Abstract
Purpose
This study aimed to analyze the waiting time for initial treatment after breast cancer diagnosis and determine the factors influencing treatment delay in South Korea.
Methods
This nationwide retrospective cohort study was conducted using the Health Insurance Review and Assessment data. The participants were classified according to the regions where their biopsy and treatment were performed (Seoul-Seoul, Metro-Metro, Other-Other, Metro-Seoul, Other-Seoul). Waiting time was analyzed according to regional subgroup, year of diagnosis, and type of treatment. Multivariable logistic regression models were constructed to identify the factors associated with treatment delay (after 30 days of diagnosis).
Results
A total of 133,514 participants newly diagnosed between January 2010 and December 2017 were included in the study. The median waiting time for initial treatment in the total population increased from 8 days, in 2010, to 14 days, in 2017. In the Seoul-Seoul group, the waiting time increased from 10 days, in 2010, to 16 days, in 2017. Although the median waiting time was approximately 10 days in the Metro-Metro and Other-Other groups, it was 27 and 24 days, in the Metro-Seoul and Other-Seoul group, respectively, in 2017. The proportion of delayed upfront surgery by more than 30 days was higher in the Metro-Seoul (odds ratio [OR], 8.088; 95% confidence interval [CI], 7.357–8.893; p < 0.001) and Other-Seoul (OR, 6.210; 95% CI, 5.717–6.750; p < 0.001) groups than in the Metro-Metro (OR, 1.468; 95% CI, 1.352–1.594; p < 0.001) and Other-Other (reference) groups. Previous medical history and treatment at tertiary hospital were observed as factors related to delayed surgery.
Conclusion
Waiting times for breast cancer surgery have increased across all regions of Korea, with those traveling to Seoul experiencing particularly long wait times.
Keywords: Breast Neoplasms; Drug Therapy; Surgical Procedures, Operative; Time-to-Treatment
INTRODUCTION
Breast cancer is the most common cancer among South Korean women, and its incidence has increased [1]. Hence, with the increased accessibility to transportation, an increasing number of patients have been traveling to Seoul for breast cancer treatment [2]. As a result, even high-volume hospitals in Seoul are experiencing strained capacity to meet the increasing demand for treatment, causing a delay in cancer care [3]. Delays in cancer care can generate several concerns [4]. Miles et al. [5] observed that perceived diagnostic delay increased cancer-related distress in colorectal cancer patients. A systemic review reported that treatment delays were associated with lower breast cancer survival [6]. Several retrospective studies showed that the survival rate deteriorated with delayed treatment in early breast cancer patients [7,8,9,10,11]. Accordingly, cancer waiting times (CWT) have been used as targets for quality improvement in cancer care. The UK has introduced targets for maximum latency across cancer treatment pathways: The first treatment should start within 1 month after diagnosis and within 2 months after receiving referral from a general physician [12].
Nonetheless, despite the importance of CWT as a measure of the quality of cancer care, previous studies did not perform a comprehensive assessment of breast cancer treatment delays in South Korea. Therefore, this study aimed to analyze the CWT for initial treatment after breast cancer diagnosis and determine the factors that influence breast cancer treatment delays in the Republic of Korea.
METHODS
Data source and definition
The Health Insurance Review and Assessment (HIRA) manages the assessment of medical services for reimbursement in the Republic of Korea. Data from all the healthcare providers are stored in the HIRA database, consisting of six domains, including general information, healthcare services, prescriptions, diagnosis, medication information, and provider information. An incident breast cancer case is defined as the first time a case is registered with an invasive breast cancer code (C50) according to the International Classification of Diseases, 10th revision (ICD-10) and the V193 code, which is used to claim special reimbursement for the first 5 years of treatment after cancer diagnosis in the Republic of Korea. Moreover, cases which were previously denoted with the C50 codes but without a V193 code are considered prevalent cases.
Study population
From January 2010 to December 2017, 254,796 patients who were assigned the C50 and V193 codes were identified and screened for eligibility for inclusion in this study (Figure 1). Patients who received a C50 code from 2008 to 2009 (n = 87,646) were excluded because these patients were prevalent cases. Among the 167,150 incident breast cancer cases, patients with a history of in situ breast cancer (n = 3,937), male breast cancer (n = 1,214), and recurrent breast cancer (n = 2,642); patients with no previous diagnostic biopsy (n = 8,495), no follow-up record (n = 152), and no record of address (n = 1); patients who did not receive treatment within 1 year after diagnosis (n = 8,045); cases in which treatment initiation occurred 6 months after the diagnosis (n = 1,221); and patients who were diagnosed after 6 months following biopsy (n = 1,846) were excluded from this study. The participants were classified into five groups (Seoul-Seoul, Metro-Metro, Other-Other, Metro-Seoul, and Other-Seoul) according to the geographical regions where the biopsy for breast cancer diagnosis was performed and where the breast cancer treatment was administered, whereas cases from other regional matches were excluded (n = 6,080).
Figure 1. Study enrollment.
Variables and definitions
The diagnosis of breast cancer through biopsy was described using specific codes for pathologic examination claims (C5509, C5911–C5917, C5500, C5504, and C5508). The date on which pathologic examination claims codes were noted prior to the breast cancer diagnosis was taken as the biopsy date. The date on which the C50 plus V193 code were first recorded was considered as the date of breast cancer diagnosis. The claims data recorded within one year after diagnosis were used to determine the occurrence of surgery, chemotherapy, radiotherapy, endocrine therapy, and trastuzumab (Supplementary Table 1).
We categorized each region according to the administrative district of Korea. Seoul is the capital; Daegu, Daejeon, Gwangju, Incheon, Busan, and Ulsan areas were grouped together as metropolitan cities (Metro), while Chungbuk, Chungnam, Gangwon, Gyeongbuk, Gyeonggi, Gyeongnam, Jeju, Jeonbuk, Jeonnam, and Sejong were classified as other regions (Other).
We used the terminologies “upfront surgery” and “primary chemotherapy” while referring to surgery or chemotherapy as the first treatment, respectively. The Charlson comorbidity index (CCI), calculated by using the ICD-10 codes, was recorded. The waiting time was defined as the time period between the diagnosis and treatment and was categorized into five intervals: ≤ 30, 31–60, 61–180 days. Delayed treatment was defined as the treatment that was provided at least 30 days after breast cancer diagnosis.
Statistical analysis
The baseline characteristics of the study cohort were categorized into the five groups based on the regional matches for biopsy and treatment, and the waiting time by regions, treatment, and years of diagnosis were analyzed. The proportion of participants stratified by the waiting time intervals were analyzed. Furthermore, the factors that were associated with delayed treatment were analyzed using multivariable logistic regression models that were adjusted for age at diagnosis, type of insurance, CCI, regional groups, year of diagnosis, and size of the hospital.
Statistical analyses were performed using R version 3.5.1 (R Foundation for Statistical Computing, Vienna, Austria; http://www.r-project.org) and SAS version 9.4.2 (SAS Institute Inc., Cary, NC, USA). This study was approved by the Institutional Review Board (IRB) of Asan Medical Center (IRB No. 2022-1369) and performed in accordance with the principles in the Declaration of Helsinki. Informed consent was not required from the study participants.
RESULTS
Baseline characteristics
Among the 133,514 participants with incident breast cancer diagnosed between January 2010 and December 2017 (Figure 1), the mean age of the total population was 51.8 years, and 126,609 (94.8%) underwent surgery; 91,209 (68.3%) and 93,984 (70.4%) patients received radiotherapy and endocrine therapy, respectively. The proportion of breast cancer patients who received chemotherapy and trastuzumab were 61.8% and 16.5%, respectively (Table 1).
Table 1. Basic characteristics of study population.
| Variables | Seoul-Seoul (n = 54,595) | Metro-Metro (n = 29,732) | Other-Other (n = 33,455) | Metro-Seoul (n = 5,393) | Other-Seoul (n = 10,339) | Total (n = 133,514) | |
|---|---|---|---|---|---|---|---|
| Age at diagnosis (yr) | 51.4 ± 11.1 | 52.8 ± 11.2 | 52.6 ± 11.6 | 49.3 ± 9.71 | 49.7 ± 10.2 | 51.8 ± 11.2 | |
| Insurance | |||||||
| Health insurance | 53,467 (97.93) | 28,314 (95.23) | 32,012 (95.69) | 5,345 (99.11) | 10,227 (98.92) | 129,365 (96.89) | |
| Medicare | 1,128 (2.07) | 1,418 (4.77) | 1,443 (4.31) | 48 (0.89) | 112 (1.08) | 4,149 (3.11) | |
| CCI | 2.12 ± 1.98 | 2.27 ± 2.07 | 2.34 ± 2.16 | 1.98 ± 1.80 | 2.07 ± 1.89 | 2.20 ± 2.03 | |
| Previous diabetes mellitus | 4,778 (8.75) | 3,132 (10.53) | 3,795 (11.34) | 286 (5.30) | 710 (6.87) | 12,701 (9.51) | |
| Previous hypertension | 14,321 (26.23) | 8,870 (29.83) | 10,452 (31.24) | 1,060 (19.66) | 2,329 (22.53) | 37,032 (27.74) | |
| Previous dyslipidemia | 14,301 (26.19) | 8,749 (29.43) | 9,720 (29.05) | 1,162 (21.55) | 2,397 (23.18) | 36,329 (27.21) | |
| Surgery | 51,664 (94.63) | 28,348 (95.35) | 31,338 (93.67) | 5,230 (96.98) | 10,029 (97.00) | 126,609 (94.83) | |
| Chemotherapy | 32,818 (60.11) | 18,566 (62.44) | 20,700 (61.87) | 3,502 (64.94) | 6,891 (66.65) | 82,477 (61.77) | |
| Radiation | 36,984 (67.74) | 19,495 (65.57) | 23,702 (70.85) | 3,773 (69.96) | 7,255 (70.17) | 91,209 (68.31) | |
| Endocrine therapy | 38,336 (70.22) | 20,478 68.88) | 23,857 (71.31) | 3,879 (71.93) | 7,434 (71.90) | 93,984 (70.39) | |
| Trastuzumab | 8,408 (15.40) | 5,328 (17.92) | 5,319 (15.90) | 990 (18.36) | 1,925 (18.62) | 21,970 (16.46) | |
| In-hospital mortality | 2,745 (5.03) | 1,803 (6.06) | 2,103 (6.29) | 251 (4.65) | 476 (4.60) | 7,378 (5.53) | |
| Duration after cohort entry (mo) | 52 (29–78) | 50 (29–75) | 47 (27–73) | 48 (27–70) | 45 (26–68) | 49 (28–75) | |
Values are presented as mean ± standard deviation, number (%) or median (interquartile range).
CCI = Charlson comorbidity index.
Waiting time for breast cancer treatment
The median waiting time for initial treatment in the total population increased from 8 days, in 2010, to 14 days, in 2017 (Table 2). In the Seoul-Seoul group, the median waiting time increased from 10 days, in 2010, to 16 days, in 2017. In the Metro-Metro and Other-Other groups, the median waiting durations were approximately 10 days in 2017. However, in the Metro-Seoul and Other-Seoul groups, the median waiting times were 27 and 24 days, respectively, in 2017. These differences in waiting times between patients who traveled to Seoul and those who were treated in non-Seoul areas were evident in the subgroup of those who underwent upfront surgery (Figure 2A). The trend of longer waiting time for treatment in Seoul than non-Seoul areas was weak for the waiting time for primary chemotherapy (Figure 2B).
Table 2. Breast cancer waiting time for initial treatment by year of diagnosis.
| Regions | 2010 (n = 13,177) | 2011 (n = 14,721) | 2012 (n = 14,901) | 2013 (n = 15,935) | 2014 (n = 16,733) | 2015 (n = 17,547) | 2016 (n = 19,876) | 2017 (n = 20,624) |
|---|---|---|---|---|---|---|---|---|
| Total | 8 (4–16) | 9 (4–16) | 10 (5–16) | 10 (5–17) | 11 (6–19) | 12 (6–20) | 13 (7–22) | 14 (7–25) |
| Seoul-Seoul (day) | 10 (4–17) | 11 (5–19) | 11 (5–17) | 11 (6–18) | 12 (6–19) | 13 (7–21) | 14 (8–24) | 16 (8–27) |
| Metro-Metro (day) | 7 (3–14) | 7 (2–13) | 8 (4–14) | 8 (4–14) | 8 (4–15) | 9 (5–16) | 9 (5–17) | 11 (5–19) |
| Other-Other (day) | 6 (1–10) | 7 (2–12) | 8 (4–13) | 8 (4–14) | 9 (5–16) | 9 (5–15) | 11 (6–17) | 12 (6–19) |
| Metro-Seoul (day) | 19 (12–26.5) | 20 (12–30) | 16 (10–25) | 18 (11–26) | 18 (12–28) | 21 (14–32) | 21 (14–33) | 27 (19–39.8) |
| Other-Seoul (day) | 17 (10–26) | 18 (10–28) | 16 (10–22.8) | 17 (10–26) | 17 (11–25) | 19 (12–29) | 21 (14–31) | 24 (15–35) |
Values are presented as median (interquartile range).
Figure 2. Annual breast cancer waiting time by regions and treatment. (A) Upfront surgery. (B) Primary chemotherapy.
SS = Seoul-Seoul; MM = Metro-Metro; OO = Other-Other; MS = Metro-Seoul; OS = Other-Seoul.
During the study period, 90.3% and 90.2% of breast cancer patients received upfront surgery or primary chemotherapy at least within 30 days. From 2010 to 2017, the proportion of patients who underwent upfront surgery within 30 days following diagnosis had decreased over time (Supplementary Table 2); in 2017, it was 79.4% in the Seoul-Seoul group, 90.4% in the Metro-Metro group, 94.0% in Other-Other group, 51.6% in Metro-Seoul group, and 63.8% in Other-Seoul group. The proportion of patients who received primary chemotherapy at 30 days or less after their diagnosis had decreased over time since 2010 (Supplementary Table 3); the proportion was the highest in the Seoul-Seoul group, in 2017 (88.2%). The waiting times between patients who traveled to Seoul and the those who were treated in non-Seoul areas were similar, at approximately 80%.
Factors associated with delayed treatments
The multivariate analyses considered the risk factors for delayed upfront surgery (after 30 days of diagnosis) included a high CCI, regions where the treatment was administered, year of diagnosis, and treatment at tertiary hospitals (Table 3). Patients aged 60 or above showed a trend of undergoing delayed upfront surgery, but without any association with the type of health insurance. Compared to the Other-Other group, the Metro-Seoul and Other-Seoul groups were significantly associated with delayed surgery.
Table 3. Factors associated with delayed upfront surgery more than 30 days.
| Variables | No. of cases | No. of events | Proportion (%) | OR | 95% CI | p-value | ||
|---|---|---|---|---|---|---|---|---|
| Lower | Upper | |||||||
| Age at diagnosis (yr) | ||||||||
| < 40 | 11,223 | 1,066 | 9.5 | Reference | ||||
| 40–49 | 38,260 | 3,778 | 9.9 | 1.061 | 0.985 | 1.143 | 0.120 | |
| 50–59 | 33,574 | 3,253 | 9.7 | 1.040 | 0.963 | 1.123 | 0.320 | |
| ≥ 60 | 26,068 | 2,502 | 9.6 | 1.080 | 0.995 | 1.174 | 0.068 | |
| Insurance | 109,125 | |||||||
| Health insurance | 105,850 | 10,371 | 9.8 | Reference | ||||
| Medical aid | 3,275 | 228 | 7.0 | 1.067 | 0.923 | 1.229 | 0.373 | |
| CCI (continuous) | NA | NA | NA | 1.017 | 1.005 | 1.028 | 0.004 | |
| Regions | ||||||||
| Other-Other | 27,465 | 1,042 | 3.8 | Reference | ||||
| Seoul-Seoul | 43,535 | 4,971 | 11.4 | 2.815 | 2.625 | 3.022 | < 0.001 | |
| Metro-Metro | 25,876 | 1,459 | 5.6 | 1.468 | 1.352 | 1.594 | < 0.001 | |
| Metro-Seoul | 4,145 | 1,200 | 29.0 | 8.088 | 7.357 | 8.893 | < 0.001 | |
| Other-Seoul | 8,104 | 1,927 | 23.8 | 6.210 | 5.717 | 6.750 | < 0.001 | |
| Year of diagnosis | ||||||||
| 2010 | 10,749 | 591 | 5.5 | Reference | ||||
| 2011 | 12,064 | 772 | 6.4 | 1.223 | 1.094 | 1.369 | < 0.001 | |
| 2012 | 12,474 | 652 | 5.2 | 0.909 | 0.809 | 1.021 | 0.108 | |
| 2013 | 13,241 | 900 | 6.8 | 1.185 | 1.063 | 1.323 | 0.002 | |
| 2014 | 13,918 | 1,191 | 8.6 | 1.506 | 1.357 | 1.673 | < 0.001 | |
| 2015 | 14,357 | 1,579 | 11.0 | 2.110 | 1.909 | 2.335 | < 0.001 | |
| 2016 | 16,013 | 2,190 | 13.7 | 2.721 | 2.471 | 3.000 | < 0.001 | |
| 2017 | 16,309 | 2,724 | 16.7 | 3.473 | 3.160 | 3.822 | < 0.001 | |
| Hospital | ||||||||
| Others | 32,313 | 1,160 | 3.6 | Reference | ||||
| Tertiary hospital | 76,812 | 9,439 | 12.3 | 2.446 | 2.292 | 2.613 | < 0.001 | |
OR = odds ratio; CI = confidence interval; CCI = Charlson comorbidity index; NA = not available.
DISCUSSION
This nationwide retrospective study showed that patients diagnosed with breast cancer in non-Seoul regions and who traveled to Seoul for treatment had longer CWT than their counterparts. From 2010 to 2017, both the CWT and regional differences increased in all regions. The increasing trend of CWT was more prominent in the case of upfront surgery than for primary chemotherapy. Medical history and tertiary hospitals were factors that were related to delayed upfront surgery. Higher age was associated with a trend of delayed surgery.
To the best of our knowledge, this is the first comprehensive report of CWT in the Republic of Korea. Compared with the result from other countries, the CWT in South Korea was relatively short. In the US, among the 246,957 breast cancer patients who were diagnosed between 1995 and 2005, as per the from the National Cancer Data Base, only 65.9% were treated within 30 days after their diagnosis [13]. Moreover, among the breast cancer patients diagnosed between 1992 and 2009 by the Surveillance, Epidemiology, and End Results-Medicare database in the US, 96% of the patients underwent surgery within 60 days and 77.7% received surgery within 30 days of diagnosis [10]. In Australia, among patients with low-urgency breast cancer, between 2006 and 2011, 94.1% of the patients underwent surgery within 90 days, whereas, between 2012 and 2015, 90.8% received surgery within 90 days after diagnosis [14]. According to the National Health Service statistics on CWT, between 2019 and 2020, 89.4% of breast cancer patients started their first treatment within 2 months (62 days) after receiving a referral from a general physician in the UK [15]. Meanwhile, evaluation of date from other European countries showed that, among esophageal or gastric cancer patients who were diagnosed between 2006 and 2012 in Sweden, 90.8% and 68.2% started treatment within 60 and 30 days of diagnosis, respectively [16]. Lastly, in Singapore, from 2005 to 2011, the proportion of breast cancer patients who received their first treatment within 60 and 30 days of diagnosis was 85.4% and 64.5%, respectively [17]. The common trend in the US, Europe, and Asia was that the rate of first treatment initiation or surgery within 30 days after diagnosis was only 60%–70%. A possible reason for the similar patterns in many countries with different medical policies and backgrounds could be medical supply, which inevitably has limits. In our data, 90% of the patients who were diagnosed with breast cancer in Korea between 2010 and 2017 received their first treatment or upfront surgery within 30 days after the diagnosis, and this finding suggests the agility of the healthcare system in Korea as compared with that in other countries.
Furthermore, although the CWT in Korea can be considered relatively acceptable compared with the CWT in other countries, the overall increase of CWT along with the increasing number of breast cancer patients is noteworthy [1]. In addition, among patients who had breast biopsy for diagnosis in non-Seoul areas and traveled to Seoul for treatment, the proportion of treatment delays was higher than those in the other patients. This trend has worsened over time and can be explained by the effect of medical travel [18]. The Korean government initiated the Regional Cancer Center Support Program in 2004, designating 12 university hospitals as Regional Cancer Centers since 2012 to enhance cancer care quality and reduce regional disparities in cancer treatment across the country. Even with the financial support, the number of breast cancer patients traveling to Seoul for treatment has continued to increase. Therefore, considering the current situation, long-term plans for efficient medical resource allocation are needed.
An interesting finding of the present study is that primary chemotherapy was initiated relatively early in Seoul. In the case of primary chemotherapy initiation in metropolitan and other areas, the proportion of patients who received treatment after 60 days or more were greater in Seoul. From this, it can be inferred that the long interval to CWT is attributable to time and space constraints. Compared to surgical intervention, there are relatively fewer resource limitations for chemotherapy. However, we are unsure whether this acceptability will be maintained when the CWT is prolonged as the overall number of breast cancer patients increases.
The question whether a treatment delay affects cancer survival remains controversial. In two retrospective studies [7,8], delayed treatment was associated with poor survival outcomes in breast cancer patients (adjusted hazard ratio, 1.5–2.0). In another study conducted in the US [9], the 5-year survival rate was lower in patients who waited longer for surgery (p = 0.005). Additionally, a large-scale case series study conducted using the National Cancer Database in the US found that breast cancer patients who underwent surgery nine weeks or more after their diagnosis had a significantly worse overall survival rate (p < 0.001) [19]. Furthermore, similar results for chemotherapy have been reported for patients with metastatic breast cancer [17]. However, in some studies [18,20,21], treatment delay was unrelated to survival. In the present study, a survival analysis according to the CWT was not performed. Therefore, it is difficult to determine the relationship between treatment delay and the survival rate. Delaying the start of treatment may often cause anxiety, which reduces the quality of life and negatively affects mental health [5,16,22]. Although the effect of delayed treatment on breast cancer survival is unclear, efforts to shorten the CWT are an important factor for quality improvement in breast cancer care.
The findings of this study are influenced by the following limitations. First, factors that could potentially affect CWT, such as demographic and disease characteristics, were not included in the HIRA data. Therefore, such factors were not considered in this analysis. Second, our analysis may be limited to Korea or countries that have similar medical practices. Third, although the present study showed the CWT of breast cancer treatment in South Korea, the effect on CWT on survival outcomes was not investigated. Although Table 1 presents in-hospital mortality data, it contains only very limited information for analyzing survival outcomes. Further studies are needed to assess whether the CWT is associated with adverse effects on breast cancer survival.
In conclusion, the findings of this study indicate that South Korean breast cancer patients may have better access to timely treatment compared with the patients in other countries. However, the CWT of breast cancer has been increasing over time and has particularly increased rapidly in patients who seek breast cancer surgeries in Seoul. Despite the financial support, this trend has continued to worsen. Consequently, policies for efficient resource allocation and nationwide studies may require evaluation of the effect of this phenomenon on treatment outcomes in patients with breast cancer.
ACKNOWLEDGMENTS
We express our gratitude to the Health Insurance Review and Assessment Service for providing the nationwide claims data.
Footnotes
Funding: This study was supported by a grant from the Asan Institute for Life Sciences and Corporate Relations of Asan Medical Center, Seoul, Republic of Korea (2022IP0064-1).
Conflict of Interest: The authors declare that they have no competing interests.
Presentation: This study was presented at the 74th Annual Congress of the Korean Surgical Society on November, 5, 2022.
- Conceptualization: Lee JW, Chung IY.
- Data curation: Jeong JH, Jung J, Chung IY.
- Formal analysis: Lee YJ, Chung IY.
- Investigation: Lee YJ, Kim J.
- Methodology: Lee YJ, Yoo TK, Lee SB, Ko BS, Kim HJ, Son BH, Chung IY.
- Project administration: Chung IY.
- Resources: Lee YJ, Chung IY.
- Software: Jeong JH, Jung J, Chung IY.
- Supervision: Yoo TK, Lee SB, Kim J, Ko BS, Kim HJ, Lee JW, Son BH, Chung IY.
- Validation: Chung IY.
- Visualization: Chung IY.
- Writing - original draft: Lee YJ.
SUPPLEMENTARY MATERIALS
Electronic data interchange codes of treatments and generic codes of medications
Breast cancer waiting time for upfront surgery by year of diagnosis
Breast cancer waiting time for primary chemotherapy by year of diagnosis
References
- 1.Kang SY, Lee SB, Kim YS, Kim Z, Kim HY, Kim HJ, et al. Breast cancer statistics in Korea, 2018. J Breast Cancer. 2021;24:123–137. doi: 10.4048/jbc.2021.24.e22. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Jeong JH, Jung J, Kim HJ, Lee JW, Ko BS, Son BH, et al. Domestic medical travel from non-Seoul regions to Seoul for initial breast cancer treatment: a nationwide cohort study. Ann Surg Treat Res. 2023;104:71–79. doi: 10.4174/astr.2023.104.2.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Healthcare Bigdata Hub. Find a medical institution. 2022. [Accessed May 15, 2022]. http://gisopendata.hira.or.kr/map.do .
- 4.Bleicher RJ, Ruth K, Sigurdson ER, Ross E, Wong YN, Patel SA, et al. Preoperative delays in the US Medicare population with breast cancer. J Clin Oncol. 2012;30:4485–4492. doi: 10.1200/JCO.2012.41.7972. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Miles A, McClements PL, Steele RJ, Redeker C, Sevdalis N, Wardle J. Perceived diagnostic delay and cancer-related distress: a cross-sectional study of patients with colorectal cancer. Psychooncology. 2017;26:29–36. doi: 10.1002/pon.4093. [DOI] [PubMed] [Google Scholar]
- 6.Richards MA, Westcombe AM, Love SB, Littlejohns P, Ramirez AJ. Influence of delay on survival in patients with breast cancer: a systematic review. Lancet. 1999;353:1119–1126. doi: 10.1016/s0140-6736(99)02143-1. [DOI] [PubMed] [Google Scholar]
- 7.Yun YH, Kim YA, Min YH, Park S, Won YJ, Kim DY, et al. The influence of hospital volume and surgical treatment delay on long-term survival after cancer surgery. Ann Oncol. 2012;23:2731–2737. doi: 10.1093/annonc/mds101. [DOI] [PubMed] [Google Scholar]
- 8.Shin DW, Cho J, Kim SY, Guallar E, Hwang SS, Cho B, et al. Delay to curative surgery greater than 12 weeks is associated with increased mortality in patients with colorectal and breast cancer but not lung or thyroid cancer. Ann Surg Oncol. 2013;20:2468–2476. doi: 10.1245/s10434-013-2957-y. [DOI] [PubMed] [Google Scholar]
- 9.Smith EC, Ziogas A, Anton-Culver H. Delay in surgical treatment and survival after breast cancer diagnosis in young women by race/ethnicity. JAMA Surg. 2013;148:516–523. doi: 10.1001/jamasurg.2013.1680. [DOI] [PubMed] [Google Scholar]
- 10.Bleicher RJ, Ruth K, Sigurdson ER, Beck JR, Ross E, Wong YN, et al. Time to surgery and breast cancer survival in the United States. JAMA Oncol. 2016;2:330–339. doi: 10.1001/jamaoncol.2015.4508. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Khorana AA, Tullio K, Elson P, Pennell NA, Grobmyer SR, Kalady MF, et al. Time to initial cancer treatment in the United States and association with survival over time: an observational study. PLoS One. 2019;14:e0213209. doi: 10.1371/journal.pone.0213209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Bate A, Baker C, Mackley A. NHS Cancer Targets. London: House of Commons Library; 2018. [Google Scholar]
- 13.Bilimoria KY, Ko CY, Tomlinson JS, Stewart AK, Talamonti MS, Hynes DL, et al. Wait times for cancer surgery in the United States: trends and predictors of delays. Ann Surg. 2011;253:779–785. doi: 10.1097/SLA.0b013e318211cc0f. [DOI] [PubMed] [Google Scholar]
- 14.Prang KH, Canaway R, Bismark M, Dunt D, Miller JA, Kelaher M. The impact of public performance reporting on cancer elective surgery waiting times: a data linkage study. BMC Health Serv Res. 2021;21:129. doi: 10.1186/s12913-021-06132-w. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Richardson J, Ubaldo AR, Dai D, McDonnell P. Waiting Times for Suspected and Diagnosed Cancer Patients: 2019-20 Annual Report. London: National Health Service; 2020. [Google Scholar]
- 16.Song H, Fang F, Valdimarsdóttir U, Lu D, Andersson TM, Hultman C, et al. Waiting time for cancer treatment and mental health among patients with newly diagnosed esophageal or gastric cancer: a nationwide cohort study. BMC Cancer. 2017;17:2. doi: 10.1186/s12885-016-3013-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Ho PJ, Cook AR, Binte Mohamed Ri NK, Liu J, Li J, Hartman M. Impact of delayed treatment in women diagnosed with breast cancer: a population-based study. Cancer Med. 2020;9:2435–2444. doi: 10.1002/cam4.2830. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Neal RD, Tharmanathan P, France B, Din NU, Cotton S, Fallon-Ferguson J, et al. Is increased time to diagnosis and treatment in symptomatic cancer associated with poorer outcomes? Systematic review. Br J Cancer. 2015;112(Suppl 1):S92–107. doi: 10.1038/bjc.2015.48. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Wiener AA, Hanlon BM, Schumacher JR, Vande Walle KA, Wilke LG, Neuman HB. Reexamining time from breast cancer diagnosis to primary breast surgery. JAMA Surg. 2023;158:485–492. doi: 10.1001/jamasurg.2022.8388. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Brazda A, Estroff J, Euhus D, Leitch AM, Huth J, Andrews V, et al. Delays in time to treatment and survival impact in breast cancer. Ann Surg Oncol. 2010;17(Suppl 3):291–296. doi: 10.1245/s10434-010-1250-6. [DOI] [PubMed] [Google Scholar]
- 21.Mujar M, Dahlui M, Yip CH, Taib NA. Delays in time to primary treatment after a diagnosis of breast cancer: does it impact survival? Prev Med. 2013;56:222–224. doi: 10.1016/j.ypmed.2012.12.001. [DOI] [PubMed] [Google Scholar]
- 22.Jones RV, Greenwood B. Breast cancer: causes of patients’ distress identified by qualitative analysis. Br J Gen Pract. 1994;44:370–371. [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Electronic data interchange codes of treatments and generic codes of medications
Breast cancer waiting time for upfront surgery by year of diagnosis
Breast cancer waiting time for primary chemotherapy by year of diagnosis