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Article first published online: 3 NOV 2008
Published 2008 by the American Cancer Society
Supplement: Assessing the Burden of HPV-Associated Cancers in the United States
Volume 113, Issue Supplement 10, pages 2873–2882, 15 November 2008
How to Cite
Wu, X., Matanoski, G., Chen, V. W., Saraiya, M., Coughlin, S. S., King, J. B. and Tao, X.-G. (2008), Descriptive epidemiology of vaginal cancer incidence and survival by race, ethnicity, and age in the United States. Cancer, 113: 2873–2882. doi: 10.1002/cncr.23757
The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.
This is a US government work and, as such, is in the public domain in the United States of America.
- Issue published online: 3 NOV 2008
- Article first published online: 3 NOV 2008
- Manuscript Accepted: 15 MAY 2008
- Manuscript Received: 14 APR 2008
- Cooperative Agreement. Grant Number: U50 DP424071-04
- Centers for Disease Control and Prevention
- vaginal cancer;
- human papillomavirus;
Vaginal cancer is a rare malignancy. It has many of the same risk factors as cervical cancer, including a strong association with persistent human papillomavirus infection. Descriptive studies of the epidemiology of vaginal cancer are scarce in the literature.
The 1998 through 2003 incidence data from 39 population-based cancer registries were used, covering up to 83% of the US population. The 1996 through 2003 data from 17 cancer registries were used for survival analysis. Incidence rates, disease stage, and 5-year relative survival rates were calculated by race, ethnicity, and age group. Data analysis focused mainly on squamous cell carcinoma (SCC).
Incidence rates for all vaginal cancers combined were 0.18 per 100,000 female population for in situ cases and 0.69 for invasive cases. The median age of invasive cases was older than that of in situ cases (aged 68 years vs 58 years). SCC was the most common histologic type (71% of in situ cases and 66% of invasive cases). Compared with the rate for white women, the age-adjusted incidence rate of invasive SCC was 72% higher (P < .05) among black women, whereas the rate among Asian/Pacific Islander (API) women was 34% lower (P < .05). Hispanic women had a 38% higher rate than non-Hispanic women (P < .05) of invasive SCC. The rates for in situ SCC peaked at age 70 years and then declined, whereas the rates of invasive SCC increased continuously with advancing age. Black, API, and Hispanic women as well as older women were more likely to be diagnosed with late-stage disease, and these groups had lower 5-year relative survival rates than their white, non-Hispanic, and younger counterparts.
Incidence rates of vaginal SCC varied significantly by race, ethnicity, and age group. Black, API, and Hispanic women as well as older women had a high proportion of late-stage disease and a low 5-year survival rate. Cancer 2008;113(10 suppl):2873–82. Published 2008 by the American Cancer Society.
Vaginal cancer is a rare malignancy. There are approximately 1100 invasive vaginal cancers diagnosed annually in the United States, accounting for about 0.3% of all invasive cancers among women and for 1% to 2% of all gynecologic malignancies.1 Previous case-control and retrospective cohort studies have suggested that vaginal cancer, especially vaginal squamous cell carcinoma (SCC), which accounts for the majority of vaginal cancer cases, may have many of the same risk factors as cervical cancer, including a strong association with persistent human papillomavirus (HPV) infection.2–9 It has been reported that 40% of vaginal cancers could be attributed to HPV, and HPV type 16 (HPV-16) was detected in 50% to 64% of high-grade vaginal intraepithelial lesions.10–12
Although prevalence estimates of persistent oncogenic HPV infections are similar in cervical and vaginal specimens,13 incidence rates of cervical cancer are much higher than those of vaginal cancer around the world. A possible reason may be that the cervical transformation zone is more susceptible to persistent oncogenic HPV infection.12, 14 Although the natural history of vaginal cancer remains unclear, scientific evidence has indicated that this malignancy is preceded by its precursor, known as vaginal intraepithelial neoplasia (VAIN),15, 16 which is similar to cervical intraepithelial neoplasia.17 Because only a small proportion of women who are infected with oncogenic HPV develop vaginal cancer, additional factors, such as a previous history of anogenital cancer (especially cervical cancer), cigarette smoking, and decreased immune function, also may play a role in the progression from a precursor lesion to this malignacy.4, 6, 18
Data from the quadrivalent efficacy trials have produced some promising results for preventing vaginal precancerous lesions (VAIN grade 2 [VAIN-2]/VAIN-3).19 Among women who had not been infected with the vaccine types (HPV-16 or HPV-18), the vaccine was 100% effective against VAIN-2/VAIN-3. Overall, the vaccine was 49% (95% CI, 18-29) effective against VAIN-2/VAIN-3 associated with HPV-16 or HPV-18. In any effort to assess the effectiveness of HPV vaccine in populations, vaginal cancer incidence patterns, including VAIN-2/VAIN-3, need to be assessed. However, because of the rarity of this disease, there is a paucity in the literature of descriptive vaginal cancer epidemiology studies that use population-based cancer registry data. For the current study, we examined vaginal cancer age-specific and age-adjusted incidence rates (both in situ and invasive), disease stage at diagnosis, and 5-year relative survival rates by race, ethnicity, and age using a large, aggregated database from population-based cancer registries in the United States.
MATERIALS AND METHODS
These analyses were based on 2 sets of data. Cancer incidence and stage analyses were based on the 1998 through 2003 vaginal cancer incidence data from 39 population-based cancer registries that were participants in the Centers for Disease Control and Prevention's National Program of Cancer Registries (NPCR) and/or the National Cancer Institute's Surveillance, Epidemiology, End Results (SEER) Program.20 Data from these registries covered 83% of the US population and met the criteria of high-quality incidence data for inclusion in the United States Cancer Statistics (USCS) publication. Survival analysis was based on data from 1996 through 2003 in 17 SEER registries (Atlanta, Connecticut, Detroit, Hawaii, Iowa, New Mexico, San Francisco-Oakland, Seattle-Puget Sound, Utah, Los Angeles, San Jose-Monterey, Rural Georgia, and the Alaska Native Tumor Registry, Greater California, Kentucky, Louisiana, and New Jersey), which cover about 26% of the US population. Registries that participate in the SEER Program are the only source for population-based cancer survival data in the United States. All analyses by race included data for whites, blacks, and Asians/Pacific Islanders (APIs). American Indians and Alaska Natives were not included because of the large misclassification for this race group.21
This study included incident cases of in situ and invasive primary vaginal cancer (International Classification of Diseases for Oncology [ICD-O] site codes C52.9). Information on anatomic subsites of vaginal cancer was not available, because only 1 topographic code in the ICD-O manual is designated for vaginal cancer. VAIN-3 cases that were categorized as in situ in cancer registry data were not included, because they were not available in the analytic data file for most cancer registries. Lymphomas were excluded in conformance with the standard cancer site groups for cancer surveillance statistics in the United States. We also excluded approximately 2.8% of vaginal cancers that were not confirmed microscopically. We grouped vaginal cancers into the following histologic subtypes by using ICD-O (3rd edition) morphology codes: SCC, adenocarcinoma, other specified carcinomas, unspecified carcinomas, and noncarcinomas (eg, sarcoma).20 We combined all other specified histologic types together in the ‘other specified carcinomas’ category because of the small numbers of cases for those histologic types. Our analysis focused mainly on SCC, because this histologic type is associated with HPV infection more than other histologic types. Moreover, the small number of cases in the other histology categories did not allow in-depth analysis.
Vaginal cancers that were diagnosed from 1996 through 2000 were staged by using the 1977 SEER Summary Stage Manual (SS1977), whereas vaginal cancers that were diagnosed from 2001 through 2003 were staged according to the 2000 SEER Summary Stage Manual (SS2000).22, 23 According to the North American Association of Central Cancer Registries' assessment of the compatibility of SS1977 and SS2000, these 2 staging systems are not compatible for the regional- and distant-stage diseases of vaginal cancer.24 To make the stage data from different years comparable, we grouped vaginal cancer cases into 4 categories: in situ, localized, regional and distant, and unknown stage.
Frequency, age-specific incidence rates, and age-adjusted incidence rates were computed. All rates were presented per 100,000 female population. The 2000 US standard population was used for age-adjusted incidence rates. We calculated 95% confidence intervals according to the modification of Tiwari et al for age-adjusted incidence rates to assess the range of variation and stability.25 Incidence rate ratios and their modified 95% confidence intervals were calculated for rate comparisons.26 To facilitate stage comparisons, stage-specific, age-adjusted incidence rates were divided by overall age-adjusted incidence rates for each race, ethnicity, and age group to obtain age-adjusted stage distributions. Tests of significance for comparisons were at a level of P < .05. We included only first primary vaginal cancers for calculating 5-year relative survival rates.27 Vaginal cancer cases that were ascertained solely on the basis of a death certificate or that were diagnosed through an autopsy were excluded from the survival analysis. Rates based on fewer than 6 cases were suppressed except in the graphs. Data analyses were performed by using SEER*Stat software (version 6.2.4).
During the period from 1998 to 2003, in total, 1370 in situ vaginal cancers (VAIN-3 not included) and 5430 invasive vaginal cancers were diagnosed in the study areas, averaging 1133 cases per year. The majority of these cases were invasive (80%). Overall, the age-adjusted (2000 US) incidence rates of vaginal cancers combined were 0.18 per 100,000 women for in situ cases and 0.69 per 100,000 women for invasive cases (Table 1). The median age of women with invasive cancer (68 years) was older than that of women with in situ cancer (58 years). For invasive vaginal cancer, white women had the oldest median age (69 years), whereas API women had the youngest median age (63 years). The median age was older for women with invasive vaginal SCC (70 years) than for women with adenocarcinoma (65 years).
|Variable||Annual Average Incident Count‡||Percentage‡||Rate*||95% CI||Median Age, y|
|Other specified carcinoma||—**||—**||—**||—**||∼|
|Other specified carcinoma||28||3.1||0.02||(0.02-0.03)||60|
Of 1370 in situ vaginal cancers, 71% were SCC, and 27% were unspecified carcinoma; adenocarcinoma and noncarcinoma each accounted for about 1% of cases (Table 1). Of 5430 invasive vaginal cancers, 66% were SCC, 15% were adenocarcinoma, and 12% were noncarcinoma; each of the other specified carcinomas and unspecified carcinomas accounted for 3% to 4% of cases. Overall, the rates of vaginal SCC were 0.13 per 100,000 for in situ cases and 0.45 per 100,000 for invasive cases (Table 2).
|Variable||Annual Average Incident Count§||Percentage§||Rate*||95% CI||RR (95% CI)|
Differences in Incidence Rates of Vaginal SCC by Race, Ethnicity, and Age
Compared with the rate of invasive vaginal SCC among white women, the rate among black women was 72% higher (P < .05), whereas the rate among API women was 34% lower (P < .05) (Table 2). Hispanic women had a 38% higher rate of invasive vaginal SCC (P < .05) than non-Hispanic women. Unlike the rates of invasive vaginal SCC, the rates of in situ vaginal SCC were about the same among white women and black women, and the difference in the rates between Hispanic women and non-Hispanic women also was not statistically significant. The rates for in situ vaginal SCC increased with age until age 70 years; then, they declined, whereas the rates of invasive vaginal SCC increased continuously with advancing age (Fig. 1). For invasive vaginal SCC, the rate increases were more striking for black women than for white and API women, and the rates for Hispanic women were higher than the rates for non-Hispanic, white, and API women after age 60 years but lower than for black women, except those in their 70s. (Fig. 2).
Stage of Vaginal SCC by Race, Ethnicity, and Age
About 22% of vaginal SCC cases were diagnosed at the in situ stage and 35% were diagnosed at the localized stage (Table 3). Black and API women were more likely to be diagnosed with late-stage (regional and distant) disease than white women (40% and 52% vs 32%). Hispanic women also had a higher proportion of late-stage disease than non-Hispanic women (37% vs 33%). The percentage of late-stage vaginal SCC increased with advancing age. Among women aged ≥65 years, 35% had a late-stage disease, much higher than the 25% rate among women aged <50 years. The percentages of unstaged cases varied by race and age group. Black women and white women had higher percentages of unstaged cases than API women. Hispanic women had a higher percentage of unstaged cases than non-Hispanic women. With increasing age, the percentage of unstaged cases increased.
|Variable||R%||||Rate (95% CI)|
|In Situ¶||Localized||Reg & Dis||Unstaged||In Situ¶||Localized||Reg & Dis||Unstaged|
|All cases||22.4||34.5||32.8||10.3||0.13 (0.12-0.14)||0.20 (0.19-0.21)||0.19 (0.18-0.20)||0.06 (0.05-0.07)|
|White||23.2||33.9||32.1||10.7||0.13 (0.12-0.13)||0.19 (0.18-0.20)||0.18 (0.17-0.19)||0.06 (0.05-0.06)|
|Black||14.0||36.1||39.5||10.5||0.12 (0.10-0.15)||0.31 (0.27-0.35)||0.34 (0.29-0.38)||0.09 (0.07-0.12)|
|API||12.1||30.3||51.5||6.1||0.04 (0.02-0.08)||0.10 (0.06-0.15)||0.17 (0.12-0.23)||0.02 (0.00-0.40)|
|Non-Hispanic||22.4||34.5||32.8||10.3||0.13 (0.12-0.14)||0.20 (0.19-0.21)||0.19 (0.18-0.20)||0.06 (0.05-0.06)|
|Hispanic||15.1||32.9||37.0||15.1||0.11 (0.09-0.14)||0.24 (0.20-0.28)||0.27 (0.23-0.32)||0.11 (0.08-0.14)|
|<50||37.5||31.3||25.0||6.3||0.06 (0.06-0.07)||0.05 (0.05-0.06)||0.04 (0.04-0.05)||0.01 (0.01-0.01)|
|50-64||24.8||32.3||33.3||9.5||0.26 (0.23-0.29)||0.34 (0.30-0.37)||0.35 (0.31-0.38)||0.10 (0.08-0.12)|
|≥65||14.8||37.0||35.4||12.8||0.36 (0.32-0.40)||0.90 (0.85-0.96)||0.86 (0.81-0.92)||0.31 (0.28-0.34)|
Five-Year Survival Rate of Vaginal SCC by Race, Ethnicity, Age, and Stage
Overall, the combined 5-year relative survival rate for in situ and invasive vaginal SCC for cases diagnosed between 1996 and 2003 in the 17 SEER areas was 64% (Table 4). The 5-year relative survival rate of late-stage (regional and distant) vaginal SCC was 42%, which was substantially lower than the survival rates for in situ and localized vaginal SCC (96% and 76%, respectively) for all races and ethnicities combined. The 5-year relative survival rates for vaginal SCC varied markedly by race, ethnicity, and age. Overall, the 5-year relative survival rate was much higher for white women (66%) than for black women (55%) and API women (57%), but the rate was about the same for Hispanic women and non-Hispanic women (62% and 64%, respectively). Black women with in situ or localized vaginal SCC had a lower 5-year relative survival rate than white women and API women with the same stage of disease. Women aged ≥65 years had a lower 5-year relative survival rate than women aged <65 years with the same stage of disease.
|Variable||5-Year Relative Survival Rate, %|
|In Situ||||Localized||Regional and Distant||Unstaged||All Stage¶|
The current study provides a comprehensive description of vaginal cancer incidence patterns in the United States according to data from population-based cancer registries. We observed that incidence rates of invasive vaginal SCC varied by race and ethnicity. The variation may reflect racial and ethnic differences in oncogenic HPV infection and in other risk factors. The cross-sectional 2003 to 2004 National Health and Nutrition Examination Survey (NHANES) reported that non-Hispanic black women had 54% higher odds of infection with oncogenic HPV than non-Hispanic white women,29, 30 a finding consistent with the high incidence rates of vaginal SCC among black women compared with white women in this study. The NHANES data, however, demonstrated that the prevalence of oncogenic HPV infection was not higher among Hispanic women than among non-Hispanic white women and the prevalence of oncogenetic HPV infection among Mexican-American women was significantly lower than that among non-Hispanic white women, a finding inconsistent with the higher vaginal SCC incidence rates among Hispanics than among non-Hispanics observed in this study.30
Other factors that have been associated with the risk of vaginal cancer include low socioeconomic status, multiple sex partners, a family history of anogenital cancer, marital status, and cigarette smoking.4, 18 Apparently, most of these factors increase the risk of vaginal cancer through high exposure to oncogenic HPV infection. Women with histories and/or family histories of anogenital cancers had an increased risk for vaginal cancer, which also may be related to the finding that anogenital cancers have similar risk factors, and family members share similar environmental exposure or sexual behavior.18, 31 It is not clear what role genetic factors play in the development of vaginal cancer. Although smoking has been associated with vaginal cancer in several studies,4, 6, 11, 32 the mechanism of how smoking induces the development of vaginal cancer is not well understood. Previous studies suggest that nicotine may block apoptosis and suppress the immune system, possibly promoting the development of vaginal cancer.33–35 It is unknown whether there is synergism between cigarette smoking and HPV infection in the development of vaginal cancer, as there is for cervical cancer.36 Because of the limited literature about HPV prevalence and other risk factors in API women, it is not clear why the incidence rate of vaginal SCC was lower among API women than among women of other races.
Incidence rates of invasive vaginal SCC increased with advancing age in all racial and ethnic groups in this study. Compared with cervical cancer, vaginal cancer is more likely to occur among older women.2 The median age for invasive cervical cancer was 47 years19; whereas, in our study, the median age for invasive vaginal cancer was 68 years. Little is known about the age-related etiology of vaginal SCC. Previous reports indicate that up to 30% of women with vaginal cancer have a previous history of anogenital malignancies.4, 37 Women with cervical cancer who survive for ≥2 months have a 16-fold risk of subsequent vaginal cancer.38 Existing evidence suggests that radiation treatment for other anogenital disorders or malignancies may induce the development of vaginal cancer at least 10 years after the treatment.4, 39, 40 Regarding the relation between prior hysterectomy and an increased risk of vaginal cancer, it is believed that the risk may be related to previous HPV-associated anogenital diseases that led to the surgery, which reported are more frequent among women with vaginal cancer.41 Another reason for an older age diagnosis of vaginal cancer may be because of misclassifying the recurrence of cervical cancer as vaginal cancer when a metastatic lesion of the cervix is attributable to the vagina.2
Our data show that incidence rates of in situ vaginal SCC were about the same for white and black women as well as for Hispanic and non-Hispanic women. In contrast, the rates for invasive cancer were higher among black women than white women and were higher among Hispanic women than non-Hispanic women. These observations may indicate that the incidence pattern of in situ lesions is not the same as that of invasive lesions. One of the explanations could be that many in situ lesions among black and Hispanic women were not diagnosed until they progressed to invasive lesion, because black and Hispanic women were less likely to have regular sources of medical care and healthcare coverage than white women.42, 43 The current study also indicated that the relative percentage of in situ cases was much lower among black women than among white women and much lower among Hispanic women than among non-Hispanic women. It is not clear whether there are other factors influencing the transformation from in situ to invasive vaginal SCC. Nevertheless, investigators need to proceed with caution when using incidence counts and rates of in situ vaginal SCC to predict results of HPV vaccine effectiveness, especially when VAIN-3, 1 type of vaginal in situ cancer, is not defined, collected, or reported consistently.
Our data also indicate that API women had the highest percentage of late-stage vaginal SCC among all racial groups. Along with the lack of regular sources of care and health insurance coverage among API women, who have a high risk of anogenital cancers, linguistic and cultural differences also may contribute to the high percentage of late-stage disease among API women.44, 45 The 2000 National Health Interview Survey data indicated that Asian women had the lowest percentage of Papanicolaou (Pap) tests in the past 3 years compared with white, black, and Hispanic women (66% vs 82%, 84%, and 77%, respectively).46 Although the Pap test is used mainly for the early detection of cervical cancer, Pap test use in populations may indicate whether women have routine pelvic examinations, because the Pap test and routine pelvic examination often are performed at the same time. Having routine pelvic examinations may lead to an early diagnosis of vaginal cancer. The detection of precancerous lesions of the cervix may lead to a more thorough colposcopy, which may result in an early diagnosis of vaginal cancer.
Although vaginal cancer predominantly occurs among older women, these women were less likely than younger women to be diagnosed with early stages of the disease in the current study. It has been reported that women aged ≥65 years are less likely than their younger counterparts to receive a Pap test, although they are more likely to have access to medical care and health insurance coverage.47, 48 This phenomenon may be related to the uncertainty about the benefit of the Pap test at older ages, especially for women with normal Pap tests in previous screenings.49, 50
Our study also revealed that, within the same stage of vaginal SCC, 5-year relative survival rates were lower among black women than among white women, and they were lower among older women than among younger women. This may be related to the care received by patients with vaginal cancer. Although information on vaginal cancer treatment by race, ethnicity, and age is not available in the literature, the 2005 National Health Disparities Report indicated that there are disparities in all aspects of healthcare by race and ethnicity.51 Lower 5-year relative survival rates among older women than among young women also may be related to high comorbidity among older women. Older age alone may have an impact on decisions to withhold certain types of cancer treatment.52
Several limitations of this study should be noted. First, the actual incidence rates of vaginal SCC may be higher than what we presented because of several factors. First, we included only vaginal cancer cases that were confirmed microscopically. Second, according to SEER and the Facility Oncology Registry Data Standard coding rules, if a patient is diagnosed with multiple lesions of the cancer in more than 1 of the female genital organs (ie, vulva, vagina, other specified female genital organs, and unspecified female genital organs), then only a single cancer is counted. However, coding manuals for the years covered by the current study do not specify which site should be counted.53 It is possible that some of the vaginal lesions were coded as a nonvaginal site for the latter reason. Third, there were 27% of in situ and 4% of invasive vaginal cancers coded as an unspecified carcinoma in the study data file; some of these cases may be SCC. Large proportions of nonspecific vaginal carcinomas also may have an impact on the accuracy of incidence rates. In addition, VAIN-3 cases were not included in this study, because they were not available for the NPCR registries in the study data file. In the United States, data on VAINs have not been collected in any systematic fashion. According to the American College of Surgeons Commission on Cancer's (COC) guideline, VAIN-3 is no longer reportable for diagnoses after January 1, 1996.54 Because of that ruling, COC hospitals may not collect VAIN-3 cases unless their state cancer registries enforced a state law to collect them. Because of concerns about incompleteness of VAIN-3 reporting, cancer registries were not required to submit VAIN-3 cases for the NPCR data submission, which was the source of data used for the current study. In situ and VAIN-3 are considered the same disease by some pathologists. VAIN-3 has the same behavior code as in situ cases. Incompleteness of VAIN-3 cases in data from population-based cancer registries diminished our ability to measure the impact of the HPV vaccine, because VAIN-3 lesions typically occur at earlier ages, and data on VAIN-3 would have allowed us to measure the potential impact of the HPV vaccine at an earlier stage of vaginal cancer development. Finally, because information on the histories of cervical cancer, hysterectomy, or radiation of patients before vaginal cancer diagnoses either was not available or was incomplete for vaginal cancer cases in this study, we were not able to present the data in such patients.
Despite these limitations, the current study contributes not only to our knowledge about this rare malignancy, but it also provides baseline data on vaginal cancer epidemiology before the introduction of the HPV vaccine. Although the public health burden of vaginal cancer is relatively small, measures to prevent infection of higher risk types with HPV, such as HPV vaccination and reducing risky sexual practices (eg, reduction in numbers of sexual partners), combined with avoidance of cigarette smoking, could prevent many cases of vaginal cancer in the United States. Other potential measures to prevent vaginal cancer may include having vaginal examinations at the time women are screened for other gynecologic problems, especially for those women who have histories of cervical dysplasia or malignancy. For more information on vulvar cancers, please visit www.cdc.gov/cancer/gynecologic accessed on July 24, 2008.
- 5Relationship between human papillomavirus infection and tumours of anogenital sites other than the cervix. In: MunozN,BoschFX,ShahKV,MeheusA, eds. The Epidemiology of Human Papillomavirus and Cervical Cancer (IARC Scientific Publication No. 119). Lyon, France: IARC; 1992: 223–241., .
- 19Efficacy of a quadrivalent prophylactic human papillomavirus (types 6, 11, 16, and 18) L1 virus-like-particle vaccine against high-grade vulval and vaginal lesions: a combined analysis of three randomised clinical trials. Lancet. 2007; 369: 1693–1702., , , et al.
- 22YoungJJ,RoffersS,RiesL,FritzA,HurlbutA, eds. SEER Summary Staging Manual—2000: Codes and Coding Instructions. National Cancer Institute. NIH Publication No. 01-4969, Bethesda, Md: National Cancer Institute; 2001.
- 23Surveillance, Epidemiology, and End Results Program. Extent of Disease: Code and Coding Instructions. Bethesda, Md: National Institutes of Health, National Cancer Institute; 1977.
- 26Cancer Incidence in Five Continents. Vol VIII. Lyon, France: International Agency for Research on Cancer; 2002., , , , , .
- 27SEER Program Self-Instructional Manual for Cancer Registrars. Book 7: Statistics and Epidemiology for Cancer Registrars. National Cancer Institute. NIH Publication No.94-3766. Bethesda, Md: National Institutes of Health; 1994., , , , , .
- 28Population Projections of the United States by Age, Sex, Race, and Hispanic Origin: 1995 to 2050, US Bureau of the Census, Current Population Reports, P25-1130. Washington, DC: US Government Printing Office; 1996..
- 38Chapter 8: new malignancies following cancer of the cervix uteri, vagina, and vulva. In: CurtisRE,FreedmanDM,RonE, et al, eds. New Malignancies Among Cancer Survivors: SEER Cancer Registries, 1973-2000. National Cancer Institute. NIH Publication No. 05-5302. Bethesda, Md: National Cancer Institute; 2006., , .
- 46U.S. Department of Health and Human Services. 2004 National Healthcare Disparities Report. Rockville, Md: Agency for Healthcare Research and Quality; 2004.
- 50US Preventive Services Task Force. Cervical Cancer—Screening. Release date, January 2003. Available at: http//www.ahrq.gov/clinic/uspstf/uspscerv.htm. Accessed July 30, 2007.
- 53SEER. The SEER Program Code Manual, 3rd ed, revision 1 (updated January 2003). NIH Publication No. 98-1999. Bethesda, Md: National Institutes of Health, National Cancer Institute; 1998.
- 54HavenerL,HultstromD, eds.Standard for Cancer Registries Volume II: Data Standard and Data Dictionary, 11th ed, version 11.1. Springfield, Ill: North American Association of Central Cancer Registries; 2006.