HHS Public Access Author manuscript Author Manuscript
J Okla State Med Assoc. Author manuscript; available in PMC 2015 August 14. Published in final edited form as: J Okla State Med Assoc. 2014 March ; 107(3): 99–107.
Cancer Incidence and Staging among American Indians in Oklahoma Janis E. Campbell, PhD, Sydney A. Martinez, MPH, Amanda E. Janitz, RN, MPH, Anne E. Pate, PhD, Julie Erb-Alvarez, MPH, David F Wharton, MPH, RN, David Gahn, MD, MPH, Vicki L. Tall, Chief, Ed.D, Cuyler Snider, MPH, and Tom Anderson, MPH
Author Manuscript
Abstract Background—This study describes overall and site specific cancer incidence among AI/ANs compared to whites in Oklahoma and differences in cancer staging. Methods—Age-adjusted incidence rates obtained from the Oklahoma Central Cancer Registry are presented for all cancer sites combined and for the most common cancer sites among AI/ANs with comparisons to whites. Percentages of late stage cancers for breast, colorectal, and melanoma cancers are also presented.
Author Manuscript
Results—AI/ANs had a significantly higher overall cancer incidence rate compared to whites (629.8/100,000 vs. 503.3/100,000), with a rate ratio of 1.25 (95% CI: 1.22, 1.28). There was a significant disparity in the percentage of late stage melanoma cancers between 2005 and 2009, with 14.0% late stage melanoma for whites and 20.0% for AI/ANs (p-value: 0.03). Conclusions—Overall, there were cancer disparities between AI/ANs and whites in Oklahoma. Incidence rates were higher among AI/ANs for all cancers and many site specific cancers. Keywords Indians; North American; Neoplasms; Registries; Health Policy; Health Status Disparities
BACKGROUND
Author Manuscript
Cancer is a serious cause of morbidity and mortality in the United States. Disparities exist in incidence, mortality, survival and stage of diagnosis between American Indians and Alaska Natives (AI/ANs) and whites.1–23 When accounting for racial misclassification, AI/ANs have some of the highest mortality rates in the US.24,25 In the US, regional differences exist with significantly disparate cancer incidence rates among AI/ANs compared to whites in the Alaska, the Northern Plains, and the Southern Plains regions.15 In 2011, approximately 3.8 million people resided in Oklahoma. Of these, 8.9% reported that they were AI/AN only. Within the AI/AN population, estimated at 337,000, there is a wide diversity of cultures represented by 39 tribal nations. Oklahoma has the second largest number and the second highest proportion of AI/AN individuals of all US states. The
Correspondence to: Janis E. Campbell, PhD, Assistant Professor of Research, The University of Oklahoma Health Sciences Center, 801 N.E. 13th Street, Room 309, Oklahoma City, OK, USA, 73104, t(405) 271-2229, f(405)271-2068, [email protected].
Campbell et al.
Page 2
Author Manuscript
Oklahoma City Area Indian Health Service (IHS) had 332,658 health care and environmental services users in fiscal year 2012. Oklahoma is unique compared to other areas in the US because AI/ANs live with a higher level of integration into mainstream society, rather than on tribal reservations. The purpose of this study is to describe cancer incidence among AI/ANs in Oklahoma. We describe statewide age-adjusted cancer incidence rates for AI/ANs and whites in Oklahoma, stage of diagnosis for specific cancers and cancer incidence rates for Oklahoma City Area IHS service units within Oklahoma.
METHODS AND MATERIALS
Author Manuscript Author Manuscript
Central cancer registries receive case information from multiple sources, including hospitals, outpatient surgery centers, freestanding radiation centers, laboratories, and death certificates. Two federal programs fund the two central cancer registries in Oklahoma. The Centers for Disease Control and Prevention, National Program of Cancer Registries (CDC-NPCR) funds the Oklahoma Central Cancer Registry (OCCR) and the National Cancer Institute’s (NCI) Surveillance, Epidemiology, and End Results (SEER) Program funds the Cherokee Nation Cancer Registry (CNCR). OCCR is the central cancer registry responsible for all cancers diagnosed or treated in the state of Oklahoma and CNCR is responsible for those diagnosed or treated among AI/ANs in the Cherokee Nation Tribal jurisdictional area. OCCR and CNCR perform an annual data exchange and, thus for this study, data from OCCR will be used as it includes CNCR cases. OCCR has a greater than 95% estimated case completeness for each year of data collected between 1997 and 2009. The OCCR has received the highest level of certification available from the North American Association of Central Cancer Registries (NAACCR) based on quality, completeness and timeliness of data collected for 2001–2009.26 To identify AI/AN cancer cases that were misclassified as other races, OCCR works with IHS to link cancer registry records with IHS patient registration files.5 AI/AN individuals must provide proof of membership in a federally recognized tribe to receive healthcare from the Indian health system which includes IHS, Tribal, and Urban facilities. An individual’s race was determined using the OCCR race 1 variable in combination with the IHS link variable or race 1 alone if it was coded as AI/AN. Thus, this study considers AI/ANs to be those coded as AI/ANs on the race 1 variable or the IHS Link variable and excludes that person from any other race codes. For this study only AI/ANs and whites are considered.
Author Manuscript
Age-adjusted incidence rates are presented for all cancer sites combined and for the most common cancer sites among AI/AN bridged population estimates in Oklahoma; site categories are consistent with prevailing reporting standards.27,28 Lymphomas (ICD-O histology codes 9590-9729) are presented as two separate categories (i.e., Hodgkin and nonHodgkin lymphoma) and are not included with other tumors of specific anatomic sites. Mesothelioma (ICD-O histology codes 9050-9055) and Kaposi sarcoma (ICD-O histology code 9140) are not included with other tumors of specific anatomic sites. In situ and invasive bladder tumors are combined in a single category.29 For gender-specific cancers including prostate, breast, corpus uteri, ovary, cervix uteri, testis, and penis cancers, the
J Okla State Med Assoc. Author manuscript; available in PMC 2015 August 14.
Campbell et al.
Page 3
Author Manuscript
incidence rates were calculated using gender-specific populations. All other benign tumors (ICD-O behavior codes 0) and tumors of uncertain or unknown behavior (ICD-O behavior code 1) were excluded for the analysis.
Author Manuscript
Cancer stage at diagnosis for breast and colorectal cancer was determined using the derived SEER Summary Stage 2000. To review staging changes through time, we considered two periods, the earliest years available and the latest years available. For breast and colorectal cancer we used three years of data (1997–1999 and 2007–2009); for melanoma and cervical cancers we used five years of data (1997–2001 and 2005–2009) because of the small number of cases among AI/ANs for these sites. In situ was included for breast, colorectal cancer and melanoma but not included for cervical cancer. Early stage for cervical cancers was local stage and early stage for breast, colorectal and melanoma was in situ and local stages combined. Late stage included regional and distant stages for all sites. Cases that were identified as Death Certificate Only or had unknown stages were excluded from the analysis, but the percentages for unknown stage are shown.
Author Manuscript
Incidence rates were calculated per 100,000 population using bridged population estimates and were age-adjusted by the direct method30 using the 2000 United States standard population. Incidence rates, rate ratios and 95% confidence limits were calculated. Denominators for rate calculations were derived from population estimates obtained from SEER population files. Incidence rates were calculated for the whole state and for each of the nine IHS service units in Oklahoma (Figure 1). These IHS service units were chosen because they are consistent with IHS reports and IHS service provision in Oklahoma. Incidence rates were calculated using the Oklahoma State Department of Health’s webbased query system, Oklahoma Statistics on Health Available for Everyone (OK2SHARE).31 For this analysis the two sample z-test for comparing a difference in proportions was calculated to allow us to test for a statistical significance for primary payer and for stage at diagnosis. To ensure confidentiality, numbers were not reported when total counts were less than ten.
RESULTS Overall, we found an increase in the age-adjusted incidence rates in AI/ANs compared to whites in Oklahoma from 2005–2009. When accounting for misclassification, AI/ANs had a significantly higher overall cancer incidence rate than whites (629.8/100,000 vs 503.3/100,000) with a rate ratio of 1.25 (95% CI: 1.22,1.28). Females had an increased rate ratio between AI/ANs and whites at 1.31 (95% CI: 1.27,1.35) compared to males at 1.19 (95% CI: 1.15,1.23; Table 1).
Author Manuscript
Age-group specific cancer rates were higher among AI/ANs compared to whites among each age group, with the exception of those ages 5 to 9. Rates were significantly higher among AI/ANs compared to whites in all but four of these age groups (Table 2). All agespecific groups 25 years and older showed significantly increased rates among AI/ANs when compared to whites.
J Okla State Med Assoc. Author manuscript; available in PMC 2015 August 14.
Campbell et al.
Page 4
Author Manuscript
Primary payer at diagnosis is an important variable for understanding access to care and to screening services. Primary payer at diagnosis was significantly different for AI/ANs and whites for all payer sources (Table 3). AI/ANs were more likely than whites to have unknown insurance (11.2% vs 8.3%), to have Medicaid (7.8% vs 4.1%), and to have IHS/ Public Health Service coverage (12.7% vs 0.0%) as their primary payer. AI/ANs were less likely to be uninsured (2.3% vs 3.7%), to have military insurance (0.5% vs 1.1%), to have Veterans Affairs insurance (0.8% vs 1.1%) and have private insurance (24.0% vs 31.7%) as their primary payer. Primary Site
Author Manuscript
For 36 specific cancer sites, 21 had rate ratios that were significantly higher among AI/ANs compared to whites(Table 4). The highest site specific incidence among both AI/ANs and whites was found to be prostate cancer. The prostate cancer rate for AI/ANs was significantly higher among AI/ANs compared to whites, with a rate ratio of 1.10 (95% CI: 1.01, 1.16). Lung cancer was the most commonly diagnosed cancer for both AI/ANs and whites. AI/ANs had a significantly higher rate of lung cancer, with a rate ratio of 1.50 (95% CI: 1.37, 1.58). Primary sites demonstrating large disparities between the two populations included: kidney and renal pelvis (RR: 1.90, 95% CI: 1.70, 2.10), liver and bile duct (RR: 2.21, 95% CI: 1.84, 2.58), stomach (RR: 2.02, 95% CI: 1.63, 2.41), gallbladder (RR: 3.40, 95% CI: 2.20, 4.60), and penis (RR: 4.00, 95% CI: 1.88, 6.12). Four of the primary sites had rate ratios that reflected lower incidence among AI/ANs, but only two of those sites had rates that were significantly higher among whites: melanomas of the skin (RR: 0.60, 95% CI: 0.52, 0.68) and bladder (RR: 0.87, 95% CI: 0.75, 0.99; Table 4). Stage at diagnosis
Author Manuscript Author Manuscript
From 1997–1999 there was a significant disparity in the percent of female breast cancers diagnosed at the late stage between whites and AI/ANs (29.5% vs 41.5% respectively, pvalue
J Okla State Med Assoc. Author manuscript; available in PMC 2015 August 14. Published in final edited form as: J Okla State Med Assoc. 2014 March ; 107(3): 99–107.
Cancer Incidence and Staging among American Indians in Oklahoma Janis E. Campbell, PhD, Sydney A. Martinez, MPH, Amanda E. Janitz, RN, MPH, Anne E. Pate, PhD, Julie Erb-Alvarez, MPH, David F Wharton, MPH, RN, David Gahn, MD, MPH, Vicki L. Tall, Chief, Ed.D, Cuyler Snider, MPH, and Tom Anderson, MPH
Author Manuscript
Abstract Background—This study describes overall and site specific cancer incidence among AI/ANs compared to whites in Oklahoma and differences in cancer staging. Methods—Age-adjusted incidence rates obtained from the Oklahoma Central Cancer Registry are presented for all cancer sites combined and for the most common cancer sites among AI/ANs with comparisons to whites. Percentages of late stage cancers for breast, colorectal, and melanoma cancers are also presented.
Author Manuscript
Results—AI/ANs had a significantly higher overall cancer incidence rate compared to whites (629.8/100,000 vs. 503.3/100,000), with a rate ratio of 1.25 (95% CI: 1.22, 1.28). There was a significant disparity in the percentage of late stage melanoma cancers between 2005 and 2009, with 14.0% late stage melanoma for whites and 20.0% for AI/ANs (p-value: 0.03). Conclusions—Overall, there were cancer disparities between AI/ANs and whites in Oklahoma. Incidence rates were higher among AI/ANs for all cancers and many site specific cancers. Keywords Indians; North American; Neoplasms; Registries; Health Policy; Health Status Disparities
BACKGROUND
Author Manuscript
Cancer is a serious cause of morbidity and mortality in the United States. Disparities exist in incidence, mortality, survival and stage of diagnosis between American Indians and Alaska Natives (AI/ANs) and whites.1–23 When accounting for racial misclassification, AI/ANs have some of the highest mortality rates in the US.24,25 In the US, regional differences exist with significantly disparate cancer incidence rates among AI/ANs compared to whites in the Alaska, the Northern Plains, and the Southern Plains regions.15 In 2011, approximately 3.8 million people resided in Oklahoma. Of these, 8.9% reported that they were AI/AN only. Within the AI/AN population, estimated at 337,000, there is a wide diversity of cultures represented by 39 tribal nations. Oklahoma has the second largest number and the second highest proportion of AI/AN individuals of all US states. The
Correspondence to: Janis E. Campbell, PhD, Assistant Professor of Research, The University of Oklahoma Health Sciences Center, 801 N.E. 13th Street, Room 309, Oklahoma City, OK, USA, 73104, t(405) 271-2229, f(405)271-2068, [email protected].
Campbell et al.
Page 2
Author Manuscript
Oklahoma City Area Indian Health Service (IHS) had 332,658 health care and environmental services users in fiscal year 2012. Oklahoma is unique compared to other areas in the US because AI/ANs live with a higher level of integration into mainstream society, rather than on tribal reservations. The purpose of this study is to describe cancer incidence among AI/ANs in Oklahoma. We describe statewide age-adjusted cancer incidence rates for AI/ANs and whites in Oklahoma, stage of diagnosis for specific cancers and cancer incidence rates for Oklahoma City Area IHS service units within Oklahoma.
METHODS AND MATERIALS
Author Manuscript Author Manuscript
Central cancer registries receive case information from multiple sources, including hospitals, outpatient surgery centers, freestanding radiation centers, laboratories, and death certificates. Two federal programs fund the two central cancer registries in Oklahoma. The Centers for Disease Control and Prevention, National Program of Cancer Registries (CDC-NPCR) funds the Oklahoma Central Cancer Registry (OCCR) and the National Cancer Institute’s (NCI) Surveillance, Epidemiology, and End Results (SEER) Program funds the Cherokee Nation Cancer Registry (CNCR). OCCR is the central cancer registry responsible for all cancers diagnosed or treated in the state of Oklahoma and CNCR is responsible for those diagnosed or treated among AI/ANs in the Cherokee Nation Tribal jurisdictional area. OCCR and CNCR perform an annual data exchange and, thus for this study, data from OCCR will be used as it includes CNCR cases. OCCR has a greater than 95% estimated case completeness for each year of data collected between 1997 and 2009. The OCCR has received the highest level of certification available from the North American Association of Central Cancer Registries (NAACCR) based on quality, completeness and timeliness of data collected for 2001–2009.26 To identify AI/AN cancer cases that were misclassified as other races, OCCR works with IHS to link cancer registry records with IHS patient registration files.5 AI/AN individuals must provide proof of membership in a federally recognized tribe to receive healthcare from the Indian health system which includes IHS, Tribal, and Urban facilities. An individual’s race was determined using the OCCR race 1 variable in combination with the IHS link variable or race 1 alone if it was coded as AI/AN. Thus, this study considers AI/ANs to be those coded as AI/ANs on the race 1 variable or the IHS Link variable and excludes that person from any other race codes. For this study only AI/ANs and whites are considered.
Author Manuscript
Age-adjusted incidence rates are presented for all cancer sites combined and for the most common cancer sites among AI/AN bridged population estimates in Oklahoma; site categories are consistent with prevailing reporting standards.27,28 Lymphomas (ICD-O histology codes 9590-9729) are presented as two separate categories (i.e., Hodgkin and nonHodgkin lymphoma) and are not included with other tumors of specific anatomic sites. Mesothelioma (ICD-O histology codes 9050-9055) and Kaposi sarcoma (ICD-O histology code 9140) are not included with other tumors of specific anatomic sites. In situ and invasive bladder tumors are combined in a single category.29 For gender-specific cancers including prostate, breast, corpus uteri, ovary, cervix uteri, testis, and penis cancers, the
J Okla State Med Assoc. Author manuscript; available in PMC 2015 August 14.
Campbell et al.
Page 3
Author Manuscript
incidence rates were calculated using gender-specific populations. All other benign tumors (ICD-O behavior codes 0) and tumors of uncertain or unknown behavior (ICD-O behavior code 1) were excluded for the analysis.
Author Manuscript
Cancer stage at diagnosis for breast and colorectal cancer was determined using the derived SEER Summary Stage 2000. To review staging changes through time, we considered two periods, the earliest years available and the latest years available. For breast and colorectal cancer we used three years of data (1997–1999 and 2007–2009); for melanoma and cervical cancers we used five years of data (1997–2001 and 2005–2009) because of the small number of cases among AI/ANs for these sites. In situ was included for breast, colorectal cancer and melanoma but not included for cervical cancer. Early stage for cervical cancers was local stage and early stage for breast, colorectal and melanoma was in situ and local stages combined. Late stage included regional and distant stages for all sites. Cases that were identified as Death Certificate Only or had unknown stages were excluded from the analysis, but the percentages for unknown stage are shown.
Author Manuscript
Incidence rates were calculated per 100,000 population using bridged population estimates and were age-adjusted by the direct method30 using the 2000 United States standard population. Incidence rates, rate ratios and 95% confidence limits were calculated. Denominators for rate calculations were derived from population estimates obtained from SEER population files. Incidence rates were calculated for the whole state and for each of the nine IHS service units in Oklahoma (Figure 1). These IHS service units were chosen because they are consistent with IHS reports and IHS service provision in Oklahoma. Incidence rates were calculated using the Oklahoma State Department of Health’s webbased query system, Oklahoma Statistics on Health Available for Everyone (OK2SHARE).31 For this analysis the two sample z-test for comparing a difference in proportions was calculated to allow us to test for a statistical significance for primary payer and for stage at diagnosis. To ensure confidentiality, numbers were not reported when total counts were less than ten.
RESULTS Overall, we found an increase in the age-adjusted incidence rates in AI/ANs compared to whites in Oklahoma from 2005–2009. When accounting for misclassification, AI/ANs had a significantly higher overall cancer incidence rate than whites (629.8/100,000 vs 503.3/100,000) with a rate ratio of 1.25 (95% CI: 1.22,1.28). Females had an increased rate ratio between AI/ANs and whites at 1.31 (95% CI: 1.27,1.35) compared to males at 1.19 (95% CI: 1.15,1.23; Table 1).
Author Manuscript
Age-group specific cancer rates were higher among AI/ANs compared to whites among each age group, with the exception of those ages 5 to 9. Rates were significantly higher among AI/ANs compared to whites in all but four of these age groups (Table 2). All agespecific groups 25 years and older showed significantly increased rates among AI/ANs when compared to whites.
J Okla State Med Assoc. Author manuscript; available in PMC 2015 August 14.
Campbell et al.
Page 4
Author Manuscript
Primary payer at diagnosis is an important variable for understanding access to care and to screening services. Primary payer at diagnosis was significantly different for AI/ANs and whites for all payer sources (Table 3). AI/ANs were more likely than whites to have unknown insurance (11.2% vs 8.3%), to have Medicaid (7.8% vs 4.1%), and to have IHS/ Public Health Service coverage (12.7% vs 0.0%) as their primary payer. AI/ANs were less likely to be uninsured (2.3% vs 3.7%), to have military insurance (0.5% vs 1.1%), to have Veterans Affairs insurance (0.8% vs 1.1%) and have private insurance (24.0% vs 31.7%) as their primary payer. Primary Site
Author Manuscript
For 36 specific cancer sites, 21 had rate ratios that were significantly higher among AI/ANs compared to whites(Table 4). The highest site specific incidence among both AI/ANs and whites was found to be prostate cancer. The prostate cancer rate for AI/ANs was significantly higher among AI/ANs compared to whites, with a rate ratio of 1.10 (95% CI: 1.01, 1.16). Lung cancer was the most commonly diagnosed cancer for both AI/ANs and whites. AI/ANs had a significantly higher rate of lung cancer, with a rate ratio of 1.50 (95% CI: 1.37, 1.58). Primary sites demonstrating large disparities between the two populations included: kidney and renal pelvis (RR: 1.90, 95% CI: 1.70, 2.10), liver and bile duct (RR: 2.21, 95% CI: 1.84, 2.58), stomach (RR: 2.02, 95% CI: 1.63, 2.41), gallbladder (RR: 3.40, 95% CI: 2.20, 4.60), and penis (RR: 4.00, 95% CI: 1.88, 6.12). Four of the primary sites had rate ratios that reflected lower incidence among AI/ANs, but only two of those sites had rates that were significantly higher among whites: melanomas of the skin (RR: 0.60, 95% CI: 0.52, 0.68) and bladder (RR: 0.87, 95% CI: 0.75, 0.99; Table 4). Stage at diagnosis
Author Manuscript Author Manuscript
From 1997–1999 there was a significant disparity in the percent of female breast cancers diagnosed at the late stage between whites and AI/ANs (29.5% vs 41.5% respectively, pvalue
