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Characteristics and chronologically changing patterns of late-onset breast cancer in Korean women of age ≥ 70 years: A hospital based-registry study

Abstract

Background

Women from Asian and western countries have vastly different ages of onset of breast cancer, with the disease tending to occur at an older age in the West. Through an investigation of the patterns of old-onset breast cancer (OBC) in Korean women, we aimed to identify the characteristics of Korean OBC and evaluate whether these patterns are changing in relation to increasing westernization.

Methods

This study retrospectively evaluated 102,379 patients who underwent surgical treatment of primary breast cancer between January 1, 2000 and December 31, 2013 in Korea. We used hospital -based breast cancer registry and analyzed data from these patients using multiple linear regression analysis to compare the characteristics and chronologically changing patterns between OBC (70 years of age or older) and non-OBC (40–69 years of age) patients in Korea.

Results

A total of 6% of the 102,379 patients had OBC. Overall, OBC had more favorable biological features, such as a higher incidence of luminal A subtype, than did non-OBC, except for a higher incidence rate of triple-negative breast cancer (TNBC). However, OBC also presented with a higher overall disease stage, including higher T and M stages. Although the incidence rates of both OBC and non-OBC have increased overtime, the relative proportion of OBC patients has slightly increased, whereas that of non-OBC has slightly decreased. The increase in the incidence of both OBC and non-OBC was primarily due to the luminal A subtype.

Conclusions

Based on a hospital-based registry, overall, Korean OBC had favorable biological features but showed a higher rate of TNBC and advanced cancer stages. The incidence trend of breast cancer in Korea is slowly shifting toward an older age at onset, largely due to the luminal A subtype. Our results may provide novel insights into OBC in Asia, and aid in the development of optimal management of the disease in Asia.

Trial registration

Retrospectively registered.

Peer Review reports

Background

Currenly, breast cancer is the most prevalent among other famale malignancies globally [1, 2]. Because the incidence of breast cancer and the associated mortality have been shown to increase with age in developed countries, aging is recognized as the strongest risk factor for the disease [3]. Although the incidence and mortality associated with breast cancer have been decreasing in developed countries since the early 2000s, this trend is less significant or even reversed among elderly women [4]. In 2012, breast cancer in women aged 70 years or older accounted for 30.1% of the entire new breast cancer diagnoses and 51.2% of breast cancer mortalities in developed countries [3]. Moreover, with the global population trend in aging, late-onset breast cancer diagnosis poses a significant disease burden. More attention is now directed towards the epidemiology, clinical and biological aspects, and clinical results of old-onset breast cancer (OBC) than of non-OBC [3, 5].

Regarding breast cancer, Asia faces more rapid increases in the incidence rate than does the West [6]. In 2020, Asians accounted for, 1,026,171 (45.4%) of the 2,261,419 new diagnoses of breast cancer worldwide [7]. Asian and western populations are starkly different in terms of their breast cancer-related epidemiologic and biologic profiles [8,9,10]. Noticeably, the peak age at disease onset is much younger in Asia than in the West (40–50 years vs. 60–70 years) [8]. Despite the lower incidence rate in the older age group in Korean women, the incidence rate increased mostly in the oldest group, age ≥ 70 years. It was reported as 2.3 times among women in their thirties, 2.5 times among those in their forties, 2.6 times among women in their fifties, 3.4 times among those in their sixties, and 3.8 times among women in their seventies, between 1998 and 2010 [11]. Nevertheless, most of the global research studies on breast cancer in elderly women have focused on western populations, and there is a relative lack of relevant data for Asian populations [3].

We intended to assess the features of breast cancer in elderly Korean women and determine the variations in the incidence and subtypes of OBC over time. Finally, we also intended to evaluate the future trends in OBC in Korea.

Methods

Korean Breast Cancer Registry

The entire dataset on breast cancer cases in this study were derived from the Korean Breast Cancer Registry (KBCR). The KBCR is a multiinstituional, online breast cancer database collected in a prospective manner (http://registry.kbcs.or.kr/ecrf/login.php), which was estalished by the Korean Breast Cancer Society (KBCS) 〔11〕. More than100 instituions with over 400 beds each volountarilly took part in this registry 〔11〕. In 2013, it was assumed that this registry would reflect over 65% of new breast cancer cases detected in Korea [12]. The KBCR provides diverse data on breast cancer research, beyond basic registry data (sex, age), encompassing social circumstances (region, education level, marital status), clinical information (body mass index, history of breast feeding, menopausal status), pathological results (histological features, stage in accoradence with the American Joint Committee on Cancer classification, biomarker expressions of estrogen receptors [ERs], progesterone receptors [PRs], human epidermal growth factor receptor 2 [HER2]), and treatment methods (surgery, neoadjuvant, adjuvant therapy) 〔11〕.

By contrast, the Korean Central Cancer Registry (KCCR) is a nationwide cancer database established by the Korean Ministry of Health and Welfare, and the KCCR data includes the entire cancer cases in Korea (https://kccrsurvey.cancer.go.kr/index.do). However, the KCCR only contains cancer data confined to general epidemiology (incidence, mortality, survival rate), brief patient information (age, sex, and region) .

Definition of OBC and breast cancer incidence

Previous studies on breast cancer in older women show inconsistencies in the definition of the OBC cutoff age [3, 13,14,15,16]. We defined OBC as breast cancer developing in a woman aged 70 years or older. We further defined breast cancer incidenace as the number of newly detected breast cancer case per 100 Korean women per year 〔17〕. The exclusion criteria were breast cancer cases without information on cancer stage or surgical methods used. Therefore, the incidence of breast cancer, as reported in our study, is not equal to the whole breast cancer incidence in Korea recorded by the nation-wide registry data.

Definition of breast cancer subtypes

In respect of molecular subtype classification of breast cancer, immunohistochemical surrogates for ER, PR, HER2 status were used to determine breast cancer subtypes. Positivity or negetivity of ER and PR expression was solely based on immunohistochemistry (IHC) staining, whereas positivity or negetivity of HER2 expression was based on both IHC staining and in situ hybridization (fluorescence [FISH] or silver [SISH] in situ hybridization methods). IHC reults of zero or 1+ (week) HER2 staining were considered to have a negative HER2 status, whereas those with 3 + (strong) HER2 staining were considered to have a positive. For cases with 2+ (equivocal) HER2 staining, FISH or SISH results that determined the the final HER2 expression; cases with positive FISH or SISH results were considered as HER2-positive, whereas those with negative FISH or SISH results were considered as HER2-negative. Cases with missing FISH or SISH results were determined as having an unknown HER2 status.

According to the status of hormone receptor and HER2 expression, patients were classified into four breast cancer subtypes. These subtypes included ‘luminal A’: postive-ER and/or PR and negative-HER2; ‘luminal B’: positive-ER and/or PR and positive- HER2; ‘triple negative breast cancer (TNBC)’: negative - ER and PR and negative -HER2; ‘HER2’: negative-ER and PR and postive–HER2.

Study population (Fig. 1)

This study attained an approval from the Instituional Review Board of Haeundae Paik Hospital (Institutional Review Board file no. 2019–09-010). The KBCS anonymized and de-identified personal information from the records for the protection of patient privacy.

Fig. 1
figure 1

Patient selection. LCIS, lobular carcinoma in situ

For this analysis, we excluded male patients, patients aged less than 40 years, those with a histopathology of lobular carcinoma in situ, phyllodes tumor, sarcoma and lymphoma, cases without data on age, types of surgery, pathological stages, and those diagnosed prior to the year 2000 owing to their questionable reliability. Patients younger than 40 years of age were excluded from the non-OBC group because young-age breast cancer (under 40 years of age) is reported to have dissimilar clinicopathological characteristics compared with older-age breast cancer (age 40 years and older) [17]. In addition, the issue of patients aged less than 40 years had already been intensively dealt and analyzed in the preceding study which used the identical database and study period as this study [17]. In this retrospective study drawn from a hostpial-based Korean registry, we finally included 102,379 patients who underwent surgical treatment of primary breast cancer from January 1, 2000 to December 31, 2013 in Korea.

Based on this dataset, we compared between the OBC and non-OBC groups to assess the features of OBC and examine chronological changes in incidence rates of OBC. To assess chronological changes in subtypes, we performed subset analysis of 76,349 cases having accurate data on status of ER, PR, and HER2 expression.

Statistical analysis

Regarding comparison between the OBC and non–OBC groups, clinicopathological features presented as categorial variables were compared using Fisher’s exact or Chi-squared test. However, those presented as continous variables were compared using Mann-Whitney U or independent test. A large amount of data on clinicopathological variables were missing, and the missing data were excluded from the analysis. To check the normality of the distribution, we used the Shapiro-Wilk test. To compare changes in the frequencies, incidences, and proportions with time among different age and subtype groups, we performed multiple linear regression test and checked interaction effects between variables regarding changes. Bonferroni-corrected p values were calculated for multiple comparison tests. Estimates of the frequency and incidence of each subtype were derived by the slope of the regression line, which represents the annual rate of change in the frequency and incidence. For all statistical analyses, SPSS version 24.0 was used, and p values less than 0.05 were idenified as having statistial significance.

Results

Clinicopathological features of OBC in Korea

Of a total of 102,379 patients, 6.0% had OBC. A comparison of the OBC and non-OBC data is shown in Tables 1 and 2. OBC was diagnosed at the mean age of 73 (range, 70–108) years. Patients with OBC were significantly more likely to have late menarche, late menopause, an early first delivery, high parity, lactation experience, be obese, have a lower education level, have undergone fewer previous mammographic screenings, a more symptomatic initial presentation including palpation of the tumor, undergone a total mastectomy, as well as lower rates of breast reconstruction, chemotherapy, and radiation therapy. OBC tumors showed favorable biologic features, except for a higher proportion of TNBC. Those favorable biologic features included a lower histologic grade, weaker lymphovascular invasion, higher negative HER2 status, a higher proportion of the luminal A subtype, and lower proportions of the luminal B and HER2 subtypes. However, OBC was associated with aggressive clinical manifestations related to symptomatic presentation, degree of palpation of the tumor, degree of negative PR expression, and advanced pathologic stage (advanced T, M, and overall stages).

Table 1 Clinical characteristics of elderly Korean women with breast cancer
Table 2 Pathological and biological characteristics of elderly Korean women with breast cancer

Korean breast cancer occurence according to ages (Fig. 2)

The frequencies and incidence rates of total breast cancer, non-OBC, and OBC significantly increased with time (p < 0.001 for all). The frequency and incidence rates of OBC increased more radiply than did the non-OBC and total breast cancer (p < 0.001 for both frequency and incidence rate, from the regression analysis after Bonferroni correction). The proportion of OBC cases neared 4% in 2000. And this low proportion of OBC cases increased annually to 7.6% in 2013.

Fig. 2
figure 2

Breast cancer occurence with time (frequency, incidence rate, proportion) within age subgroups. The age subgroups that are compared are 40–69 and ≥ 70 years

Korean breast cancer occurence according to the subtypes within different ages (Figs. 3, 4)

We assessed how the frequency and incidence have changed with time according to the subtype within each age group. In the OBC group, both the frequency and incidence of all subtypes significantly increased with time (p < 0.001 for all, Fig. 3). However, regarding incidence, the rate of increase was significantly more higher in the luminal A subtype than did the remaining subtypes (p < 0.001). In descending order of numerical value, the frequencies of subtypes were estimated as 33.36 (luminal A), 8.25 (TNBC), 5.40 (HER2), and 4.31 (luminal B), respectively. In addition, their incidence were estimated as 0.000133 (luminal A), 0.000033(TNBC), 0.000021 (HER2), and 0.000017 (luminal B), respectively. Of all the subtypes, the incidence of the luminal A subtype increased the fastest, and the associated rate of increase was four to eight times higher than that of the other subtypes (p < 0.001).

Fig. 3
figure 3

Breast cancer development (frequency, incidence rate) by subtype (luminal A, B, HER2, TNBC). Two age subgroups were compared (i.e., 40–69 and ≥ 70 years) among patients with old-onset breast cancer. HER, human epidermal growth factor receptor; TNBC, triple-negative breast cancer

Fig. 4
figure 4

Breast cancer development (frequency, incidence rate) by subtype (luminal A, B, HER2, TNBC). Two age subgroups were compared (i.e., 40–69 and ≥ 70 years) among patients with non-old-onset breast cancer. HER, human epidermal growth factor receptor; TNBC, triple-negative breast cancer

In the non-OBC group, both the frequency and incidence of all the subtypes significantly increased with time (p < 0.001 for all, Fig. 4). In descending order of numerical value, the frequencies of subtypes were estimated as 397.45 (luminal A), 71.20 (HER2), 70.56 (luminal B), and 64.91 (TNBC), respectively. Moreover, the estimates of their incidence were 0.00157 (luminal A), 0.00028 (HER2), 0.00028 (luminal B), and 0.00025 (TNBC), respectively. Of all the subtypes, the luminal A subtype demonstrated the fastest increase in incidence, and the associated rate of increase was about six times higher than that of the other subtypes (p < 0.0001).

Future trend in the proportion of OBC in Korea

Based on data from the KBCR, the porportion of OBC was low (6%) in Korea. However, the increase rate was steeper in OBC than non-OBC; consequently, the relative proportion of OBC has increased slowly over time. Assuming that the current trend persists, the relative proportion of OBC will eventually proceed toward the values reported in western countries.

Discussion

This hospital-based database study showed that, in Korea, OBC has clinicopathological characteristics that are distinct from those of non-OBC, and that the incidences of total breast cancer, OBC, and non-OBC have continuously increased in the country. Noticeably, the increase in the incidence of OBC was slightly steeper than that of non-OBC in Korea; as a result, the proportion of OBC has been slowly increasing. The increase in the incidence of the luminal A subtype of breast cancer predominantly contributed to the increase in the incidence of both OBC and non-OBC, whereas increases in the incidence of other subtypes were relatively less evident.

In 2012, in the developed world, the ratio of female patinets with breast cancer at age ≥ 70 years accounted for 32.1% of all female patients with breast cancer at age ≥ 40 years [3]. Breast cancer incidence in Korea peaks at ages 45–49 years and, thereafter, declines with age [18]. In 2015, later-onset breast cancer at age ≥ 70 years account for only 8.8% of all breast cancer in Korea [17]. This pattern is unlike that noted in western countries, in which the incidence continuously increases with increasing age [8]. Although the proportion of OBC cases is still lower in Korea than in the West, our data show that the trend is shifting toward the values observed in the West, clearly indicating that age significanly increases the risk of breast cancer in the country. By 2050, the population of people who are 70 years or older is expected to rise sharply, up to 30.4% of the total population [19]. Considering the synergistic effect of the steep degree in population aging in Korea [19], the degree of increase in the relative ratio of OBC cases in the country may be larger than expected because the values noted in the West may be reached sooner than expected. The increase in the incidence of OBC can be attributed to prolonged life expectancy, which results in age-related biological alterations such as ER hypersensitivity, mammary epithelial cell changes, tumor microenvironment changes, and immune senescence that can increase one’s susceptibility to breast cancer [3].

In this study, OBC in Korea showed favorable biological features, except for the higher proportion of TNBC cases; however, there were discordantly advanced stages. OBC is considered to be different from non-OBC [3, 16]. Generally, OBC is characterized by favorable biological features, including a low tumor grade, low lympho-vascular invasion, histological types with good prognoses, more expressions of ER and PR, diploid and B-cell lymphoma 2 (Bcl-2) protein, and lesser expressions of HER2, Ki67, p53, and epidermal growth factor receptor [5, 14, 16, 20,21,22,23,24,25,26,27,28,29,30]. A recent meta-analysis focusing on OBC arrived at a parallel conclusion [3]. However, OBC is associated with a larger tumor size, greater lymph node involvement, a greater number of stage IV metastatic disease cases, and a more advanced overall tumor stage [3, 5, 14, 16, 25,26,27, 31,32,33,34,35]. Moreover, contrary to the general belief of the indolent course of OBC, growing evidence points to worse outcomes in older breast cancer patients [5, 33, 36]. The reasons for the worse outcomes in older patients can be attributed to under-treatment or variable disease biology, even within the same subtype [36]. Although breast cancer seemed to be more idolent in older patients than in younger ones, additional biological and genetic differences can exist even within similar disease subtypes [36].

Discrepancies between favorable biological features and advanced stages in OBC can be partly explained by an altered biological environment related to aging, which facilitates rapid disease progression, and also by society-related mechanisms such as the exclusion of elderly people from screening, or the notion of OBC being less aggressive, leading to diagnostic delays and the provision of proper care [3]. Along with omission of mammographic screening and self-breast examination, low perception of breast cancer in elderly women may also result in delayed diagnosis [26, 33].

Existing literature on OBC demonstrates great heterogeneities in terms of cancer stage, size, grade, and lymph node status at presentation, and clinical results in elderly women relative to their younger counterparts [3, 14, 16, 37]. The results of these parameters varied by study design and population, and either decreased or increased, or did not change with age [3, 14, 16, 37]. On average, elderly patients show a higher tumor stage than younger patients [14, 26, 33,34,35]. However, the proportion of those with an unknown stage increases with age because data on primary, nodal, and metastatic tumor statuses are frequently missed in elderly people [3, 14, 33, 34, 38]. Missing data in elderly populations can also be partly attributed to the discrepancy in terms of why breast cancer at older age demonstrate less aggressiveness in cancer biology despite its higher cancer stage at diagnosis, in contrast to breast cancer at younger age [14].

The distribution of breast cancer subtypes greatly fluctuates because of the complex effects of both age and race/ethnicity [39,40,41,42,43,44,45]. Regardless of race/ethnicity, the luminal subtype is universally the most predominant and is associated with the highest lifetime risk. Further, almost half of all luminal cancers develop after age 70 [40]. Breast cancer is biologically heterogeneous and intricate, and subtype alterations depending on age also vary with race [39]. A California-based study compared the proportions of breast cancer subtypes between between women groups at two different ages (40–69 years vs. ≥ 70 years), and evaluated how differently breast cancer subtypes varied according to age, depending on race [39]. The proportion of luminal A subtype cases increased after age 70 across people of all races, except Caucasians [39]. For White women, the proportion of the luminal A subtype was not influenced by age [39]. In Asian/Pacific Islander women, the proportion of the remaining subtypes other than luminal A did not change after age 70 [39]. Our data on native Korean women also show that the proportion of the luminal A subtype significantly after age 70. The global rise in the proportion of postmenopausal breast cancer and the luminal A subtype is regarded to be principally attributable to the global trend of acculturation to the Western lifestyle, including a high dietary consumption of animal fat, increased body mass index, and altered reproductive activities, such as nullipara, first childbirth at older age [17, 46,47,48]. For native Korean women, the increased incidence of the luminal A subtype was largely responsible for the overall increased incidence of both OBC and non-OBC, implying that environmental factors were predominantly responsible for the increased incidence of breast cancer in those aged 40 years and older.

In previous California-based studies, age did not significantly increase the risks of the TBNC and HER2 subtypes among Asian/Pacific Islander women [39, 49]. However, our data show that the proportion of all breast cancer subtypes did change after age 70. The proportion of the TNBC and luminal A subtypes significantly increased after age 70, whereas that of both the HER2+ and luminal B subtypes significantly decreased after that age. A recent study conducted in the United States showed that TNBC accounted for 8.4% of the 1,151,724 breast cancer cases [50]; this proportion varied according to race: 8.0% for non-Hispanic Whites, 18.1% for non-Hispanic Blacks, and 7.2% for Asians [50]. Compared with the proportion (7.2%) of TNBC observed in Asian-Americans [50], the proportions of the same in native Koreans (17.9% for OBC, 16.0% for non-OBC) are much higher, reaching the value (18.1%) observed in non-Hispanic Blacks. In the aforementioned population-based study, the proportion of TNBC cases decreased with age: 18.7, 10.5, 9.6, 7.7, 7.2% for ages < 40, 40–49, 50–64, 65–74, and ≥ 75 years, respectively), in accordance with the results of a California-based study [39]. However, interestingly, the proportion of TNBC cases in native Korean women increased after age 70. When considering the high proportion (23.8%) of TNBC cases among native Koreans under the age of 40 [17], the incidence of TNBC could have a bimodal peak before age 40 and after age 70 in native Korean women.

Our data, derived from the hospital-based voluntary cancer registry (KBCR), provide more specific information on patient and tumor characteristics, surpassing those derived from the nationwide obligatory cancer registry (KCCR). Nevertheless, the presence of selection bias cannot be ruled out. First, it cannot be guaranteed that KBCR data are fully representative of the actual breast cancer status in Korea. In fact, a period from 2000 to 2013, the proportions of OBC according to two major registry data were 6.0% (6104/102,379) in the KBCR, and 8.1% (11,162/137,540) in the nationwide cancer registry [51]. Table 3 summarizes annual difference in enrolled datasets between KBCR and KCCR. Indeed, in KBCR, enrolling institution and registered patients per each institution fluctuated annually because data collections were voluntarily carried out and altered by variable individual circumstances, which could influence results. However, our KBCR data can be somewhat representative of all Korean breast cancer cases. In terms of the differences in the proportions of OBC cases, as observed in the KBCR and nationwide registry, the 95% confidence interval of the difference was − 2.36 and − 1.95%, and the equivalence margin was 3%. Second, the matter of selection bias still persists for the subgroup analysis, as there were numerous cases with missing data on clinicopathological characteristics.

Table 3 Korean Breast Cancer Society’s registry relative to Korean central cancer registry datasets 2000–2013

Conclusions

In conclusion, based on a hospital-based database in Korea, although OBC in Korea was associated with favorable biological features, it showed a greater rate of the TNBC subtype and advanced disease stage. Currently, the Korean society continues to undergo popolution aging, and, accordingly, older Korean women ≥70 years old increasingly experienced breast cancer. Therefore, the management of breast cancer in this particular age group is expected to emerge as an urgent clinical issue in the near future. To lay the foundation for the management of OBC in Korea, there is a need for a comprehensive understanding of the disease’s characteristics, including the associated tumor biology and differences from non-OBC. Future studies should focus on this. Our results may provide novel insights into OBC in Korea, and aid in the development of optimal management of the disease in the country.

Availability of data and materials

The Korean Breast Cancer Registry, which was used for this study, is available with the permission of the Korean Breast Cancer Society. The corresponding author will provide information on where data supporting the results reported in this article can be found, including, where applicable, hyperlinks to publicly archived datasets analyzed or generated during the study.

Abbreviations

DCIS:

Ductal carcinoma in situ

ER:

Estrogen receptor

FISH:

Fluorescence in situ hybridization

HER:

Human epidermal growth factor receptor

IDC:

Invasive ductal carcinoma

IHC:

Immunohistochemistry

ISH:

In situ hybridization

KBCR:

Korean Breast Cancer Registry

KBCS:

Korean Breast Cancer Society

KCCR:

Korean Central Cancer Registry

OBC:

Old-onset breast cancer

PR:

Progesterone receptor

SISH:

Silver in situ hybridization

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.

    Article  PubMed  Google Scholar 

  2. Ferlay J, Ervik M, Lam F, Colombet M, Mery L, Piñeros M, et al. Global cancer observatory. Cancer Today. 2018; https://gco.iarc.fr/today. Accessed 4 Jan 2019.

  3. Lodi M, Scheer L, Reix N, Heitz D, Carin AJ, Thiébaut N, et al. Breast cancer in elderly women and altered clinico-pathological characteristics: a systematic review. Breast Cancer Res Treat. 2017;166:657–68.

    Article  PubMed  CAS  Google Scholar 

  4. Smith BD, Jiang J, McLaughlin SS, Hurria A, Smith GL, Giordano SH, et al. Improvement in breast cancer outcomes over time: are older women missing out? J Clin Oncol. 2011;29:4647–53.

    Article  PubMed  Google Scholar 

  5. van de Water W, Markopoulos C, van de Velde CJ, Seynaeve C, Hasenburg A, Rea D, et al. Association between age at diagnosis and disease-specific mortality among postmenopausal women with hormone receptor-positive breast cancer. JAMA. 2012;307:590–7.

    PubMed  Google Scholar 

  6. Shin HR, Joubert C, Boniol M, Hery C, Ahn SH, Won YJ, et al. Recent trends and patterns in breast cancer incidence among Eastern and southeastern Asian women. Cancer Causes Control. 2010;21:1777–85.

    Article  PubMed  Google Scholar 

  7. Ferlay J, Ervik M, Lam F, Colombet M, Mery L, Piñeros M, et al. Global cancer observatory: cancer today breast cancer fact sheets; 2020. https://gco.iarc.fr/today/data/factsheets/cancers/20-Breast-fact-sheet.pdf. Accessed 23 March 2021.

    Google Scholar 

  8. Leong SP, Shen ZZ, Liu TJ, Agarwal G, Tajima T, Paik NS, et al. Is breast cancer the same disease in Asian and western countries? World J Surg. 2010;34:2308–24.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Youlden DR, Cramb SM, Yip CH, Baade PD. Incidence and mortality of female breast cancer in the Asia-Pacific region. Cancer Biol Med. 2014;11:101–15.

    PubMed  PubMed Central  Google Scholar 

  10. Green M, Raina V. Epidemiology, screening and diagnosis of breast cancer in the Asia–Pacific region: current perspectives and important considerations. Asia Pac J Clin Oncol. 2008;4:S5–S13.

    Article  Google Scholar 

  11. Ko BS, Noh WC, Kang SS, Park BW, Kang EY, Paik NS, et al. Changing patterns in the clinical characteristics of Korean breast cancer from 1996-2010 using an online nationwide breast cancer database. J Breast Cancer. 2012;15:393–400.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Min SY, Kim Z, Hur MH, Yoon CS, Park EH, Jung KW, et al. The basic facts of Korean breast cancer in 2013: results of a nationwide survey and breast cancer registry database. J Breast Cancer. 2016;19:1–7.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Syed BM, Green AR, Nolan CC, Morgan DA, Ellis IO, Cheung KL. Biological characteristics and clinical outcome of triple negative primary breast cancer in older women - comparison with their younger counterparts. PLoS One. 2014;9:e100573.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Schonberg MA, Marcantonio ER, Li D, Silliman RA, Ngo L, McCarthy EP. Breast cancer among the oldest old: tumor characteristics, treatment choices, and survival. J Clin Oncol. 2010;28:2038–45.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Chatzidaki P, Mellos C, Briese V, Mylonas I. Does primary breast cancer in older women (≥80 years) have unfavorable histological characteristics? Arch Gynecol Obstet. 2011;284:705–12.

    Article  PubMed  Google Scholar 

  16. Diab SG, Elledge RM, Clark GM. Tumor characteristics and clinical outcome of elderly women with breast cancer. J Natl Cancer Inst. 2000;92:550–6.

    Article  PubMed  CAS  Google Scholar 

  17. Lee SK, Kim SW, Yu JH, Lee JE, Kim JY, Woo J, et al. Is the high proportion of young age at breast cancer onset a unique feature of Asian breast cancer? Breast Cancer Res Treat. 2019;173:189–99.

    Article  PubMed  Google Scholar 

  18. Kang SY, Kim YS, Kim Z, Kim HY, Lee SK, Jung KW, et al. Basic findings regarding breast cancer in Korea in 2015: data from a breast cancer registry. J Breast Cancer. 2018;21:1–10.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Projected population by age group (Korea). http://kosis.kr/eng/statisticsList/statisticsListIndex.do?menuId=M_01_01&vwcd=MT_ETITLE&parmTabId=M_01_01&statId=1962001&themaId=#SelectStatsBoxDiv. Accessed 26 Jan 2017.

  20. Albrektsen G, Heuch I, Thoresen SØ. Histological type and grade of breast cancer tumors by parity, age at birth, and time since birth: a register-based study in Norway. BMC Cancer. 2010;10:226.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Ma CD, Zhou Q, Nie XQ, Liu GY, Di GH, Wu J, et al. Breast cancer in Chinese elderly women: pathological and clinical characteristics and factors influencing treatment patterns. Crit Rev Oncol Hematol. 2009;71:258–65.

    Article  PubMed  Google Scholar 

  22. Anderson WF, Pfeiffer RM, Dores GM, Sherman ME. Comparison of age distribution patterns for different histopathologic types of breast carcinoma. Cancer Epidemiol Biomark Prev. 2006;15:1899–905.

    Article  Google Scholar 

  23. Daidone MG, Coradini D, Martelli G, Veneroni S. Primary breast cancer in elderly women: biological profile and relation with clinical outcome. Crit Rev Oncol Hematol. 2003;45:313–25.

    Article  PubMed  Google Scholar 

  24. Fisher CJ, Egan MK, Smith P, Wicks K, Millis RR, Fentiman IS. Histopathology of breast cancer in relation to age. Br J Cancer. 1997;75:593–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Mathew J, Lee S, Syed BM, Morgan DA, Ellis IO, Cheung KL. A study of ductal versus non-ductal invasive breast carcinomas in older women: long-term clinical outcome and comparison with their younger counterparts. Breast Cancer Res Treat. 2014;147:671–4.

    Article  PubMed  CAS  Google Scholar 

  26. Gennari R, Curigliano G, Rotmensz N, Robertson C, Colleoni M, Zurrida S, et al. Breast carcinoma in elderly women: features of disease presentation, choice of local and systemic treatments compared with younger postmenopasual patients. Cancer. 2004;101:1302–10.

    Article  PubMed  Google Scholar 

  27. Molino A, Giovannini M, Auriemma A, Fiorio E, Mercanti A, Mandarà M, et al. Pathological, biological and clinical characteristics, and surgical management, of elderly women with breast cancer. Crit Rev Oncol Hematol. 2006;59:226–33.

    Article  PubMed  Google Scholar 

  28. Cheung KL, Wong AW, Parker H, Li VW, Winterbottom L, Morgan DA, et al. Pathological features of primary breast cancer in the elderly based on needle core biopsies--a large series from a single centre. Crit Rev Oncol Hematol. 2008;67:263–7.

    Article  PubMed  CAS  Google Scholar 

  29. Dimitrakopoulos FI, Kottorou A, Antonacopoulou AG, Makatsoris T, Kalofonos HP. Early-stage breast cancer in the elderly: confronting an old clinical problem. J Breast Cancer. 2015;18:207–17.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Syed BM, Green AR, Paish EC, Soria D, Garibaldi J, Morgan L, et al. Biology of primary breast cancer in older women treated by surgery: with correlation with long-term clinical outcome and comparison with their younger counterparts. Br J Cancer. 2013;108:1042–51.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Botteri E, Bagnardi V, Goldhirsch A, Viale G, Rotmensz N. Axillary lymph node involvement in women with breast cancer: does it depend on age? Clin Breast Cancer. 2010;10:318–21.

    Article  PubMed  Google Scholar 

  32. Wildiers H, Van Calster B, van de Poll-Franse LV, Hendrickx W, Røislien J, Smeets A, et al. Relationship between age and axillary lymph node involvement in women with breast cancer. J Clin Oncol. 2009;27:2931–7.

    Article  PubMed  Google Scholar 

  33. Bastiaannet E, Liefers GJ, de Craen AJ, Kuppen PJ, van de Water W, Portielje JE, et al. Breast cancer in elderly compared to younger patients in the Netherlands: stage at diagnosis, treatment and survival in 127,805 unselected patients. Breast Cancer Res Treat. 2010;124:801–7.

    Article  PubMed  CAS  Google Scholar 

  34. Louwman WJ, Vulto JC, Verhoeven RH, Nieuwenhuijzen GA, Coebergh JW, Voogd AC. Clinical epidemiology of breast cancer in the elderly. Eur J Cancer. 2007;43:2242–52.

    Article  PubMed  CAS  Google Scholar 

  35. McCarthy EP, Burns RB, Freund KM, Ash AS, Shwartz M, Marwill SL, et al. Mammography use, breast cancer stage at diagnosis, and survival among older women. J Am Geriatr Soc. 2000;48:1226–33.

    Article  PubMed  CAS  Google Scholar 

  36. Freedman RA, Keating NL, Lin NU, Winer EP, Vaz-Luis I, Lii J, et al. Breast cancer-specific survival by age: worse outcomes for the oldest patients. Cancer. 2018;124:2184–91.

    Article  PubMed  CAS  Google Scholar 

  37. Singh R, Hellman S, Heimann R. The natural history of breast carcinoma in the elderly: implications for screening and treatment. Cancer. 2004;100:1807–13.

    Article  PubMed  Google Scholar 

  38. Yancik R, Wesley MN, Ries LA, Havlik RJ, Edwards BK, Yates JW. Effect of age and comorbidity in postmenopausal breast cancer patients aged 55 years and older. JAMA. 2001;285:885–92.

    Article  PubMed  CAS  Google Scholar 

  39. Parise CA, Bauer KR, Caggiano V. Variation in breast cancer subtypes with age and race/ethnicity. Crit Rev Oncol Hematol. 2010;76:44–52.

    Article  PubMed  Google Scholar 

  40. Kurian AW, Fish K, Shema SJ, Clarke CA. Lifetime risks of specific breast cancer subtypes among women in four racial/ethnic groups. Breast Cancer Res. 2010;12:R99.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Choi DH, Shin DB, Lee MH, Lee DW, Dhandapani D, Carter D, et al. A comparison of five immunohistochemical biomarkers and HER-2/neu gene amplification by fluorescence in situ hybridization in white and Korean patients with early-onset breast carcinoma. Cancer. 2003;98:1587–95.

    Article  PubMed  CAS  Google Scholar 

  42. Parise CA, Bauer KR, Brown MM, Caggiano V. Breast cancer subtypes as defined by the estrogen receptor (ER), progesterone receptor (PR), and the human epidermal growth factor receptor 2 (HER2) among women with invasive breast cancer in California, 1999-2004. Breast J. 2009;15:593–602.

    Article  PubMed  Google Scholar 

  43. Parise C, Caggiano V. Disparities in the risk of the ER/PR/HER2 breast cancer subtypes among Asian Americans in California. Cancer Epidemiol. 2014;38:556–62.

    Article  PubMed  Google Scholar 

  44. Telli ML, Chang ET, Kurian AW, Keegan TH, McClure LA, Lichtensztajn D, et al. Asian ethnicity and breast cancer subtypes: a study from the California Cancer Registry. Breast Cancer Res Treat. 2011;127:471–8.

    Article  PubMed  Google Scholar 

  45. Gomez SL, Von Behren J, McKinley M, Clarke CA, Shariff-Marco S, Cheng I, et al. Breast cancer in Asian Americans in California, 1988-2013: increasing incidence trends and recent data on breast cancer subtypes. Breast Cancer Res Treat. 2017;164:139–47.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Porter P. "Westernizing" women's risks? Breast cancer in lower-income countries. N Engl J Med. 2008;358:213–6.

    Article  PubMed  CAS  Google Scholar 

  47. Turkoz FP, Solak M, Petekkaya I, Keskin O, Kertmen N, Sarici F, et al. Association between common risk factors and molecular subtypes in breast cancer patients. Breast. 2013;22:344–50.

    Article  PubMed  Google Scholar 

  48. Lambertini M, Santoro L, Del Mastro L, Nguyen B, Livraghi L, Ugolini D, et al. Reproductive behaviors and risk of developing breast cancer according to tumor subtype: a systematic review and meta-analysis of epidemiological studies. Cancer Treat Rev. 2016;49:65–76.

    Article  PubMed  Google Scholar 

  49. Parise CA, Caggiano V. Risk factors associated with the triple-negative breast cancer subtype within four race/ethnicities. Breast Cancer Res Treat. 2017;163:151–8.

    Article  PubMed  Google Scholar 

  50. Scott LC, Mobley LR, Kuo TM, Il'yasova D. Update on triple-negative breast cancer disparities for the United States: a population-based study from the United States Cancer Statistics database, 2010 through 2014. Cancer. 2019;125:3412–7.

    Article  PubMed  Google Scholar 

  51. Cancer incident cases and incidence rate by site, sex, age group (Source: Korean Ministry of Health and Welfare, Cancer Registration Statistics). https://kosis.kr/eng/statisticsList/statisticsListIndex.do?menuId=M_01_01&vwcd=MT_ETITLE&parmTabId=M_01_01#content-group. Accessed 26 Jan 2022.

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Acknowledgments

This work was supported by the Inje University Haeundae Paik Hospital. Further, the article was supported by the Korean Breast Cancer Society.

Funding

This work was supported by the 2018 Inje University research grant. The funding body did not have any influence on the design of the study, collection, analysis, interpretation of data or writing of manuscript.

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Contributions

SKJ and HJP conceived and designed the study; HJP, KSK, YK, SKL, SHK, JJ, HJY, and the KBCS constructed the data; SKJ and HJP analyzed the data; KSK, YK, SKL, and SHK contributed reagents, materials, and/or analysis tools; HJP and SKJ wrote the manuscript; and the KBCS provided the data. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Suk Jung Kim.

Ethics declarations

Ethics approval and consent to participate

The Institutional Review Board of Haeundae Paik Hospital approved this study (Institutional Review Board file no. 2019–09-010). The Korean Breast Cancer Society anonymized and de-identified personal information from the records for the protection of patient privacy, and the need for informed consent was waived.

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Not applicable.

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The authors declare that they have no competing interests.

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Paik, HJ., Kim, S.J., Kim, K.S. et al. Characteristics and chronologically changing patterns of late-onset breast cancer in Korean women of age ≥ 70 years: A hospital based-registry study. BMC Cancer 22, 1261 (2022). https://doi.org/10.1186/s12885-022-10295-y

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Keywords

  • Old-onset breast cancer
  • Triple-negative breast cancer
  • Asia
  • Korea