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Long-term outcomes of Türkiye’s first population-based mammography screening program: a decade of breast cancer detection and survival analysis in Bahçeşehir

BMC Women's Health volume 25, Article number: 5 (2025) Cite this article

Abstract

Background

The Bahçeşehir population-based mammography screening program (BMSP) is an example of Türkiye’s first population-based screening program. This study aims to reveal the successful implementation of population-based secreening program in one of the low- and middle-income countries, Türkiye and long-term results of patients diagnosed with breast cancer during BMSP.

Methods

This study was conducted between 2009 and 2019, in the Bahçeşehir county of Istanbul. Women between the ages of 40 and 69 living in this region were invited every two years to undergo clinical breast examination (CBE) and mammography screening. All data was recorded in a dedicated software program. Women diagnosed with breast cancer were followed as a separate cohort.

Results

During the 10-year screening period, 8,825 women were screened and 146 (1.7%) breast cancers were detected. The median age at diagnosis for these patients was 52.9 years (40–69). The risk of breast cancer was 1.39 times higher (95% CI: 1.01–1.93) in women aged ≥ 50 compared to those less than 50 years (p = 0.045). The Cox regression analysis revealed that age at first birth, and number of births were significant predictors of breast cancer risk (p < 0.001, and p = 0.011). The breast cancer rate tends to increase as the breast density category progresses from A to D (p < 0.001). The median follow-up time for 146 breast cancer patients was 95.3 months. The 10-year breast cancer specific survival rate was 85%.

Conclusions

This study demonstrates that with a committed team and sufficient infrastructure, screening mammography can be effectively carried out in Türkiye, leading to early detection and lower mortality rates. The recommended age to commence screening is 40 years old.

Peer Review reports

Background

Mammography screening is particularly effective in detecting breast cancer, and early diagnosis has been shown to reduce mortality by 40% [1,2,3,4,5,6,7,8]. Today, the United States Preventive Services Task Force (USPSTF) finalized new recommendations for breast cancer screening that advise women to start regular mammograms at 40 years old instead of the previously recommended at 50 years [9]. Countries with routine screening programs have higher rates of early diagnosis and lower mortality rates. In comparison, countries without such programs tend to have higher rates of locally advanced and metastatic disease, as well as higher mortality rates. Low breast cancer awareness, lack of necessary infrastructure and trained personnel, and economic reasons make it impossible to conduct community-based screening in low- and middle-income countries. Instead, these countries rely on opportunistic screening or diagnosis based on breast-related complaints.

In Türkiye, there is a national breast cancer screening program that recommends monthly self-breast examination (BSE), annual clinical breast examination (CBE), and mammography every two years for women aged 40–69 [10]. However, this program is currently implemented as opportunistic screening, and the regular practice of inviting all eligible women has not been fully implemented.

The Bahçeşehir population-based mammography screening program (BMSP) is an example of Türkiye’s first population-based screening program, which was conducted between 2009 and 2019. In this program, all women aged 40–69 residing in the Bahçeşehir county of Istanbul were invited every two years to undergo CBE and mammography screening. The first results of BMSP and the results of the Turkish Breast Cancer Registry Program showed that 47% of the women diagnosed with breast cancer in Türkiye were under the age of 50 [11, 12]. This rate is less than 25% in developed countries [13]. Regarding the results of our two studies, the Ministry of Health of the Republic of Türkiye revised the mammographic screening guide in Türkiye and reduced the screening age from 50 to 40 in 2012 [10].

Now, we want to present the long term results of BMSP and to reveal the successful implementation of population-based secreening program in one of the low- and middle-income countries, Türkiye with long-term results of patients diagnosed with breast cancer during BMSP.

Methods

This study was conducted between 2009 and 2019, in the Bahçeşehir county of Istanbul. Women between the ages of 40 and 69 living in this region were recorded in a dedicated software program and included in the screening program thorough invitation. The exclusion criteria were as follows: (i) women who passed away, (ii) older than 69 (iii) having moved from the county (iv) having a breast cancer diagnosis (v) pregnancy.

All eligible women were invited for screening at the Bahçeşehir Breast Center (MEMEDER) every two years through letters, emails, or phone calls. In 2019, no new women were added to the study population, but the screening of registered women continued for one more year, and the study was closed in 2020. Women diagnosed with breast cancer were followed as a separate cohort.

Ethical approval was obtained from the Institutional Review Board of Istanbul University Istanbul Faculty of Medicine (Application No.: 2007/152, Date: 24.01.2007/01). All women included in the study were informed and provided written consent forms. After obtaining written consents, the detailed information form including women’s demographic data, social and marital status, breast cancer risk factors, and family history were filled out. Then, all women who visited Bahcesehir Breast Center underwent evaluations by general practitioners trained in clinical breast examination, and routine breast examinations were conducted and also educated for BSE. Following this, mediolateral oblique (MLO) and cranio-caudal (CC) digital mamographic projections were obtained using full-field digital mammographic equipment (Selenia, Hologic). Two expert radiologists with more than 5 years of experience evaluated the mammography images and collaborated on reporting. In case of any discrepancies, a third radiologist with over 20 years of experience in breast imaging assessed the images. The reporting process followed the guidelines of the 4th edition of the Breast Imaging-Reporting and Data System of the American College of Radiology (ACR BIRADS) [14]. Women with BIRADS 0 were recalled for spot mammography or ultrasonography (USG) evaluation. Those with BIRADS 4 and 5 were referred to a tertiary hospital for further examination and histopathological evaluation. The results of additional studies (USG, MRI, biopsy) were recorded and patients diagnosed as breast cancer were followed as a seperate cohort and all additional diagnostic tests and pathology results were taken from the patients by e-mail. Staging and molecular subtype evaluation of patients diagnosed with breast cancer were done according to the AJCC 8th version [15] and to the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013 [16, 17].

Statistical analysis

Continuous variables that followed a normal distribution were analyzed using t-tests. Violations of the normal distribution were assessed using the Shapiro-Wilk test, while variables that did not follow a normal distribution were analyzed using the Kruskal-Wallis test. Chi-square tests were used to compare the frequency differences of categorical variables between the breast cancer and no breast cancer groups. Survival rates were estimated using Kaplan-Meier log-rank tests. Cox models were employed to estimate hazard ratios and 95% confidence intervals for the survival analyses. The proportional hazards assumption was tested for both overall and each group’s survival analyses, and for all comparisons and analyses, the proportional hazards assumption was found to be met (P > 0.10). P-values less than 0.05 were considered statistically significant. All statistical analyses were conducted using R version 3.6.1 (R Foundation for Statistical Computing, Vienna, Austria, https://www.r-project.org/) software packages.

Results

During the 10-year screening period, 12,308 women were invited for secreening and 8,825 women were screened and 22,621 mammograms were conducted. The overall screening participation rate during the screening period was 71.7%, and 146 (1.7%) breast cancers were detected.

The demographic characteristics of women in the BMSP were presented in Table 1. The median age of breast cancer patients was 49.13 years, while healthy screened women were 47.15 years old (p = 0.001). No differences were found between breast cancer patients and healthy women regarding the age of first menarche, the number of missed or induced abortions, duration of lactation, breast size, breast volume, educational level, job, marital status, body mass index (BMI), belly circumference and family history. The mean age at first birth was 24.7 years in breast cancer cases and 23.2 years in other screened women (p = 0.001). It was observed that the risk of breast cancer decreased as the number of births increased: while this rate was 2.4% in those who gave birth only once, it was found to be lower in those who gave birth 2, 3 or more times (1.6%, 1.4%, and 1.1%, respectively, p = 0.012). The breast cancer rate also appeared to increase correlated with the breast density categories progressing from A to D. The rates were 1.1% in category A, and 2.0% in category B, 1.5% in category C, and 4.0% in category D (p = 0.004) (Table 1).

Table 1 Demographic characteristics of women in BMSP
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The Cox regression analysis identified age as a significant predictor of breast cancer risk (p = 0.041) when adjusted for the time from the beginning of screening to the detection of breast cancer. The risk of breast cancer was 1.39 times higher (95% CI: 1.01–1.93) in women aged ≥ 50 compared to those less than 50 years (p = 0.045) (Table 2). Furthermore, the Cox regression analysis revealed that age at first birth, and number of births were significant predictors of breast cancer risk (p < 0.001, and p = 0.011). The number of missed abortions did not significantly predict the development of breast cancer (p = 0.090), despite the breast cancer rate being higher in women who had experienced a missed abortion compared to those who had never (HR: 0.56, 95% CI: 0.31–0.99) (p = 0.044). The breast cancer rate tends to increase as the breast density category progresses from A to D (p < 0.001) (Table 2).

Table 2 Factors influencing breast cancer risk identified by Cox regression analyses
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During 10-year screening, 146 (146/8825, 1.7%) breast cancer patients were detected. The median age at diagnosis for these patients was 52.9 years (40–69). Of these, 16 (10.9%) were DCIS and the remaining were invasive cancers where 71 (48.6%) were at stage 1, 40 (27.4%) at stage 2, 15 (10.3%) at stage 3, and 4 (2.8%) at stage 4. Table 3 provides the clinical stages of 130 invasive cancers and their distribution according to age at diagnosis. Forty-three (33%) of the patients with invasive cancer were below 50 years and 87 (67%) were equal to or older than 50. Breast-conserving surgery (BCS) was performed in 103 (79%) patients. The axillary metastasis rate was 33%. The distribution of molecular subtypes of 130 invasive breast cancers were as follows: 56 (43%) luminal A, 60 (47%) luminal B, 7 (5%) Her 2+, and 7 (5%) triple negative breast cancer (TNBC) (Table 3).

Table 3 Distribution of age, surgery type and tumor characteristics of patients diagnosed with invasive breast cancer according to their clinical stages
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The median follow-up time for 146 breast cancer patients was 95.3 months (25th percentile: 61.3 months, 75th percentile: 123.9 months). The 10-year breast cancer specific survival rate was 85% (95% confidence interval: 67%, 100%). The 10-year overall survival rate of DCIS patients was 100%. The 10-year overall survival rate of 130 invasive breast cancer cases was 79% (95% CI: 55%, 100%) (Fig. 1). The survival rates based on stage distribution and age groups can be seen in Figs. 2 and 3. No significant survival difference was observed among molecular subtypes of breast cancers and age at diagnosis of breast cancers.

Fig. 1
figure 1

The 10-year overall survival of 130 invasive breast cancer cases

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Fig. 2
figure 2

The overall survival rates according to the stage distributions

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Fig. 3
figure 3

The overall survival rates according to the age groups

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Discussion

This study presents the 10-year results of the first population-based mammographic breast cancer screening project in Türkiye. In the current study, we analyzed the risk factors for breast cancer in 8825 women and we observed that similar risk factors to those in the literature are valid for women in Türkiye [18,19,20,21,22,23]. Similar results were also found in a study by Özmen et al. on breast cancer risk factors in Türkiye [24]. In both studies, it was observed that the incidence of breast cancer increases with age and that the age at first childbirth is higher in the breast cancer group. Unlike our previous study, this study did not find induced abortion, body mass index, and a positive family history as risk factors for breast cancer [25]. In the current study, the risk of breast cancer was found to be 1.39 times higher in women equal to or older than 50 years compared to those less than 50 years old, and the risk decreases as the number of births increases. Additionally, no differences were detected between breast cancer cases and healthy screened women in terms of age at first menarche, duration of lactation, menopausal status, age of menopause, breast size, breast volume, educational background, job, marital status, and belly circumference. We have found that increased breast density was associated with breast cancer risk. Specifically, the risk of breast cancer in women with ACR breast density D was eight fold higher than in women with breast density A (p < 0.001).

Increased breast density carries significant clinical implications, including the potential to obscure malignancies and serving as an independent risk factor for breast cancer development. Breast density has been integrated into breast cancer risk assessment models. A recent meta-analysis by Kusumaningtyas N et al. demonstrated a strong correlation between volumetric breast density and breast cancer risk [26]. Additionally, another meta-analysis published in 2024 found that elevated breast cancer risk is linked to higher body mass index (BMI), oral contraceptive use among premenopausal women, higher BIRADS classifications, and increased breast density [27]. A thorough systematic review identified 2,387 systematic reviews, of which 122 were included, revealing six overarching themes. Notably, in their “top list” of the 36 most significant findings, a study on breast density exhibited the highest effect size in relation to the increased risk of breast cancer [28].

For a high-quality breast cancer screening program, it is recommended that over 70% of invited women attend for screening, and the breast cancer detection rate is three times higher than the rate of breast cancer incidence without screening [29, 30]. In the current study, the total screening participation rate over a 10-year period was 71.7%, and the breast cancer detection rate was 1.7%. This study represents the first population-based screening program in Türkiye, and the total participation rate is considered quite successful, meeting the recommended rate in the European Screening Guidelines [31]. The success of this program can be attributed to several factors: regular updates of the population list to be screened every two years, careful tracking of women entering and exiting the screening program, multiple invitations for screening through letters, emails, and phone calls, as well as various awareness studies conducted to emphasize the importance of breast cancer screening to increase participation rate among the population.

The main philosophy underlying mammographic screening programs is early detection, which has been supported by studies conducted in high-income countries. These studies have shown that population-based breast cancer screening programs lead to early detection and a reduced risk of breast cancer-related deaths [4, 5, 7, 8, 31,32,33]. Screening is expected to detect breast cancer at least three times more often than without screening, with diagnoses likely to be in earlier stages, such as in situ and early invasive cancers. Although there is robust evidence from high-income countries supporting this, in low- and middle-income countries the supporting data is currently insufficient [3, 34,35,36,37,38,39,40,41]. According to cancer data from the Turkish Ministry of Health in 2018, the incidence of breast cancer in Türkiye was 48.6 per 100,000 [42], and the breast cancer detection rate in the BMSP was 1.7%. It appears that implementing a population-based screening program leads to a higher rate of breast cancer diagnosis compared to opportunistic screening.

In low- and middle-income countries, breast cancer cases tend to occur at a younger age, are diagnosed at more advanced stages, and have higher rates of triple-negative cancer [40, 41, 43, 44]. A study analyzing breast cancer cases from Northern India found that 45% of women were under 50 at the time of diagnosis, 21% had distant metastases, 59% had positive axillary lymph nodes, and 27% had triple-negative breast cancer [45]. These cases had larger tumor sizes and higher rates of axillary lymph node involvement compared to studies from high-income countries [46, 47]. In a study conducted by the Turkish Federation of Breast Diseases Societies, the median age at diagnosis was 51, with 17.2% of all breast cancer cases in Türkiye occurring in women under 40 and 37.2% in premenopausal women. Only 4.7% of cases were ductal carcinoma in situ (DCIS), and 28.5% were stage 1. Most cases were initially diagnosed at locally advanced stages (62.8%), with 4% being metastatic [11]. Additionally, according to a study, luminal A accounted for 58% of all cancers, 12% were Her-2 enriched and 8% were TNBC. In the BMSP, the median age of diagnosis was 52.9 years, and 33% of cases were seen in women under 50 years. This rate is higher than the rate of young breast cancer detected in high-income countries [13, 46]. At the time of diagnosis, 10.9% of cases were identified as DCIS, 48.6% as stage 1, and only 2.8% were metastatic. These findings imply that a properly executed population-based screening program can lead to a higher rate of early and non-invasive breast cancer detection. In the BMSP, luminal A accounted for 44% of all invasive cancers, while Her-2 enriched and triple-negative breast cancer each represented 5%. It is worth mentioning that these results are consistent with those reported in another Turkish study [11].

Mammographic screening leads to a reduction in breast cancer-specific mortality across all age groups. However, to fully evaluate the impact of screening on mortality, follow-up of 20 years or more is necessary [48,49,50,51]. It is important to note that most studies demonstrating these results have been conducted in high-income countries [31, 52]. The evidence is currently insufficient regarding the effects of screening in low- and middle-income countries. One study conducted in Sweden, including 549,091 women, found that breast cancer cases detected through mammographic screening were 25% less likely to be locally advanced and the risk of breast cancer-related death rate over a 10-year period was 41% lower [3]. Turkish Breast Cancer Registry Program, in which 20,000 patients were analyzed, revealed a 5-year overall survival rate of 85.8% and a 10-year survival rate of 75.7% [11]. Furthermore, the BMSP reported a 10-year breast cancer specific survival rate of 85%. These findings indicate that the survival rate for cancers detected through screening programs is higher than for those detected without screening, even in middle-income countries like Türkiye.

Conclusions

In conclusion, the successful implementation of a population-based breast cancer screening program necessitates a high level of breast cancer awareness and knowledge among women, a well-established screening infrastructure, and effective teamwork. The lack of these poses significant challenges in low- and middle-income countries, leading to late-stage diagnoses and high mortality rates. However, this study demonstrates that with a committed team and sufficient infrastructure, screening mammography can be effectively carried out in Türkiye, one of the low- and middle-income countries. The recommended age to commence screening is 40 years old.

Data availability

No datasets were generated or analysed during the current study.

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Acknowledgements

We all thanks to Prof. Ayse Nilufer Ozaydin, Prof. Arda Kayhan, Assoc. Prof. Cennet Sahin, Omur Can MD, Enis Ozturk MD; Gonul Aykuter MD; Ayten Balikcioglu MD; and Nukhet Aytug MD for support to include women in the registration program at the beginning of our Bahçeşehir Screening Project and data collection of this project. We are also thankful to Gulcin Vatandas, Nursen Has, Sevil Sevinc, Deniz D. Ozkanli, Ahu Ozdemir and Semra Yasar for their technical support. Additionally, we would like to thank Bahadir M. Gulluoğlu MD, Prof; Serra Gorpe, Prof; and Pemra C. Unalan MD, Prof. for supervising in the beginning of the screening program. Lastly, we are grateful to all study participants who accepted our invitation and attended our screening program continuously in our center.

Funding

BMSP was funded mainly by the Breast Health Society of Türkiye (MEMEDER) and partly by Roche Türkiye. The Breast Health Center was rented by Bahcesehir Municipality. General Electric supported the periodic routine maintenance of the digital mammography device.

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Authors and Affiliations

  1. Department of General Surgery, İstanbul Faculty of Medicine, İstanbul University, İstanbul, 34093, Türkiye

    Beyza Ozcinar, Neslihan Cabioglu & Vahit Ozmen

  2. Department of Radiology, School of Medicine, Acibadem Mehmet Ali Aydinlar University, İstanbul, Türkiye

    Erkin Aribal

  3. Department of General Surgery, School of Medicine, Namik Kemal University, Tekirdag, Türkiye

    Sibel Ozkan Gurdal

  4. Department of Public Health, School of Medicine, Namik Kemal University, Tekirdag, Türkiye

    Gamze Varol

  5. Department of Medical Imaging Techniques, Vocational School of Health Services, Marmara University, İstanbul, Türkiye

    Nuran Akyurt

  6. Department of Food Engineering, İzmir Institute of Technology, İzmir, Türkiye

    Efe Sezgin

  7. Istanbul Florence Nightingale Hospital, Breast Health Center, İstanbul, Türkiye

    Vahit Ozmen

Authors
  1. Beyza Ozcinar
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  2. Erkin Aribal
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  3. Neslihan Cabioglu
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  4. Sibel Ozkan Gurdal
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  5. Gamze Varol
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  6. Nuran Akyurt
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  7. Efe Sezgin
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  8. Vahit Ozmen
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Contributions

Idea/concept: BO, EA, NC, VO. Control/supervision: EA, VO, NC, SOG, GV, NA. Data collection and/or processing: BO, EA, NC, SOG, GV, NA, ES, VO. Analysis and/or Interpretation: BO, VO, EA, ES. Writing the article: BO, VO, EA, NC, ES. Critical review: BO, EA, NC, SOG, GV, NA, ES, VO.

Corresponding author

Correspondence to Beyza Ozcinar.

Ethics declarations

Ethics approval and consent to participate

Ethical approval was obtained from the Institutional Review Board of Istanbul University Istanbul Faculty of Medicine (Application No.: 2007/152, Date: 24.01.2007/01).

This study has been performed in accordance with the Declaration of Helsinki.

All women included in the study were informed and provided written consent forms.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

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Ozcinar, B., Aribal, E., Cabioglu, N. et al. Long-term outcomes of Türkiye’s first population-based mammography screening program: a decade of breast cancer detection and survival analysis in Bahçeşehir. BMC Women's Health 25, 5 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12905-024-03521-1

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12905-024-03521-1

Keywords

BMC Women's Health

ISSN: 1472-6874

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