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Cancer Research and Treatment > Epub ahead of print
Hwang, Yoo, Lee, Kim, Ko, Kim, Lee, Son, and Chung: Implementation of BRCA Test among Young Breast Cancer Patients in South Korea: A Nationwide Cohort Study

Abstract

Purpose

This study aimed to investigate the frequency of BRCA testing and related factors among young breast cancer patients (age < 40 years) in South Korea

Materials and Methods

We conducted a nationwide retrospective cohort study using data from the Health Insurance Review and Assessment claims. Newly diagnosed breast cancer patients younger than 40 were included. Annual BRCA testing ratios (number of BRCA test recipients/the number of patients undergoing breast cancer surgery in each year) were analyzed by region and health care delivery system. We investigated the location of breast cancer diagnosis and BRCA testing.

Results

From January 2010 to December 2020, there were 25,665 newly diagnosed young breast cancer patients, of whom 12,186 (47.5%) underwent BRCA testing. The BRCA testing ratios increased gradually from 0.084 (154/1,842) in 2010 to 0.961 (1,975/2,055) in 2020. Medical aid (vs. health insurance) and undergoing surgery in metropolitan cities or others (vs. Seoul), general hospitals, and clinics (vs. tertiary hospitals) were associated with a lower likelihood of BRCA testing. While 97.8% of the patients diagnosed in Seoul underwent BRCA testing in Seoul, 22.9% and 29.2% of patients who were diagnosed in metropolitan areas and other regions moved to Seoul and underwent BRCA testing, respectively.

Conclusion

The frequency of BRCA testing has increased over time in South Korea, with Seoul showing a particularly high rate of testing. About one-quarter of patients diagnosed with breast cancer outside of Seoul moved to Seoul and underwent BRCA testing.

Introduction

Breast cancer gene (BRCA) testing can identify individuals who have a higher risk of developing breast or ovarian cancer. This genetic testing can inform patients of management and treatment decisions, such as personalized surveillance or risk reduction surgery [1]. This can also be important for managing family members who may benefit from genetic counseling or testing [2].
Recently, with the development of olaparib, a poly(ADP ribose) polymerase inhibitor, the significance of BRCA mutation testing is increasing. Breast cancer patients with a BRCA mutation and human epidermal growth factor receptor 2 (HER2)–negative status, who can benefit from olaparib, show a proportion of approximately 7% [3]. In metastatic breast cancer, olaparib monotherapy reduced the risk of disease progression or death by 42% compared to standard therapy [4]. In patients who received local treatment with adjuvant or neoadjuvant chemotherapy, olaparib was associated with an improvement in invasive disease-free survival or distant metastasis-free survival [5].
While BRCA testing can be beneficial for some patients, not all individuals with a family history of breast cancer or other risk factors may be eligible for or benefit from testing. Testing can be expensive and may not be accessible to all patients, although in Korea it is covered by national insurance [6]. In addition, genetic counseling, which is an important component of the testing process [7], is not always feasible due to limited personnel availability [8,9]. It is expected that there will be variations in genetic counseling practices depending on the hospital’s circumstances; therefore, it is necessary to identify the disparities in the implementation of genetic testing.
As management strategies for mutation carriers continue to evolve, the significance of BRCA testing is emphasized, and it is now more crucial than ever to comprehend how this testing is being utilized in the real world. In this study, we investigated the annual implementation of BRCA testing in South Korea using national insurance claims data and identified regional or temporal variations in testing.

Materials and Methods

1. Data sources

Our data was obtained from the Health Insurance Review and Assessment (HIRA) database, which contains nationwide claims data from all healthcare providers in South Korea [10]. The data includes six domains of information: general demographics, healthcare services, prescriptions, diagnoses, medication information, and provider information. Breast cancer cases were identified using the International Classification of Diseases, 10th revision (ICD-10) code for invasive breast cancer (C50) and the V193 code, which is a reimbursement code for cancer treatment within the first 5 years after cancer diagnosis.

2. Definitions

Among the indications for reimbursement for BRCA testing, one that could be identified with national insurance data was the age at breast cancer diagnosis. Because BRCA tests for patients under the age of 40 have been covered by the national insurance from the beginning and the tests for patients aged 40 have started to be covered from July 2020, we only included patients under 40 in the analysis. We used ICD-10 codes to analyze the basic demographics of the patients, including their Charlson comorbidity index (CCI). Underlying diseases were defined using ICD-10 codes and prescriptions, such as hypertension (I10-13, 15) and diabetes mellitus (E10-14). Surgery, chemotherapy, radiation, endocrine therapy, and trastuzumab were considered as conducted if performed within one year of breast cancer diagnosis [11]. Patients who underwent surgery for the initial benign breast disease or in situ carcinoma within 3 months before the breast cancer diagnosis were regarded to have undergone breast cancer surgery in this analysis [12]. The date when the C50 with V193 code first appeared was set as the date of breast cancer diagnosis. We also investigated the locations of breast cancer diagnosis and BRCA testing.

3. Variables

The BRCA testing ratio was defined as the number of patients tested for BRCA in a specific unit during a given year, divided by the number of patients who underwent surgery in a particular region or health care delivery system. Annual frequencies of BRCA tests were analyzed according to the region or health care delivery system. Regions were divided into three categories based on the administrative districts of Korea. The first category was Seoul, and the second category, known as metropolitan cities, included Daejeon, Daegu, Busan, Gwangju, Incheon, and Ulsan. The remaining regions were classified as other regions. The health care delivery system was categorized into tertiary hospitals, general hospitals, and clinics, according to the classification of the Ministry of Health and Welfare.

4. Statistical analysis

The number and ratio of breast cancer patients, patients who underwent surgery, and patients who received BRCA testing were analyzed by year. Factors related to the implementation of BRCA testing were identified using a multivariable logistic regression model, and age at diagnosis, insurance type, CCI (continuous variable), regions of surgery, health care delivery system, and year of diagnosis were adjusted. We used Sankey diagram to depict the locations of breast cancer diagnosis and BRCA testing. We used R ver. 4.3.0 (Vienna, Austria; http://www.r-project.org) and SAS ver. 9.4 (SAS Institute Inc., Cary, NC) for statistical analysis.

Results

1. Identification of eligible patients for BRCA testing

From January 2010 to December 2020, a total of 338,751 individuals were diagnosed with breast cancer; of them, 88,167 patients who had been recorded with either the C50 or D05 code from January 2008 to December 2009 were excluded from the study. There were 250,584 newly diagnosed cases of breast cancer reported after washing out. Among them, we excluded 7,234 cases of carcinoma in situ recurrence, 365 cases without follow-up, and 217,320 cases aged 40 and above. Finally, 25,665 patients with breast cancer younger than 40 years were included in the study (Fig. 1).

2. Baseline characteristics

The mean follow-up duration of the study population was 63.4 months, and the BRCA test was conducted on 47.5% (12,186/25,665) of the participants. The mean age at diagnosis was 35.1 years, and 98.9% had health insurance while 1.1% had medical aid. The mean CCI score was 1.5. Surgery was performed in 88.5% (22,719/25,665) of cases, chemotherapy in 64.1% (16,446/25,665), radiation therapy in 56.4% (14,473/25,665), and trastuzumab in 15.6% (3,397/25,665) (Table 1).

3. Trends in the implementation of BRCA testing

The number of surgeries for breast cancer gradually increased in Seoul, from 1,034 cases in 2010 to 1,217 cases in 2020. However, there was no significant change in metropolitan cities and other regions (S1 Table). BRCA testing ratios increased in all three regions, with the largest increase observed in Seoul (0.108 in 2010 to 1.061 in 2020). In 2020, the BRCA testing ratio was 0.973 in metropolitan cities and 0.692 in other regions (Fig. 2A, S2 Table). The annual frequency of BRCA testing implementation had increased in all health care delivery system, with the largest increase observed in tertiary hospitals (0.096 in 2010 to 0.977 in 2020) (Fig. 2B, S2 Table).

4. Factors associated with the implementation of BRCA testing

The age at diagnosis was inversely correlated with the likelihood of BRCA testing. Compared to patients with health insurance, those covered by medical aid received fewer BRCA tests (odds ratio [OR], 0.432; 95% confidence interval [CI], 0.320 to 0.578; p < 0.001). The increase in the number of examinations according to CCI was marginal, despite statistical significance (OR, 1.022; 95% CI, 1.002 to 1.042; p=0.028). Comparison based on the geographical location of the surgery showed that BRCA tests were less likely to be conducted in metropolitan cities (OR, 0.528; 95% CI, 0.486 to 0.573; p < 0.001) and other regions (OR, 0.516; 95% CI, 0.357 to 0.558; p < 0.001) compared to Seoul. Also, fewer tests were performed in general hospitals (OR, 0.860; 95% CI, 0.796 to 0.928; p < 0.001) and clinics (OR, 0.447; 95% CI, 0.357 to 0.558; p < 0.001) than in tertiary hospitals. Compared to 2010, the later the year of surgery, the more tests were performed (Table 2).

5. Location of breast cancer diagnosis and BRCA testing

For most of the patients diagnosed with breast cancer in Seoul and received a BRCA test, the test was conducted in Seoul (97.8%, 6,498/6,644). Out of the patients diagnosed with breast cancer in metropolitan cities and received a BRCA test, 71% (1,692/2,363) of the tests were conducted in metropolitan cities, while 22.9% (541/2,363) moved to Seoul and underwent testing. For patients who were diagnosed with breast cancer in other regions and received a BRCA test, 67.0% (2,130/3,179) of the tests were conducted in other regions, while 29.2% (929/3,179) moved to Seoul and underwent testing. Of the patients diagnosed in Seoul, metropolitan cities, and other regions, 47.3% (5,957/12,601), 58.2% (3,294/5,657), and 57.1% (4,228/7,407) did not undergo BRCA testing (Fig. 3).

Discussion

We found that between 2010 and 2020, the frequency of BRCA testing in breast cancer patients undergoing surgery has continued to increase, especially in Seoul. BRCA testing ratios increased in all health care delivery system, and the ratio in tertiary hospitals reached a plateau in 2018. BRCA testing was performed more often among individuals who were younger, had health insurance, had no co-morbidity, operated in Seoul, operated in tertiary hospitals, and were more recent. The majority of patients who were diagnosed with breast cancer in Seoul (97.8%) underwent testing in Seoul. In contrast, in metropolitan areas and other regions, a significant number of cases moved to Seoul and underwent BRCA testing (22.9% and 29.2%, respectively).
To our knowledge, this is the first nationwide study to report the implementation of BRCA testing in real practice and provide data for a possible explanation of the testing patterns. Previous studies have also reported chronological increases in the number of BRCA tests; however, the number of cases was limited as it was conducted in a single institution [13]. While other studies included only patients from specific regions [14] or patients with specific private insurance [15], our study was able to account for regional differences within a nation and identify the factors that contribute to these differences.
There was a study from South Korea that reported major cities had more tests than rural areas [16]. Another study identified differences in the frequency of BRCA testing according to geographic locations in the United States [17]. Additionally, a study using the Employer-Sponsored Health Insurance in the United States found that nonmetropolitan areas had significantly fewer BRCA tests compared to metropolitan areas and had significantly fewer cases of receiving magnetic resonance imaging within 90 days or 1 year after testing [18]. In our study, we traced the location of breast cancer diagnosis and BRCA testing of patient. Although there were differences in testing ratios between regions, a significant number of patients from non-Seoul areas were assumed to have moved to Seoul for breast cancer treatment, suggesting that the low testing ratios in non-Seoul areas reported in previous studies may have been underestimated.
We determined the ratios for BRCA testing based on patients who underwent surgery. Most patients were expected to receive BRCA testing at the site where they were receiving treatment, rather than at the site where they received the breast cancer diagnosis, for the convenience of testing and of correlating the testing results with the surgical procedures or adjuvant therapy. Of the study patients who underwent BRCA testing, 92.1% underwent surgery. The proportion of breast cancer cases in which BRCA testing was performed but surgery was not performed was low (7.9%); therefore, there was no difficulty in observing the overall trend, and it was an appropriate method to compare BRCA testing behavior by region or health care delivery system.
We identified that a significant number of patients diagnosed with breast cancer in metropolitan cities or elsewhere moved to Seoul and received BRCA testing. There was a report stating that in 2017, 19.8% of breast cancer patients in regions outside of Seoul moved to Seoul for their initial treatment; furthermore, compared to patients aged 60 or older, those younger than 40 were 94% more likely to move to Seoul for their treatment [11]. BRCA test also showed the same trend, which is likely because the initial treatment site and the site where BRCA testing is conducted usually coincide. However, the low ratio of BRCA testing in patients treated outside of Seoul cannot be solely attributed to the migration of patients, as the testing ratio in non-Seoul patients was only slightly lower than that in Seoul. While genetic counseling is required for BRCA testing, it is currently not covered by Korea’s national insurance. In one study, 55.6% of respondents in a professional survey said that financial burden was a challenge in genetic counseling [19]. In our study, the testing ratio was low in patients with medical aid, suggesting that there are additional barriers beyond insurance for these patients, who are exempt from most of their medical expenses [20]. It is known that patients may decline genetic counseling for various reasons, including concerns about the future impact of test results, emotional repercussions for themselves and their families, and a low perceived risk of cancer [21-23]. It is possible that psychological factors are distributed differently depending on the region.
In Korea, the National Health Insurance has covered BRCA testing since 2008, and there have been several studies on BRCA in Koreans, such as the Korean Hereditary Breast Cancer (KOHBRA) study [24,25]. From May 2012, reimbursement indications were specified for breast cancer patients under the age of 40, those with a second-degree family history of breast or ovarian cancer, those with bilateral breast cancer, those with multiple organ cancer, as well as male breast cancer and ovarian cancer patients. From July 2020, the reimbursement criteria were expanded to include breast cancer patients aged 40 and triple-negative patients aged 60 years or younger. The criteria for determining family history have also been expanded to include breast cancer, ovarian cancer, male breast cancer, metastatic prostate cancer, and pancreatic cancer within the patient’s third-degree relatives. The definition of multiple organ cancer was specified as breast cancer combined with either ovarian cancer or pancreatic cancer [26]. In our study, the pattern of annual increase in BRCA testing ratio did not match the expansion of major expansions in insurance standards, suggesting that there are other factors contributing to the pattern.
Although olaparib was not included in South Korea’s national insurance system, it was approved by South Korea’s Ministry of Food and Drug Safety for the treatment of metastatic breast cancer in October 2019 [27], and as an adjuvant treatment for early breast cancer in February 2023 [28]. In our study, there were a certain number of patients in other regions who did not receive BRCA testing even in 2020. With the introduction of olaparib and the increasing importance of confirming BRCA mutations, patients with an indication for testing should be informed to aid in their decision-making.
Since this study utilized nationwide claims data, information regarding hormone receptor or HER2 status, family history, and bilaterality—aside from age—was not available among the national insurance reimbursement indications for BRCA testing. And our study didn’t include patients aged 40. However, age under 40 years alone was helpful in identifying trends in BRCA testing ratios among people with indications. The BRCA mutation can also be diagnosed through multigene panel testing [29], but it was not additionally included in the analysis, as it may overlap with standalone BRCA tests and could be captured in national claims data only since February 2018, which was nearly the end of our study period. Since the timing and location of BRCA testing for some patients were different from those of breast cancer diagnosis, we had to calculate the ratio, rather than the proportion or rate, of BRCA-tested patients to the total number of patients who underwent surgery. However, since it would be rare for the time of surgery and BRCA testing to be significantly different, there would be no disruption to the overall trend. Although we were able to identify the increases or decreases in the test ratio by region and hospital size, the specific cause could not be determined.
The frequency of BRCA testing has increased over time in all regions of Korea. Especially, Seoul showed a higher frequency of BRCA testing compared to those of metropolitan areas or other areas. Also, about one-quarter of patients diagnosed in metropolitan cities and other regions moved to Seoul for medical purposes and underwent BRCA testing.

Electronic Supplementary Material

Supplementary materials are available at Cancer Research and Treatment website (https://www.e-crt.org).

Notes

Ethical Statement

This study was conducted in accordance with the principles outlined in the Declaration of Helsinki and approved by the Institutional Review Board of Asan Medical Center (IRB No. 2022-1369). Informed consent was not required from study subjects as it was waived by the board due to the retrospective nature of the study and the use of de-identified data.

Author Contributions

Conceived and designed the analysis: Chung IY.

Collected the data: Chung IY.

Contributed data or analysis tools: Chung IY.

Performed the analysis: Hwang YH, Chung IY.

Wrote the paper: Hwang YH.

Writing - review and editing: Hwang YH, Yoo TK, Lee SB, Kim J, Kim HJ, Ko BS, Lee JW, Son BH, Chung IY.

Conflicts of Interest

Conflict of interest relevant to this article was not reported.

Fig. 1.
Study flowchart.
crt-2023-1186f1.jpg
Fig. 2.
Annual BRCA testing ratio in young breast cancer patients (< 40 years). (A) By region. (B) By health care delivery system. BRCA testing ratio: ratio of the number of patients tested to the number of patients according to the region or health care delivery system in that unit in a given year.
crt-2023-1186f2.jpg
Fig. 3.
Sankey diagram of the location of breast cancer diagnosis and BRCA testing.
crt-2023-1186f3.jpg
Table 1.
Basic characteristics of study population
Characteristic Value (n=25,665)
Age at diagnosis (yr) 35.1±3.8
Type of insurance
 Health insurance 25,382 (98.9)
 Medical aid 283 (1.1)
 Charlson comorbidity index 1.5±1.4
 Previous diabetes mellitus 329 (1.3)
 Previous hypertension 1,049 (4.1)
 Previous dyslipidemia 1,162 (4.5)
 Surgery 22,719 (88.5)
 Chemotherapy 16,446 (64.1)
 Radiation 14,473 (56.4)
 Endocrine therapy 15,587 (60.7)
 Trastuzumab 3,997 (15.6)
 BRCA testing 12,186 (47.5)
 In-hospital mortality 1,877 (7.3)
 Duration after entry 63.4±37.8

Values are mean±standard deviation or number (%). BRCA, breast cancer gene.

Table 2.
Factors associated with BRCA testing in young breast cancer patients
Characteristic No. of cases No. of events Proportion (%) Odd ratio M-H, Fixed (95% CI) p-value
Age at diagnosis NA NA NA 0.911 (0.905-0.918) < 0.001
Type of insurance
Health insurance 25,382 12,114 47.7 Reference
Medical aid 283 72 25.4 0.432 (0.320-0.578) < 0.001
CCI (continuous) NA NA NA 1.022 (1.002-1.042) 0.028
Location of the hospital where the surgery was performed
 Seoul 13,132 7,376 56.2 Reference
 Metropolitan cities 4,206 1,684 40 0.528 (0.486-0.573) < 0.001
 Others 5,381 2,169 40.3 0.516 (0.479-0.557) < 0.001
Health care delivery system where the surgery was performed
 Tertiary hospital 17,336 9,146 52.8 Reference
 General hospital 4,829 1,958 40.5 0.860 (0.796-0.928) < 0.001
 Clinics 554 125 22.6 0.447 (0.357-0.558) < 0.001
Year of diagnosis
 2010 2,289 388 17 reference
 2011 2,346 472 20.1 1.218 (1.046-1.419) 0.011
 2012 2,160 623 28.8 2.042 (1.762-2.369) < 0.001
 2013 2,177 752 34.5 2.706 (2.342-3.131) < 0.001
 2014 2,308 931 40.3 3.508 (3.045-4.047) < 0.001
 2015 2,170 982 45.3 4.323 (3.750-4.992) < 0.001
 2016 2,469 1,356 54.9 6.788 (5.905-7.816) < 0.001
 2017 2,474 1,522 61.5 9.091 (7.899-10.482) < 0.001
 2018 2,370 1,617 68.2 12.547 (10.867-14.515) < 0.001
 2019 2,518 1,819 72.2 14.886 (12.889-17.226) < 0.001
 2020 2,384 1,724 72.3 15.970 (13.979-18.523) < 0.001

BRCA, breast cancer gene; CCI, Charlson comorbidity index; CI, confidence interval; M-H, Mantel-Haenszel; NA, not available.

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