Abstract
Background
The risk of diabetes among Asian, Native Hawaiian, and Pacific Islander (ANHPI) women after breast cancer is unclear. This study estimated the risk of incident type II diabetes in older ANHPI and older non-Hispanic White (NHW) women with breast cancer from the US National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) Medicare linked claims.
Methods
A matched cohort of 7122 older ANHPI and 21 365 older NHW women with breast cancer were identified from SEER-Medicare between 2000 and 2017. To assess the risk of incident type II diabetes after breast cancer, hazard ratios (HRs) and 95% confidence intervals (95% CI) were estimated using the Cox proportional-hazards regression model.
Results
During the mean 8 years of follow-up, 9.3% of older women with breast cancer developed incident type II diabetes. In comparison with older NHW women, older ANHPI women without a known history of diabetes had an elevated risk of diabetes after breast cancer, with strong associations observed for Pacific Islander (HR = 3.09, 95% CI = 1.43 to 6.67), Vietnamese (HR = 2.12, 95% CI = 1.33 to 2.36), and Filipino (HR = 2.02, 95% CI = 1.57 to 2.59) women with breast cancer, adjusting for potential confounders. Among ANHPI women with breast cancer, more baseline comorbidities and obesity were risk factors for developing incident type II diabetes.
Conclusion
ANHPI women diagnosed with breast cancer had an elevated risk of type II diabetes compared with older NHW women with breast cancer. Routine monitoring and management of diabetes are warranted in older ANHPI women with breast cancer.
In the United States, breast cancer is the most commonly diagnosed cancer among women, including both non-Hispanic White (NHW) and Asian, Native Hawaiian and Pacific Islander (ANHPI) women (1). The risk of breast cancer increases with age, coinciding with the increased likelihood of underlying chronic comorbidities such as diabetes, whether attributed to cancer treatment, diagnosis, or both (2). Although type II diabetes is a recognized independent risk factor for various cancers, including breast cancer (3-6), the risk of diabetes among older ANHPI women after breast cancer remains unclear, despite the predisposition to diabetes observed in Asian populations.
A recent meta-analysis of studies reported an increase in the subsequent risk of diabetes after breast cancer (7), with the majority of the cohort studies conducted in East Asia among women diagnosed over a decade ago (8-12). The US-based cohort studies reported higher odds of diabetes in adult women of different ages (14,15) but did not report race-specific estimates of diabetes (14). The US SEER-Medicare study reported higher odds of diabetes among an aggregated sample of older Asian and NHPI women diagnosed over a decade ago (15). Similarly, a large Canadian cohort observed a moderate increase in diabetes risks in postmenopausal women diagnosed with breast cancer before 2008; however, diabetes risks for specific race and ethnicity groups were not reported in the study (13).
Asians and Native Hawaiian and Pacific Islanders (NHPI) have a higher prevalence of diabetes compared to other race and ethnic groups in the United States (16). Understanding the risk of diabetes in Asian and NHPI women after cancer is essential for optimizing survivorship health outcomes and overall quality of life. Given limited diabetes-related research among older Asian and NHPI women with breast cancer, we had a unique opportunity to evaluate diabetes risk within Asian and NHPI women with breast cancer leveraging the SEER-Medicare database. Thus, this study aimed to assess the risk of incident type II diabetes in older Asian and NHPI women after breast cancer in comparison to older NHW women without a known history of prior diabetes.
Methods
Data sources
The US National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) program registry records that link to Medicare claims were used to identify all women with breast cancer who were diagnosed between 2000 and 2017. The SEER-Medicare linked database is a collaborative effort between the National Cancer Institutes (NCI), the SEER registry, and the Centers for Medicare and Medicaid Services (claims) (17). The Medicare linkage to the SEER registry varies from 91.1% to 99.2% across registries. The Medicare claims included the date of service and procedures from fee-for-service billed by hospitals (part A), physicians (part B), and outpatient facilities (part B). SEER included demographic and cancer characteristics such as cancer stage, histology, receptor subtype (available from 2010), cancer grade, residence, and the first-course treatment from cancer registries that are the comprehensive source of population-based cancer data for the United States, census-tract education and income, and socioeconomic index (as quintiles).
Study population
Older women with a reportable SEER (International Classification of Diseases (ICD)-0-3 C50.0 to C50.9) primary breast cancer diagnosis between 2000 and 2017 were included for the analysis. Women with breast cancer were included if they were: 1) diagnosed with a first primary invasive breast cancer, 2) 66 years of age and older at diagnosis, 3) had a continuous fee-for-service Medicare Parts A and B coverage for 1 year before and after the index date (breast cancer diagnosis date) and were not a health maintenance organization (HMO) member, 4) had a known diagnosis date and cancer stage information, and 5) had at least 1 year of follow-up. Breast cancer patients with the source of diagnosis as an autopsy or death certificate were excluded. One category for non-Hispanic White women was reported in the SEER, and a number of subgroups were combined to represent the Asian, Native Hawaiian, and Pacific Islander (ANHPI) subpopulations. Greedy matching without replacement was used to select non-Hispanic White (NHW) women whose age and year at breast cancer diagnosis are closest (±1) to that of ANHPI, resulting in up to 3 NHW matches (18). The final study sample included 7122 ANHPI and 21 365 NHW women with breast cancer.
Type II diabetes and baseline comorbidities
Diabetes diagnosis was identified through claims in Medicare submitted by a hospital (Medicare Provider Analysis and Review or MedPAR), physicians (the National Claims History or NCH), and outpatient facilities based on the International Classification of Diseases, Ninth Revision (ICD-9) and Tenth Revision, Clinical Modification (ICD-10-CM) diagnosis codes (19,20). All analyses were based on type II diabetes diagnosis identified in the presence of at least 1 claim in the hospital files or at least 2 claims between 30 and 60 days from physicians and outpatient files to assure that “rule-out” diagnoses (unconfirmed diagnosis) are not counted to prevent overestimation of the outcome endpoint (21). Among all the billing codes for diabetes diagnosis from the Chronic Conditions Data Warehouse (CCW), we identified and included only ICDs for type II diabetes (22). Prevalent diabetes refers to diabetes diagnoses made before a cancer diagnosis, whereas incident diabetes diagnoses are those made after a cancer diagnosis. Klabunde’s version of the Charlson Comorbidity Index (CCI) was calculated using macro codes provided by the NCI 1 year before the cancer diagnosis (23,24). A binary measure of tobacco use at baseline was obtained from ICD codes (25). Similarly, a binary measure of baseline obesity was based on the ICD-9 and ICD-10-CM codes for the diagnosis of obesity (19,20).
Statistical analysis
Baseline differences between older ANHPI and NHW women with breast cancer were compared with the Pearson’s χ2 for categorical demographic and clinical characteristics. Type II diabetes proportions were reported for women that had diabetes only before, before and after, and only after breast cancer for the ANHPI and NHW women with breast cancer. Adjusted hazard ratios (HRs) were estimated using the Cox proportional hazards model for incident type II diabetes occurring at least 1 year after cancer diagnosis, allowing adequate time for the outcome to occur, whether attributed to cancer treatment, the cancer diagnosis, or both, among older women with breast cancer with no prior known history of diabetes. We assessed the risk of diabetes within 1 to 5 and over 5-years of follow-up. All models were adjusted for potential confounders, such as the baseline Charlson Comorbidity Index (CCI), cancer registry, residence, census-tract education attainment, and income. Additional adjustments for obesity, tobacco, and cancer treatment were assessed as sensitivity analysis. The subdistribution hazards for incident type II diabetes were estimated using Fine and Gray’s model for competing risks (death was used as a competing event) as sensitivity analysis (26).
The proportional hazards assumption was tested by introducing an interaction term between each covariate and log of time. Where the assumption did not hold, flexible parametric models were used, and HR estimates were reported where inferences differed from the traditional Cox models. The follow-up time was calculated from the date of breast cancer diagnosis (index date) until either the outcome of interest or censoring time (ie, last date of follow-up, no outcome, or death). Potential risk factors associated with type II diabetes, at least 1 year of follow-up among older ANHPI women with breast cancer (Japanese as reference group) were assessed with adjustment for previously mentioned confounders.
Statistical analyses were 2-sided with statistical significance at α less than 0.05 and performed in SAS 9.4 (SAS Institute, Inc, Cary, NC). This study was approved by the University of Utah Institutional Review Board (IRB). As per the IRB regulations, this study received approval for waiver of informed consent. We followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement reporting guidelines (27).
Results
Older ANHPI women in the SEER-Medicare were predominantly Japanese (23.6%), Chinese (19.7%), or Filipino (19.4%) (Table 1). For demographic characteristics, a greater proportion of NHPI women were in census tracts with less than 20% of non-high school graduates, within 5 years of follow-up, and with 2 or more comorbidities than Asian or NHW women with breast cancer (P < .0001; Table 1). The proportion of obese women in the NHW group was nearly double that of the Asian but lower than NHPI (P < .0001; Table 1). More NHW women with breast cancer were smokers than Asian women, but similar in proportions to NHPI women (P < .0001; Table 1).
Table 1.
Demographic baseline characteristics of 28 487 older Asian, Native Hawaiian, and Pacific Islander (ANHPI) and non-Hispanic White (NHW) women with breast cancer in SEER-Medicare (2000-2017)
| Asian (n = 6587) |
NHPI (n = 535) |
NHW (n = 21 365) |
|||||
|---|---|---|---|---|---|---|---|
| Characteristics | No. | (%) | No. | (%) | No. | (%) | P a |
| Age at cancer diagnosis (y) | |||||||
| 66–70 | 1974 | (30.4) | 190 | (35.5) | 6492 | (30.4) | |
| 71–75 | 1834 | (27.9) | 152 | (28.4) | 5958 | (27.9) | |
| 76–80 | 1387 | (21.0) | 111 | (20.8) | 4494 | (21.0) | |
| 81–100 | 1392 | (20.7) | 82 | (15.3) | 4421 | (20.7) | .041 |
| Maximum follow-up time (y) | |||||||
| ≥1–5 | 2500 | (37.9) | 234 | (43.7) | 8549 | (40.0) | |
| >5–10 | 2324 | (35.3) | 193 | (36.1) | 7633 | (35.7) | |
| >10 | 1763 | (26.8) | 108 | (20.2) | 5183 | (24.3) | <.0001 |
| Education (census tract)b | |||||||
| >20% non-high school graduates | 1632 | (24.8) | 108 | (20.2) | 3359 | (15.7) | |
| 10% to <20% non-high school graduates | 1915 | (29.1) | 199 | (37.2) | 6416 | (30.0) | |
| 5% to <10% non-high school graduates | 1689 | (25.6) | 159 | (29.7) | 6207 | (29.1) | |
| <5% non-high school graduates | 1318 | (20.0) | 67 | (12.5) | 4963 | (23.2) | <.0001 |
| Income (census tract)b | |||||||
| ≤$49 999 | 1716 | (26.1) | 165 | (30.8) | 7061 | (33.0) | |
| $50 000–$69 999 | 1791 | (27.2) | 186 | (34.8) | 6050 | (28.3) | |
| $70 000–$89 999 | 1404 | (21.3) | 103 | (19.2) | 3676 | (17.2) | |
| ≥$90 000 | 1643 | (24.9) | 79 | (14.8) | 4158 | (19.5) | <.0001 |
| Yost (census tract, quantiles)b | |||||||
| Q1 (lowest SES) | 339 | (5.2) | 25 | (4.7) | 1752 | (8.2) | |
| Q2 | 558 | (8.5) | 55 | (10.3) | 2586 | (12.1) | |
| Q3 | 751 | (11.4) | 67 | (12.5) | 3189 | (14.9) | |
| Q4 | 1284 | (19.5) | 136 | (25.4) | 4007 | (18.8) | |
| Q5 | 2105 | (32.0) | 112 | (20.9) | 5639 | (26.4) | <.0001 |
| Residenceb, c | |||||||
| Urban | 6306 | (95.7) | 441 | (82.6) | 17 952 | (84.0) | |
| Rural | 281 | (4.2) | <11 | 3411 | (16.0) | <.0001 | |
| Baseline CCId | |||||||
| 0 | 4743 | (72.0) | 354 | (66.2) | 14 711 | (68.9) | |
| 1 | 1097 | (16.7) | 96 | (17.9) | 4078 | (19.1) | |
| ≥2 | 747 | (11.3) | 85 | (15.9) | 2576 | (12.0) | <.0001 |
| Baseline obesity | |||||||
| No | 6195 | (94.1) | 449 | (83.9) | 18 620 | (87.2) | |
| Yes | 392 | (5.9) | 86 | (16.1) | 2745 | (12.8) | <.0001 |
| Baseline tobacco use | |||||||
| No | 6493 | (98.6) | 511 | (95.5) | 20 195 | (94.5) | |
| Yes | 94 | (1.4) | 24 | (4.5) | 1170 | (5.5) | <.0001 |
P values for 2-sided Pearson’s χ2 test was used to compare the proportions between ANHPI and NHW women (excluding missing values).
SEER, Surveillance, Epidemiology, and End Results; CCI = Charlson Comorbidity Index; Yost SES = index measure for socioeconomic status; ANHPI = Asian, Native Hawaiian, and Pacific Islander; NHW = non-Hispanic White.
Unknown values for income and education in 420 (1.5%) NHW, 33 (0.1%) Asian, and less than or equal to 11 NHPI women; for Yost in 4192 (19.6%) NHW, 1550 (23.5%) Asian, and in 140 (26.2%) NHPI women. For residence values with <11 observations were compressed in accordance with the Medicare data confidentiality policy (unknown values compressed with rural residence).
Residence was classified based on the 2013 Rural-Urban Continuum Codes (RUCC).
CCI calculation excluded diabetes mellitus.
Statistically significant differences were observed for all clinical characteristics between ANHPI and NHW women with breast cancer (Table 2). The differences in the proportions diagnosed at different cancer stages in older ANHPI and older NHW women with breast cancer were small but statistically different (P = .001; Table 2). More NHPI women were diagnosed with distant cancer stage but more had chemotherapy than Asian or NHW women (Table 2). A higher proportion of Asian and NHPI women with breast cancer had type II diabetes after cancer diagnosis than their NHW counterparts (Table 3).
Table 2.
Clinical and treatment characteristics of 28 487 older Asian, Native Hawaiian, and Pacific Islander (ANHPI) and non-Hispanic White (NHW) women with breast cancer in SEER-Medicare (2000-2017)
| Asian (n = 6587) |
NHPI (n = 535) |
NHW (n = 21 365) |
|||||
|---|---|---|---|---|---|---|---|
| Characteristics | No. | (%) | No. | (%) | No. | (%) | P a |
| Cancer stage | |||||||
| Localized | 4680 | (71.1) | 370 | (69.1) | 15 027 | (70.3) | |
| Regional | 1569 | (23.8) | 134 | (25.1) | 4995 | (23.4) | |
| Distant | 206 | (3.1) | 20 | (3.7) | 731 | (3.4) | |
| Unknown | 132 | (2.0) | 11 | (2.1) | 612 | (2.9) | <.007 |
| Histology | |||||||
| Ductal | 4889 | (74.2) | 400 | (74.8) | 14 644 | (68.5) | |
| Lobular | 1023 | (15.5) | 89 | (16.6) | 4886 | (22.9) | |
| Other | 675 | (10.3) | 46 | (8.6) | 1835 | (8.6) | <.0001 |
| HER2 statusb,c | |||||||
| Positive | 390 | (5.9) | 33 | (6.2) | 875 | (4.1) | |
| Negative | 2565 | (38.9) | 228 | (42.6) | 7038 | (32.9) | |
| Borderline | 204 | (3.1) | 16 | (3.0) | 585 | (2.7) | <.0001 |
| Estrogen-receptor (ER)b,c | |||||||
| Positive | 4607 | (69.9) | 434 | (81.1) | 12 539 | (81.7) | |
| Negative | 815 | (12.4) | 56 | (10.5) | 1782 | (11.6) | |
| Borderline | 362 | (5.5) | 24 | (4.5) | 1035 | (6.7) | <.0001 |
| Progesterone-receptor (PR)b,c | |||||||
| Positive | 3956 | (60.1) | 371 | (69.3) | 10 687 | (69.6) | |
| Negative | 1434 | (21.8) | 115 | (21.5) | 3536 | (23.0) | |
| Borderline | 394 | (6.0) | 28 | (5.2) | 1133 | (7.4) | <.0001 |
| Surgeryc | |||||||
| No | 398 | (6.0) | 31 | (5.8) | 1078 | (7.0) | |
| Lumpectomy | 3018 | (45.8) | 291 | (54.4) | 9224 | (60.1) | |
| Mastectomy | 2368 | (36.0) | 192 | (35.9) | 4968 | (32.4) | <.0001 |
| Radiotherapyc | |||||||
| No | 2989 | (45.4) | 224 | (41.9) | 7422 | (48.3) | |
| External beam | 2518 | (38.2) | 258 | (48.2) | 6917 | (45.0) | |
| Other | 147 | (2.2) | <11 | 556 | (3.6) | <.0001 | |
| Chemotherapyc | |||||||
| No | 4610 | (70.0) | 389 | (72.7) | 12 303 | (57.6) | |
| Yes | 1174 | (17.8) | 125 | (23.4) | 3053 | (14.3) | <.043 |
P values for 2-sided Pearson’s χ2 test was used to compare the proportions between ANHPI and NHW cohorts (excluding missing values). SEER, Surveillance, Epidemiology, and End Results; ANHPI = Asian, Native Hawaiian, and Pacific Islander; HER2 = human epidermal growth factor receptor 2; NHW = non-Hispanic White.
Available in SEER registry from 2010. Unknown or borderline HER2 and ER or PR status included “equivocal, indeterminate, undetermined whether positive or negative”.
Idaho, New York, and Massachusetts SEER registries were excluded from the analyses due to unknown treatment, HER2, and receptor status. There were unknown values for HER2 in 12 867 (60.2%) NHW, 3428 (52.0%) Asian, and 258 (48.2%) NHPI women. Unknown ER or PR, chemotherapy, and surgery in 6009 (28.1%) NHW, 803 (12.2%) Asian, 21 (3.9%) NHPI women; and for radiotherapy in 6470 (30.3%) NHW, 933 (14.2%) Asian. “<11” observations was reported and missing numbers were not reported where there were fewer than 11 observations per cell in accordance with the Medicare data confidentiality policy.
Table 3.
Proportions of type II diabetes among 7122 older Asian, Native Hawaiian, and Pacific Islander (ANHPI) and 21 365 non-Hispanic White (NHW) women with breast cancer in SEER-Medicare (2000-2017)a
| Total | Diabetes only before cancer diagnosis (prevalent)b |
Diabetes before and after cancer diagnosis |
Diabetes only after cancer diagnosis (incident)c |
|||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| n = 28 487 | n = 27 048 (95.0%) |
n = 1439 (5.0%) |
n = 22 950 (80.6%) |
n = 5537 (19.4%) |
n = 25 836 (90.7%) |
n = 2651 (9.3%) |
||||||||
| Race | No. | No. | (row %) | No. | (row %) | No. | (row %) | No. | (row %) | No. | (row %) | No. | (row %) | |
| ANHPI | NHW | 21 365 | 20 415 | (95.5) | 950 | (4.5) | 17 761 | (83.1) | 3604 | (16.9) | 19 518 | (91.4) | 1847 | (8.6) |
| Japanese | 1683 | 1610 | (95.7) | 73 | (4.3) | 1348 | (80.1) | 335 | (19.9) | 1467 | (87.2) | 216 | (12.8) | |
| Chinese | 1404 | 1326 | (94.4) | 78 | (5.6) | 1044 | (74.4) | 360 | (25.6) | 1228 | (87.5) | 176 | (12.5) | |
| Filipino | 1382 | 1258 | (91.0) | 124 | (9.0) | 906 | (65.6) | 476 | (34.4) | 1240 | (89.7) | 142 | (10.3) | |
| Other Asian | 875 | 811 | (92.7) | 64 | (7.3) | 649 | (74.2) | 226 | (25.8) | 797 | (91.1) | 78 | (8.9) | |
| Asian Indian or Pakistani | 533 | 483 | (90.6) | 50 | (9.4) | 360 | (67.5) | 173 | (32.5) | 490 | (91.9) | 43 | (8.1) | |
| Korean | 398 | 360 | (90.4) | 38 | (9.6) | 290 | (72.9) | 108 | (27.1) | 353 | (88.7) | 45 | (11.3) | |
| Native Hawaiian | 370 | 345 | (93.2) | 25 | (6.8) | 255 | (68.9) | 115 | (31.1) | 330 | (89.2) | 40 | (10.8) | |
| Vietnamese | 312 | 288 | (92.3) | 24 | (7.7) | 214 | (68.6) | 98 | (31.4) | 268 | (85.9) | 44 | (14.1) | |
| Other Pacific Islander | 165 | 152 | (92.1) | 13 | (7.9) | 123 | (74.5) | 42 | (25.5) | 145 | (87.9) | 20 | (12.1) | |
Mutually exclusive proportions for diabetes only before, before and after, and only after breast cancer. SEER, Surveillance, Epidemiology, and End Results; ANHPI = Asian, Native Hawaiian, and Pacific Islander; NHW = non-Hispanic White.
Existing diabetes cases that occurred before breast cancer reported as proportions.
New diabetes cases after breast cancer reported as proportions (not incidence or rate of occurrence).
Type II diabetes International Classification of Diseases (ICD)-10 diagnosis codes included: E1100, E1101, E1110, E1111, E1121, E1122, E1129, E11311, E11319, E11321, E113211, E113212, E113213, E113219, E11329, E113291, E113292, E113293, E113299, E11331, E113311, E113312, E113313, E113319, E11339, E113391, E113392, E113393, and E113399.
Type II diabetes ICD-9 diagnosis codes included: 25000, 25002, 25010, 25012, 25020, 25022, 25030, 25032, 25040, 25042, 25050, 25052, 25060, 25062, 25070, 25072, 25080, 25082, 25090, and 25092.
Overall, older ANHPI women with breast cancer without prior known history of diabetes had a higher risk of newly diagnosed type II diabetes than their NHW counterparts (Table 4), adjusting for confounding factors. Within 5 years of follow-up, these associations remained consistent for all older ANHPI women with breast cancer without prior known history of diabetes diagnosis, except for older Native Hawaiian women, when compared with older NHW women. After 5 years of follow-up, Japanese, Filipino, and Vietnamese women with breast cancer had a higher risk of diabetes than their NHW counterparts (Table 4).
Table 4.
Hazard ratios of incident type II diabetes among older Asian, Native Hawaiian, and Pacific Islander (ANHPI) and non-Hispanic White (NHW) women with breast cancer overall, within 1 to 5, and over 5 years in SEER-Medicare (2000-2017)a
| Race | >1 year (overall) |
>1-5 years |
>5 years |
||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| HR | (95% CI) | HR | (95% CI) | HR | (95% CI) | HR | (95% CI) | HR | (95% CI) | HR | (95% CI) | ||
| ANHPI | NHW | 1.00 | 0.62 | (0.51 to 0.76) | 1.00 | 0.60 | (0.47 to 0.78) | 1.00 | 0.70 | (0.50 to 0.97) | |||
| Japanese | 1.60 | (1.31 to 1.96) | 1.00 | 1.66 | (1.29 to 2.15) | 1.00 | 1.44 | (1.03 to 2.01) | 1.00 | ||||
| Chinese | 1.46 | (1.17 to 1.83) | 0.91 | (0.68 to 1.22) | 1.67 | (1.29 to 2.18) | 1.01 | (0.71 to 1.43) | 1.08 | (0.70 to 1.66) | 0.75 | (0.44 to 1.28) | |
| Filipino | 2.02 | (1.57 to 2.59) | 1.26 | (0.92 to 1.72) | 1.93 | (1.40 to 2.65) | 1.16 | (0.78 to 1.72) | 2.22 | (1.47 to 3.37) | 1.54 | (0.92 to 2.59)b | |
| Other Asian | 1.35 | (0.99 to 1.84) | 0.84 | (0.59 to 1.21) | 1.49 | (1.02 to 2.18) | 0.90 | (0.57 to 1.41) | 1.11 | (0.65 to 1.88) | 0.77 | (0.42 to 1.42) | |
| Asian Indian or Pakistani | 1.54 | (1.00 to 2.36) | 0.96 | (0.60 to 1.54) | 1.80 | (1.11 to 2.92) | 1.08 | (0.63 to 1.86) | 0.90 | (0.35 to 2.32) | 0.62 | (0.23 to 1.71) | |
| Korean | 1.92 | (1.22 to 3.03) | 1.20 | (0.73 to 1.97) | 2.08 | (1.13 to 3.82) | 1.25 | (0.65 to 2.41) | 1.52 | (0.75 to 3.09) | 1.06 | (0.49 to 2.30)b | |
| Native Hawaiian | 1.73 | (1.10 to 2.70) | 1.08 | (0.66 to 1.75) | 1.69 | (0.99 to 2.87) | 1.02 | (0.57 to 1.82) | 1.59 | (0.67 to 3.79) | 1.10 | (0.44 to 2.76)c | |
| Vietnamese | 2.12 | (1.33 to 2.36) | 1.32 | (0.80 to 2.18) | 1.93 | (1.07 to 3.50) | 1.16 | (0.61 to 2.20) | 2.71 | (1.26 to 5.81) | 1.88 | (0.82 to 4.30)b | |
| Other Pacific Islander | 3.09 | (1.43 to 6.67) | 1.93 | (0.87 to 4.26) | 5.20 | (1.96 to 13.8) | 3.13 | (1.14 to 8.55) | 1.05 | (0.27 to 4.14) | 0.73 | (0.18 to 2.99) | |
Models were adjusted for baseline CCI, cancer registry, residence, education, and income. SEER, Surveillance, Epidemiology, and End Results; ANHPI = Asian, Native Hawaiian and Pacific Islander; NHW = non-Hispanic White; HR = hazard ratio; CI = confidence interval; CCI = Charlson Comorbidity Index.
Change in inferences at over 5 years of follow-up using Cox flexible models were observed for Korean (HR = 1.65, 95% CI = 1.02 to 2.65), Filipino (HR = 1.45, 95% CI = 1.05 to 2.02), and Vietnamese (HR = 1.72, 95% CI = 1.03 to 2.87) compared with NHW women with breast cancer.
Change in inference using competing Fine and Gray model (modeling death as competing risk) within 1 to 5 years of follow-up was observed among Native Hawaiian compared with NHW women with breast cancer (subdistributional HR = 1.65, 95% CI = 1.09 to 2.51).
Among older ANHPI women with breast cancer, more comorbidities at baseline and obesity were risk factors for developing incident type II diabetes, adjusting for potential confounders (Table 5). Income, SES, tobacco use, cancer stage, surgery, radiotherapy, or chemotherapy receipt were not observed as risk factors for type II diabetes among this cohort of older ANHPI women with breast cancer without prior history of diabetes. Older ANHPI women with breast cancer within the less than 5% (fewer) non-high school graduates (higher education) had a lower risk of incident diabetes diagnosis compared with those within the over 20% of non-high school graduates adjusting for potential confounders (Table 5). With the additional adjustment for baseline tobacco and obesity in the sensitivity analysis, except for an elevated risk of diabetes for older Other Asian women with breast cancer (HR = 1.40, 95% CI = 1.03 to 1.90) for the maximum follow-up, the risk estimates were consistent with the primary analysis of diabetes risk in older ANHPI compared with older NHW counterparts (Supplementary Table 1, available online).
Table 5.
Hazard ratios of diabetes risk predictors among 7122 older Asian and NHPI women with breast cancer in SEER-Medicare (2000-2017)
| With Diabetes |
|||||
|---|---|---|---|---|---|
| Risk predictors | n = 804 | (%) | Hazard Ratio | (95% CI) | P trend a |
| Education (census tract)b | |||||
| >20% non-high school graduates | 223 | (27.8) | 1.00 | ||
| 10% to <20% non-high school graduates | 262 | (32.6) | 0.92 | (0.76 to 1.12) | |
| 5% to <10% non-high school graduates | 190 | (23.7) | 0.78 | (0.61 to 0.98) | |
| <5% non-high school graduates | 128 | (15.9) | 0.72 | (0.54 to 0.97) | <.0001 |
| Income (census tract)c | |||||
| ≤$49 999 | 251 | (31.2) | 1.00 | ||
| $50 000–$69 999 | 231 | (28.8) | 0.92 | (0.76 to 1.11) | |
| $70 000–$89 999 | 158 | (19.7) | 0.92 | (0.73 to 1.16) | |
| ≥$90 000 | 163 | (20.3) | 0.94 | (0.72 to 1.23) | .0017 |
| Yost (census tract)d | |||||
| Q1 (lowest SES) | 37 | (7.4) | 1.00 | ||
| Q2 | 71 | (14.1) | 0.93 | (0.62 to 1.39) | |
| Q3 | 71 | (14.1) | 0.76 | (0.51 to 1.14) | |
| Q4 | 120 | (23.9) | 0.73 | (0.50 to 1.06) | |
| Q5 | 203 | (40.4) | 0.76 | (0.53 to 1.08) | <.0001 |
| Baseline CCIe | |||||
| 0 | 598 | (74.4) | 1.00 | ||
| 1 | 150 | (18.6) | 1.34 | (1.12 to 1.61) | |
| ≥2 | 56 | (7.0) | 1.46 | (1.10 to 1.93) | <.0001 |
| Baseline obesityf | |||||
| No | 766 | (95.3) | 1.00 | ||
| Yes | 38 | (4.7) | 1.90 | (1.36 to 2.65) | |
| Baseline tobacco useg | |||||
| No | 790 | (98.3) | 1.00 | ||
| Yes | 14 | (1.7) | 1.48 | (0.87 to 2.52) | |
No associations were observed for cancer stage, surgery type, and receipt of radiotherapy or chemotherapy (data not shown). SEER = Surveillance, Epidemiology, and End Results; NHPI = Native Hawaiian, and Pacific Islander; CCI = Charlson Comorbidity Index; Yost SES = index measure for socioeconomic status.
P trend where applicable (for predictors of 2 or more categories).
Model was adjusted for race, ethnicity, SEER registry, age at cancer diagnosis, income, and residence.
Model was adjusted for race, ethnicity, SEER registry, age at cancer diagnosis, education, and residence.
Model was adjusted for race, ethnicity, SEER registry, age at cancer diagnosis, and residence.
Model was adjusted for race, ethnicity, SEER registry, age at cancer diagnosis, income, education, and residence.
Model was adjusted for race, ethnicity, SEER registry, tobacco use, age at cancer diagnosis, and residence.
Model was adjusted for race, ethnicity, SEER registry, education, and residence.
Discussion
This study is the first to assess the risk of incident diabetes after breast cancer among older Asian women identified from the SEER-Medicare without prior known history of diabetes. The risk of incident diabetes was higher in nearly all older ANHPI women when compared with older HNW women with breast cancer. Older Filipino and Vietnamese women had an elevated 2.20- and 2.75-fold risk of diabetes 5 years after breast cancer, which suggests possible delayed diabetes diagnosis. This is notable given that the highest magnitude in risk is observed within the first 2 years after breast cancer across studies (11,15). In addition, Pacific Islanders (28) and Filipinos (29) have a higher genetic susceptibility to diabetes. Similarly, nonobese Vietnamese Americans were reported to have higher odds of diabetes than NHW (30). Other Pacific Islanders account for only 2.3% in this cohort. Despite this, we observed the strongest magnitude of diabetes risk for Other Pacific Islander women, and our results remain generalizable to older Pacific Islander women who developed breast cancer. Our findings offer valuable insight into the need for future assessment of the current disparities (31) in diabetes after breast cancer among ANHPI women.
Overall, the association between breast cancer and diabetes involves interactions between multiple biological pathways. Diabetes and breast cancer share common risk factors, such as obesity and age (3), and the association may further depend on differences in body mass index (BMI) and baseline risk of diabetes between older ANHPI and NHW women with breast cancer. For instance, the risk of diabetes for Asian populations in the United States is at a lower BMI of greater than 23 kg/m2 compared to the BMI of greater than 25 kg/m2 for other individuals, which does not meet the standard criteria for obesity. In general, Asian women in the United States have lower BMI than NHW women and yet are more likely to have a higher prevalence of diabetes (2,32) and less likely to receive the recommended screening for diabetes (33).
Furthermore, other suggested mechanisms that play a role in both diabetes and breast cancer include inflammation or altered endogenous hormone regulation (34), and yet type II diabetes can result as a complication of breast cancer treatments (35-37). For instance, endocrine therapy modifies insulin sensitivity with blocked estrogen production, which in turn increases the risk of diabetes (35). Others have reported an increase in diabetes risk with the onset of menopause in women receiving chemotherapy due to subsequent weight gain (37). Unlike increased risks post-adjuvant chemotherapy in postmenopausal women after breast cancer reported previously (15), the unobserved treatment-related associations and subsequent risk of diabetes in this study may be in part due to the well-known limitation of underrepresentation of chemotherapy and radiotherapy in cancer registries (38). However, the effects of chemotherapy on weight in Asian women and the risk of diabetes after cancer would be a valuable direction of future research.
Unlike other studies that reported more advanced stage diagnosis and more aggressive treatment in younger minority women (39), we observed smaller proportions of older Asian women diagnosed at advanced cancer stage (regional or distant) than NHW women, and yet a higher proportion of older NHPI received mastectomy (more aggressive treatment) than NHW breast cancer patients. This may suggest potential disparities in the current treatment patterns among the ANHPI women relating to the age and the respective stage of their breast cancer diagnosis. The assessment of increased diabetes risks for women presenting with breast cancer localized stage were observed in ANHPI women except for Other Asian and Other Pacific Islander compared with NHW women. However, there were insufficient observations for the assessment of diabetes risk for regional or distant breast cancer stages (Supplementary Table 3, available online). Other tumor characteristic such as breast cancer subtype showed an increased risk of diabetes for nearly all ANHPI women presenting with ER+ and PR+ tumor subtype compared with NHW women; however, there were insufficient observations for the assessment of diabetes risk by aggressive or ER- and PR- tumor subtype (Supplementary Table 2, available online).
The primary strength of this study is the relatively large sample of older Asian women with breast cancer. We were able to disaggregate the risk of diabetes among the subgroups of ANHPI women with breast cancer without prior known history of diabetes. To our knowledge, this is the first study to evaluate the risk of diabetes over a long follow-up time (mean follow-up time of 8 years) in ANHPI women after being diagnosed with breast cancer. Furthermore, diabetes diagnoses are based on medical claims and are not subject to recall bias. Diabetes is a clinical diagnosis based on plasma glucose criteria; however, errors in ICD coding may result in nondifferential misclassification with bias toward the null. We were able to account for risk factors such as obesity and tobacco use as potential confounders. Although tobacco use is linked with an increased risk of diabetes and many cancers, and there is a suggested association with breast cancer (40), tobacco use was not an observed risk factor for type II diabetes in this study. Our assessment of obesity and tobacco use had limitations because we relied on ICD and Current Procedural Terminology (CPT) codes, which primarily capture severe diagnoses, and we expect an undercount of both with bias toward the null.
Potential limitations include the differences between our study sample and the excluded patients enrolled in HMOs, who are reported to be healthier and younger, with a 9% higher overall survival rate among breast cancer patents (41). Additionally, cancer patients are subject to increased medical surveillance in the initial years after their diagnosis; we observed higher risks of diabetes among older ANHPI women with breast cancer even after 5 years of follow-up despite this limitation. For patients enrolled in Medicare 1 or 2 years before the first appearance of a diabetes diagnosis, it will be unclear whether they had diabetes before enrolling; thus, we excluded enrollees younger than or at 66 years of age from the analysis (42).
Furthermore, the observed overall proportion of incident diabetes among older women with breast cancer was lower than previously reported at 20% among women with breast cancer Medicare recipients diagnosed before 2013 (15). The authors used additional means of detecting diabetes such as prescription medications and did not specify whether they excluded type I diabetes. However, the prevalence of diabetes in our cohort is similar to a cohort of Canadian postmenopausal women (9.7% vs 9.3% in our study) with breast cancer diagnosed before 2008 (13). As with other studies derived from inpatient and outpatient records, our risk estimates are likely underestimated; we still observed an increased risk of diabetes in nearly all ANHPI women compared with NHW women. It is also possible that the risk of type II diabetes may be lower among this cohort of Asian women with breast cancer, as the Asian population was less likely than NHW to receive the recommended screening for diabetes based on the 2012-2014 Behavioral Risk Factor Surveillance System (BRFSS) data (33). Due to the limited sample size for some ANHPI subgroups, it is also possible that some associations were not detected or attenuated, and a large-scale study is needed to confirm the observed associations in this study among older ANHPI women with breast cancer. Furthermore, the inclusion of specific chemotherapy treatments and dosages may potentially reduce residual confounding. This consideration is particularly important as treatment-specific toxicities linked to diabetes risk in women with breast cancer (35) have been suggested.
In conclusion, the findings of this study have important clinical implications for managing diabetes and improving patient care among older ANHPI women with breast cancer. Future research efforts aimed at better understanding the relationship between diabetes risk in older Asian women with breast cancer is warranted.
Supplementary Material
Acknowledgments
The funders had no role in the design of the study; the collection, analysis, and interpretation of the data; the writing of the manuscript; or the decision to submit the manuscript for publication. The findings have not been previously presented or published.
Contributor Information
Alzina Koric, Division of Public Health Sciences, Department of Surgery, Washington University School of Medicine, Saint Louis, MO, USA; Huntsman Cancer Institute, Salt Lake City, UT, USA.
Chun-Pin Esther Chang, Huntsman Cancer Institute, Salt Lake City, UT, USA; Division of Public Health, Department of Family and Preventive Medicine, University of Utah School of Medicine, Salt Lake City, UT, USA.
Yuan-Chin Amy Lee, Huntsman Cancer Institute, Salt Lake City, UT, USA; Division of Public Health, Department of Family and Preventive Medicine, University of Utah School of Medicine, Salt Lake City, UT, USA.
Mei Wei, Huntsman Cancer Institute, Salt Lake City, UT, USA; Division of Oncology, Department of Internal Medicine, University of Utah School of Medicine, Salt Lake City, UT, USA.
Catherine J Lee, Huntsman Cancer Institute, Salt Lake City, UT, USA; Division of Hematology, Department of Internal Medicine, University of Utah School of Medicine, Salt Lake City, UT, USA.
Randa Tao, Huntsman Cancer Institute, Salt Lake City, UT, USA; Department of Radiation Oncology, University of Utah School of Medicine, Salt Lake City, UT, USA.
Jing Wang, Division of Public Health, Department of Family and Preventive Medicine, University of Utah School of Medicine, Salt Lake City, UT, USA.
Djin Tay, College of Nursing, University of Utah, Salt Lake City, UT, USA.
Mia Hashibe, Huntsman Cancer Institute, Salt Lake City, UT, USA; Division of Public Health, Department of Family and Preventive Medicine, University of Utah School of Medicine, Salt Lake City, UT, USA.
Data availability
The datasets used to conduct this study are available upon approval of a research protocol from the National Cancer Institute. Instructions for obtaining these data are available at https://healthcaredelivery.cancer.gov/seermedicare/obtain/.
Author contributions
Alzina Koric, PhD (Writing—Original draft & editing; Formal Analysis), Mia Hashibe, PhD (Funding acquisition; Project administration; Supervision; Writing—review & editing), Esther Chang, PhD (Writing—review & editing; Methodology; Data Quality and Code Check), Yuan-Chin Amy Lee, PhD, Mei Wei, MD, Catherine Lee, MD, Randa Tao, PhD, Jing Wang, PhD, and Djin Tay, PhD (Writing—review & editing).
Funding
Research reported in this publication was supported by the NCI of the NIH under award number R01 CA244326 (M. Hashibe). This study used the SEER-Medicare linked database. The interpretation and reporting of these data are the sole responsibility of the authors. The authors acknowledge the efforts of the National Cancer Institute; the Office of Research, Development, and Information, CMS; Information Management Services (IMS), Inc; and the Surveillance, Epidemiology, and End Results (SEER) Program tumor registries in the creation of the SEER-Medicare database.
This work was supported by the California Department of Public Health as part of the statewide cancer reporting program mandated by California Health and Safety Code Section 103885; the National Cancer Institute’s Surveillance, Epidemiology and End Results Program under contract HHSN261201000140C awarded to the Cancer Prevention Institute of California, contract HHSN261201000035C awarded to the University of Southern California; and contract HHSN261201000034C awarded to the Public Health Institute; and the Centers for Disease Control and Prevention's National Program of Cancer Registries, under agreement #U58DP003862-01 awarded to the California Department of Public Health. The ideas and opinions expressed herein are those of the author(s), and endorsement by the State of California Department of Public Health, the National Cancer Institute, and the Centers for Disease Control and Prevention or their contractors and subcontractors is not intended nor should be inferred. The computational resources used were partially funded by the NIH Shared Instrumentation Grant 1S10OD021644-01A1. This study was additionally supported by National Cancer Institute of the National Institutes of Health (T32CA190194); the content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Conflict of interests
The authors have no conflict of interest to report.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
The datasets used to conduct this study are available upon approval of a research protocol from the National Cancer Institute. Instructions for obtaining these data are available at https://healthcaredelivery.cancer.gov/seermedicare/obtain/.