conway E, Hocking JS, Myers E, et al. (2007) A cost-effectiveness analysis of adding a human papillomavirus vaccine to the Australian National Cervical Cancer Screening Program. Sexual Health 4: 165–175.S. KulasingamL. ConnellyE. ConwayJS HockingE. Myers2007A cost-effectiveness analysis of adding a human papillomavirus vaccine to the Australian National Cervical Cancer Screening Program.Sexual Health4165175
  61. 61. Blumenthal R (2007 April 26) Texas legislators block shots for girls against cancer virus. The New York Times. R. Blumenthal2007 April 26Texas legislators block shots for girls against cancer virus. The New York Times.Available: http://www.nytimes.com/2007/04/26/us/26texas.html. Accessed 7 May 2008. Available: http://www.nytimes.com/2007/04/26/us/26texas.html. Accessed 7 May 2008.
  62. 62. Chichareon S, Herrero R, Munoz N, Bosch FX, Jacobs MV, et al. (1998) Risk factors for cervical cancer in Thailand: A case-control study. J Natl Cancer Inst 90: 50–57.S. ChichareonR. HerreroN. MunozFX BoschMV Jacobs1998Risk factors for cervical cancer in Thailand: A case-control study.J Natl Cancer Inst905057