Abstract

METHODS

Newly diagnosed cancers of the uterus and ovary from 1999 through 2009 were identified from the population-based central cancer registries participating in the Centers for Disease Control and Prevention’s National Program of Cancer Registries and the National Cancer Institute’s Surveillance, Epidemiology, and End Results program. For data to be included for a given year, registries had to meet data quality and completeness standards developed for US Cancer Statistics.1 Participating registries classified tumor histology, tumor behavior, and primary cancer site according to the 3rd edition of the International Classification of Diseases for Oncology (ICD-O-3).22 We included only invasive cancers of the uterus (ICD-O-3 codes C540–C549 and C559), and ovaries (ICD-O-3 code C569) in our analysis. More detailed description about data sources and methodology can be found elsewhere in this supplement.13

To identify AI/AN cancer cases misclassified as other races, central cancer registries regularly link their cancer records with IHS patient registration files.17 AI/AN individuals must provide proof of enrollment in a federally recognized tribe to receive health care from the IHS. The access to health care by IHS is greatest in Contract Health Service Delivery Area (CHSDA) counties, which, in general, contain, or are adjacent to, a federally recognized tribal reservation, tribal lands, or both.19

Standards for coding of stage of disease at diagnosis changed during the period of this study; therefore, we restricted the analysis of stage at diagnosis to incident cases diagnosed during the most recent years (2004–2009). We examined stage at diagnosis using the Collaborative Stage Derived Surveillance, Epidemiology, and End Results Summary Stage 2000 variable.23

RESULTS

Age-adjusted ovarian and uterine cancer death rates, RRs, and 95% CIs by IHS region for CHSDA counties and all US counties for AI/AN women compared with White women are presented in Table 1. There were 135 549 ovarian cancer deaths (death rate = 9.1) and 59 540 uterine cancer deaths (death rate = 3.9) among AI/AN and White women from 1999 through 2009. Of these, 705 ovarian and 314 uterine cancer deaths were among AI/AN women. In CHSDA counties, AI/AN women accounted 1.7% of ovarian and 1.8% of uterine cancer deaths. The death rate for ovarian cancer among AI/AN women residing in CHSDA counties was 9.0 per 100 000 women, whereas for uterine cancer it was 4.0. We observed that AI/AN and White women in CHSDA counties had similar death rates from ovarian cancer (9.0 vs 9.2) and uterine cancer (4.0 vs 3.8). The observed death rates varied by region. From 1999 to 2009, among AI/AN women residing in CHSDA counties, ovarian cancer death rates ranged from 5.4 in the East to 10.2 in the Pacific Coast; uterine cancer death rates ranged from 1.9 in Alaska to 5.4 in the Northern Plains. When examined by age, death rates for both uterine and ovarian cancer increased with age regardless of geography.

Cancer Incidence and Death Trends

Overall, 1023 ovarian and 453 uterine cancer deaths were reported from 1990 to 2009 in AI/AN women in all US counties. Ovarian and uterine cancer IRs by year for CHSDA counties are shown in Figure 1, and death rates are shown in Figure 2. The death rates for both cancers among AI/AN women fluctuated over the past 2 decades. Among White women, ovarian cancer death rates showed a nonsignificant increase from 1990 to 1992 (APC = 3.3%), followed by a significant decrease from 1992 to 1997 (APC = −1.8%). Ovarian cancer rates remained level from 1997 to 2005 (APC = 0.5%) followed by a significant decrease from 2005 to 2009 (APC = 3.7%). Uterine cancer death rates remained level from 1990 to 2009 for both AI/AN and White women. Ovarian cancer incidence showed a decreasing trend for White women (APC = −6.0 for 1999–2002, APC = −2.3 for 2002–2009). Uterine cancer IRs remained level for AI/AN and White women (Joinpoint trend data tables are not shown).

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FIGURE 1—

Incidence rates by year for (a) ovarian cancer and (b) uterine cancer: CHSDA counties; United States; 1999–2009.

Note. AI/AN = American Indians/Alaska Natives; CHSDA = Contract Health Service Delivery Areas; CI = confidence interval; IHS = Indian Health Service; NHW = non-Hispanic White; NPCR = National Program of Cancer Registries; SEER = Surveillance, Epidemiology, and End Results Program. Rates per 100 000 persons and were age adjusted to the 2000 US standard population (11 age groups; Census P25-1130). AI/AN race is reported by NPCR and SEER registries or through linkage with the IHS patient registration database. Includes only AI/AN of non-Hispanic origin.

Source. Cancer registries in the Centers for Disease Control and Prevention’s NPCR or the National Cancer Institute’s SEER program. Years of data and registries used are as follows: 1999–2008: WI^a; 1999–2009 (43 states): AK,^a AL,^a AZ,^a CA,^a CO,^a CT,^a DE, FL,^a GA, HI, IA,^a ID,^a IL, IN,^a KS,^a KY, LA,^a MA,^a MD, ME,^a MI,^a MN,^a MO, MT,^a ND^a NE,^a NH, NJ, NM,^a NV,^a NY,^a OH, OK,^a OR,^a PA,^a RI,^a SC,^a TX,^a UT,^a VT, WA,^a WV, WY^a; 1999–2001 and 2003–2009: DC; 2001–2009: AR, NC,^a SD^a; 2002–2009: VA; and 2003–2009: MS,^a TN.

^aState with ≥ 1 county designated as CHSDA.

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FIGURE 2—

Death rates by year for (a) ovarian cancer and (b) uterine cancer: CHSDA counties; United States; 1990–2009.

Source: AI/AN–US Mortality Database (1990–2009).

Note. AI/AN = American Indian/Alaska Native; CHSDA = contract health service delivery areas; IHS indicates Indian Health Service; NHW = non-Hispanic White;. Analyses are limited to persons of non-Hispanic origin. Cancer causes of death was created using the Surveillance, Epidemiology and End Results (SEER) Cause of Death recode. AI/AN race is created using death certificate race and IHS Link. Rates are per 100 000 persons and are age-adjusted to the 2000 US standard population (11 age groups - Census P25-1130). States and years of data excluded because Hispanic Origin was not collected on the death certificate: LA: 1990; NH: 1990–1992; OK: 1990–1996. Percentage of regional coverage of AI/AN in CHSDA counties to AI/AN in all counties: Northern Plains = 64.8%; Alaska = 100%; Southern Plains = 76.3%; Southwest = 91.3%; Pacific Coast = 71.3%; East = 18.2%; Total US = 64.2%.

DISCUSSION

Our results demonstrated that, overall, ovarian and uterine cancer death rates in AI/AN women in CHSDA areas were similar to those in White women. We observed differences in IRs and death rates for ovarian and uterine cancer in AI/AN women by IHS region, with women in the Pacific Coast and Southern Plains having a higher ovarian cancer death rate and women in the Northern Plains having a higher uterine cancer death rate. Furthermore, comparing AI/AN women with White women, ovarian cancer death rates were higher in the Alaska, Southern Plains, and Southwest regions. Uterine cancer death rates, when comparing AI/AN women with White women, were higher in the Northern Plains, Southern Plains, Southwest, and Pacific Coast regions. Although overall uterine cancer IRs were marginally lower in AI/AN women in the Southern Plains, they were 35% higher than those of White women. Ovarian cancer IRs were also higher in AI/AN women than in White women in the Southern Plains. For AI/AN women aged 50 years or younger, uterine cancer IRs were higher than for White women. We observed, in comparison with White women, AI/AN women had a higher rate and proportion of ovarian cancer cases diagnosed at a distant stage and the majority of uterine cancers diagnosed at a localized stage.

To our knowledge, this study is the first focused on both ovarian and uterine cancers in AI/AN women using cancer incidence and mortality data that have been linked to improve race misclassification. Our ovarian cancer findings for all US counties were similar to a national study by Howe et al.,37 who also observed lower ovarian cancer death rates in American Indian women in comparison with White women, though this observation did not hold when looking only at CHSDA counties. As in our analysis, they also observed similar geographic variation in ovarian cancer rates, with AI/AN women in the Northeast region having the lowest rates. However, these data are from the 1990s, relied solely on vital statistics data, and did not consider misclassification of race on death certificates. Other studies describing ovarian and uterine cancer incidence and mortality have been limited to a particular geographic region or state.6,38–41

In addition to potential misclassification of race, the incidence and mortality variations we observed among IHS regions may, in part, reflect geographic variations in environmental, social, and personal determinants of health. These geographic variations in IRs may highlight differences in the prevalence of risk factors such as obesity and physical activity known to be associated with both ovarian and uterine cancers.42–44 According to Behavioral Risk Factor Surveillance System survey data, AI/AN women have a higher prevalence of obesity (35.4%) than White women (21.5) regardless of geographic region.45 Also, AI/AN women are physically less active than White women (30.6% vs 22%),45 and AI/AN women have a higher prevalence of cigarette smoking, especially in the Alaska, East, and Northern Plains regions.45 In addition, hypertension and adult onset of diabetes mellitus are associated with increased risk of uterine cancer.46,47 AI/AN women have a higher prevalence of diabetes than White women (13.9% vs 6.9%),45 and AI/AN women have been reported to have a higher rate of mortality as a result of diabetes than the general population.48

Regional variations may also be caused by differences in other risk factors influencing ovarian and uterine cancer, such as pregnancy, long-term use of oral contraceptives, hormone replacement therapy, tubal ligation, or hysterectomy (with retention of the ovaries).49 How many AI/AN women were exposed to postmenopausal hormone therapy is unknown. Observational epidemiologic evidence has strongly supported that tubal ligation and hysterectomy are associated with a decrease in the risk of ovarian cancer by approximately 26% to 30%.50 AI/AN women had a higher prevalence of hysterectomy (23.1%) compared with White women (20.9%), and higher hysterectomy rates in AI/AN women decrease risk for uterine cancer.51 In addition, trends in hysterectomy and oophorectomy may influence observed trends in ovarian and uterine cancer mortality. Tubal sterilization rates, which may influence rates of ovarian cancer, also vary by race.52 To our knowledge, accurate counts of those who have intact ovaries and uteri are not available.

Genetic variations may also partially explain observed geographic differences in IRs, though no large study has been done in AI/AN populations for genetic testing for familial cancers. Sporadic cases of breast and ovarian cancer suggestive of BRCA1/2 carriers as well as documentation of families diagnosed with Lynch syndrome have been found in Utah, Oklahoma, and Navajo Nation.53

Observed variations in stage at diagnosis and death rates for ovarian and uterine cancer for AI/AN populations may be attributable to differences in diagnostic and treatment patterns. No screening tests are recommended for either ovarian or uterine cancer54; however, differences in time of diagnosis may have resulted from differences in clinical presentation of both cancer types. Most uterine cancer presents with symptoms such as postmenopausal bleeding, and ovarian cancer presents with minimal or nonspecific symptoms such as bloating.55 The lack of screening tests and the nonspecificity of symptoms result in later stage at diagnosis for both ovarian and uterine cancer. Public education and provider education may be important to affect stage at time of diagnosis, referral for appropriate and timely treatment, and ultimately survival. A molecular screening test, particularly for ovarian cancer, may change patterns of disease for a small segment of the population for whom genetic screening may be warranted. Prophylactic total hysterectomy has been shown to reduce risk of uterine and ovarian cancer in families with BRCA mutations or Lynch syndrome.56

Finally, differences in mortality by geographic region may be reflective of geographic differences in the biological variation of the disease and access to state-of-the-art cancer care. The IHS has no gynecologic oncology surgeons, and therefore referral patterns may lead to delay in diagnosis and treatment that may affect death rates, but not IRs.57 Although public service announcements such as the Centers for Disease Control and Prevention’s Inside Knowledge campaign have been aimed at the general public, no concerted educational efforts have been made in AI/AN communities alerting women to the symptoms that require assessment by a clinician.

Human Participant Protection

References