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Florence Nightingale Journal of Nursing logoLink to Florence Nightingale Journal of Nursing
. 2023 Jun 1;31(2):91–96. doi: 10.5152/FNJN.2023.22271

Diagnosis Rates Through Cancer Screening Programs in Patients with Breast Carcinoma

Mustafa Eray Kılıç 1,✉, Sena Özcan 2, Göksu Kılıç 2,✉, Betül Bolat Küçükzeybek 3, Yusuf Atmalar 2, Badesu Talia Koç 2
PMCID: PMC10440967  PMID: 37404211

Abstract

AIM:

This study investigated whether breast cancer patients had ever applied for Cancer Early Diagnosis Screening and Training Centers (KETEM).

METHOD:

This study, conducted from November 2020 to April 2021, adopts a cross-sectional research design and is planned as a survey study. The “Diagnosis Rates with Screening Programs in Breast Cancer Patients” survey was conducted on women over 45 who were diagnosed with breast cancer in the Medical Oncology Clinic of İzmir Katip Çelebi University Atatürk Education and Research Hospital. Further information about the cancer stage was gathered from the Medical Oncology outpatient clinic file records. Data obtained in the study were evaluated using the the Statistical Package for Social Sciences version 26.0 software (IBM Corp.; Armonk, NY, USA), using the number, percentage distribution, arithmetic mean, and chi-square test methods.

RESULTS:

It has been determined that most patients diagnosed did not receive a diagnosis through screening programs, were not aware of KETEM, and did not apply to KETEM. A positive relationship was found between the level of education and participation in screening programs. It was observed that women who knew about the KETEM’s participated more often in the scans.

CONCLUSION:

The study discovered a lack of knowledge and inadequacy in screening programs for patients with breast cancer. We believe that it is essential to introduce and disseminate KETEMs so that cancers can be detected early through screening.

Keywords: Breast cancer, early detection, KETEM, mammography, screening program

Introduction

Recently, cancers have become one of the most important social health problems in Turkey as well as worldwide. When the incidence rates in women are compared around the world, the first three cancer types with the highest incidence are breast, cervical, and colorectal cancers, respectively. According to Globocan data published by the International Cancer Agency (IARC), 2.2 million women worldwide were reportedly diagnosed with breast cancer in 2020 (Sung et al., 2021). Additionally, developed countries reported a higher incidence of breast cancer and a lower mortality rate from breast cancer compared to developing countries. This is due to the effectiveness of breast cancer screening and treatment services in developed countries (Rivera-Franco & Leon-Rodriguez, 2018; Sharma, 2019). Leader in statistics, breast cancer is seen in 1 in 4 women diagnosed with cancer worldwide and in Turkey. The median age of diagnosis in Turkey is 53. About 11% of cases have been observed in advanced stages when examining breast cancer phases (Şencan & Keskinkılıç, 2017).

When the breast cancer is considered, the course of the disease is directly related to the stage at which the tumor is detected. Early diagnosis positively affects the course of the disease, reduces mortality and morbidity, and makes it possible to apply breast protection surgery in appropriate cases (Ginsburg et al., 2020; Mottram et al., 2021). Three methods stand out as cost-effective, practical, and reliable in the screening of breast cancer: mammography, clinical breast examination (CBE), and breast self-examination (BSE). Mammography is the “gold standard” of breast cancer screening methods. Mammography scanning reduces breast cancer mortality by 30%–50% in the general population (Coleman, 2017; da Costa Vieira et al., 2017; Wöckel et al., 2018).

According to Turkish National Breast Cancer Screening standards, it is recommended that women should have regular BSE every month after the age of 20, have a CBE every 2 years between the ages of 20 and 40, and annually over the age of 40 and that all women between the ages of 40 and 69 should have a mammogram every 2 years (Sağlık Bakanlığı, 2017). According to studies, Turkish women are unaware of the importance of early detection of breast cancer (Kissal et al., 2018; Sevinc et al., 2020). In a study conducted by Sönmez et al. (2012), it was determined that the frequency of regular BSE decreased with advancing age; while the rate of regular BSE practice among women aged 20–39 was 30.6%, this rate decreased to 13.5% in women over 60 years of age. In the same study, a positive and significant relationship was found between the education level of women and the frequency of BSE.

Cancer scans are performed at the Cancer Early Diagnosis Screening and Training Centers (KETEM) in Turkey. KETEMs provide free scanning services to 7 million people each year. The centers continue to perform their tasks using the “early diagnosis saves lives” principle. Breast, cervical, and colorectal cancer screening programs are carried out in the centers and it is aimed to reduce mortality due to these cancers, catching early symptoms, and people who don’t even show symptoms (Gulten et al., 2012). It is also intended to inform the age group under the scan about cancer, raise the awareness of society about cancer, and increase participation in screening programs.

In Turkey, screening is conducted in the form of opportunistic screening of people who apply to health institutions. Women who are included in the cervical and breast cancer screening programs are contacted by phone, invited to screening centers, and screened (Özkan et al., 2018; Secginli et al., 2017).

In this study, it is aimed to determine whether patients diagnosed with breast cancer who applied to the İzmir Katip Çelebi University Atatürk Education and Research Hospital Oncology Polyclinic had applied to KETEMs before. The effectiveness of screening programs at getting the diagnosis, the effect of personal and environmental risk factors on breast cancer development, and breast cancer screening program awareness are examined.

Research Questions

  1. How much do breast cancer patients know about screening programs?

  2. Do breast cancer patients get their diagnosis through screening methods?

Method

Study Design

The study has a cross-sectional research design and is planned as a survey study.

Sample

The number of people to whom the survey will be applied was found to be 164 by power analysis. Patients diagnosed with breast carcinoma at İzmir Katip Çelebi University Atatürk Education and Research Hospital’s Medical Oncology outpatient clinic were included. A total of 197 patients voluntarily agreed to participate in the survey. Data were collected between November 2020 and April 2021. Patients over the age of 40 who were diagnosed with breast carcinoma were included in the study. Patients with insufficient clinical and demographic data in the hospital’s records were excluded.

Data Collection Tools

“Diagnosis with Screening Programs: Breast Cancer Survey” consisting of 18 questions was directed to the patients who agreed to participate in the study. The clinical and demographic data of the patients were obtained from hospital medical oncology polyclinic file records. The questions are prepared to evaluate the participants’ knowledge of screening programs and risk factors.

Diagnosis with Screening Programs: Breast Cancer Survey:

This form, which was prepared by the researchers based on the literature, included three sections: Demographic evaluation (age, educational status, and number of children), characteristics for risk factors (BMI, alcohol and tobacco usage, oral contraceptive consumption, menopausal state), and knowledge about screening programs related to breast cancer. The form consists a total number of 18 questions and developed based on the existing literature. The questions were collected through a literature review and by examining similar research studies conducted on the topic of breast cancer screening programs (Dogu, 2017; Smith et al., 2019; Talas et al., 2015).

Statistical Analysis

The data were evaluated in the statistical package program The Statistical Package for Social Sciences version 26.0 software (IBM Corp.; Armonk, NY, USA). The units (n), percentage (%), average ± standard deviation (mean ± SD), median (M), minimum (min), and maximum (max) metrics are used for identifier statistics. The Shapiro–Wilk test was used to evaluate the normality of data for numerical variables, and the Levene test was used to evaluate the homogeneity of the variance. Nonparametric tests have been used because the data do not conform to the assumption of normal distribution. The single-measure numerical variables (mean age, etc.) were compared with the Mann–Whitney U-test. Fisher’s exact test and the chi-Square test were used to compare categorical data. Frequency tables and crosstabs were used to obtain results related to descriptive statistics. p < 0.05 was accepted for the significance level of the tests.

The Fisher’s exact test was used to compare the educational levels of those who received screening-related diagnoses and those who did not, as well as determine whether either group had a family history of cancer. Comparisons were made with Fisher’s exact test for T stage and lymph node metastasis. The Pearson Chi-Square test was used to determine the presence of distant metastases at the time of diagnosis between those who were diagnosed with screening and those who were not.

Ethical Considerations

For the research, first, the approval of the Non-Interventional Clinical Research Ethics Board was obtained from the İzmir Katip Çelebi University (Date: 21.10.2021/ Number: #0456). Then, necessary permissions were obtained from the İzmir Katip Çelebi University Atatürk Education and Research Hospital Chief Physician and the İzmir Provincial Health Directorate for the use of the data, and the data were analyzed retrospectively. All participants gave their verbal and written consent, and participation in the study was voluntary.

Results

The survey application was used to divide the participants into two groups: those diagnosed by screening and those who were not diagnosed by screening. In the group diagnosed by screening, the youngest participant was diagnosed at the age of 43, and the oldest participant was at the age of 77. At the time of diagnosis, the average age of the 30 people diagnosed through screening was 54.63. The youngest participant in the group that did not receive a diagnosis by scanning was 27 years old, and the oldest participant was 84 years old. The mean age of the 134 individuals who were not scanned was 54.02 years (Table 1). Among the data from 164 patients examined, there was no significant difference found in age between the groups diagnosed with screening and those who did not (p = 0.37, p > 0.05).

Table 1.

Comparison of Descriptive Variables by Screening Groups (n = 164)

Groups Test Statistics
Not Diagnosed by Screening Diagnosed by Screening Test Value p
Diagnosis age, ± SD
M (minimum–maximum)		 54.02 ± 11.18
52.00 (27–84)		 54.63 ± 7.49
54.5 (43–77)		 U = 2217.5 0.37
Level of education, n (%)
Elementary
Secondary
High school
Undergraduate
Master’s		 91 (67.8)
12 (9)
18 (13.5)
12 (9)
1 (0.7)		 18 (60)
0 (0)
11 (36.6)
1 (3.4)
0 (0)		 χ 2 = 11.6 0.021
T stage, n (%)
T1
T2
T3		 0 (0)
26 (19.5)
84 (63.2)
19 (14.3)		 2 (11.8)
6 (20)
20 (66.7)
3 (10)		 U = 1657.5 0.25
T4 3 (2.3) 0 (0)
N stage, n (%)
N0
N1
N2		 48 (36.1)
48 (36.1)
21 (15.8)		 14 (46.7)
9 (30)
3 (10)		 ρ = 1.50 0.69
N3 16 (12) 4 (13.3)
Metastasis, n (%)
No
Yes		 117 (88)
16 (12)		 29 (96.7)
1 (3.3)		 χ 2 = 1.98 0.20
Family history of cancer, n (%)
Yes
No		 67 (51.14)
64 (48.86)		 18 (60)
12 (40)		 χ 2 = 0.76 0.38
Prior cancer history, n (%)
Yes
No		 9 (6.71)
125 (93.29)		 4 (13.33)
26 (86.67)		 χ 2 = 1.47 0.25
KETEM knowledge, n (%)
No
Yes		 96 (71.6)
38 (28.4)		 13 (43.3)
17 (56.7)		 χ 2 = 8.81 0.004
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Note: U = Mann–Whitney U test; ρ = Spearman’s rank order correlation; χ 2 = chi-square distribution.

The study included five steps associated with education level (elementary, secondary, high school, undergraduate, and master’s). Of the 164 participants who participated in the study, 109 were primary school graduates, 12 were middle school graduates, 29 were high school graduates, 13 were undergraduates, and 1 was a graduate of a master’s degree. Eighteen (16.5%) of elementary school graduates were diagnosed with a scan, and 91 (83.5%) were not diagnosed with a scan. Twelve patients with secondary education and 1 patient with a master’s degree were not diagnosed by screening. While 11 (37.9%) of the 29 high school graduates who participated in the survey were diagnosed by screening, 18 (62.1%) did not get the diagnosis by screening. A significant difference was found between those who were diagnosed with screening and those who were not, in terms of educational status. The education level of the patients diagnosed by screening was higher than the patients not diagnosed by screening (p = 0.021, p < 0.05).

In the study, T stage was classified according to the WHO guidelines (an increased T stage is significantly associated with the progression of the disease and a poor prognosis). Of the patients participating in the study, 19.6% were at T1, 63.8% at T2, 13.5% at T3, 1.8% at T4, and 1.2% with carcinoma in situ stages. Thirty-two patients were diagnosed in the T1 stage (not diagnosed by screening: 26, diagnosed by screening: 6), 104 in the T2 stage (not diagnosed by screening: 84, diagnosed by screening: 20), and 22 in the T3 stage (not diagnosed by screening: 19, diagnosed by screening: 3). Three people were diagnosed at the T4 stage (not diagnosed by screening: 3, diagnosed by screening: 0), and two people were diagnosed at the carcinoma in situ stage (not diagnosed by screening: 1, diagnosed by screening: 1). No significant difference was found in terms of T stage between those who were diagnosed with screening and those who were not (p = 0.25, p > 0.05).

In the study, the N stage was classified according to the WHO guideline (Table 1). Stage N indicates whether cancer has spread to the lymph node. The increase in lymph node spread is directly proportional to the poor prognosis of cancer. Among the patients who participated in the study but did not receive the diagnosis by screening, 36.09% were in the N0, 36.09% in the N1, 15.78% in the N2, and 12.03% in the N3 stages. Among those diagnosed by screening, 46.66% were at N0, 30% at N1, 10% at N2, and 13.33% at N3 stages. There were 62 people at the N0 stage (not diagnosed by screening: 48; diagnosed by screening: 14); 57 people at the N1 stage (not diagnosed by screening: 48; diagnosed by screening: 9); and 24 people at the N2 stage (not diagnosed by screening: 21, diagnosed by screening: 3) diagnosed. Twenty people were diagnosed in the N3 stage (not diagnosed by screening: 16, diagnosed by screening: 4). There was no significant difference found in terms of lymph node metastasis between those who were diagnosed with screening and those who were not (p = 0.69, p > 0.05).

In this study, the organ of the metastases was not specified, and all types of metastases were gathered under a single heading. Accordingly, there was no metastasis in 146 (89.57%) patients, whereas 17 (10.43%) patients had metastasis at the time of diagnosis. It was determined that 1 of 17 people with metastasis was in the group of those diagnosed by screening. When the presence of distant metastases was examined between those who were diagnosed with screening and those who were not, the rate of patients who were screened (5.88%) was found to be low. However, no statistically significant difference was found (p = 0.20, p > 0.05).

Before being diagnosed, 19 of the 164 patients in the research had undergone screening programs (mammography, USG). A total of 145 of them had never been screened and were diagnosed after presenting to the hospital with complaints or for control purposes.

Of the 164 patients who participated in the study, 15 of the 30 patients diagnosed with screening were doing BSE, whereas 15 were not found to perform BSE. The number of 70 from 134 patients who have not been diagnosed with the scan (52.23%) have been self-examining breasts, while 64 (47.77%) were not self-examining breasts. As a result, the rate of BSE presence did not have a significant association between the two groups who received and did not receive a diagnosis with screening (p = 0.82, p > 0.05).

The mammography frequencies (months) of 164 patients who participated were compared. The valid data were obtained from 12 of the 30 patients diagnosed by screening. No valid data could be obtained from 18 of them. The valid data could be obtained from 37 of the 134 patients who were not diagnosed by screening. The valid data could not be obtained from 97 of them. The mean of the current data for 12 of the 30 patients diagnosed by the examination was 29 months. The mean of valid data from 37 of 134 patients who were not diagnosed by screening was found to be 20.43 months. In terms of mammography frequency (months), there was no significant relationship between the two groups diagnosed by screening and those not diagnosed (p = 0.10, p > 0.05).

In the study, two groups that knew or were not aware of KETEM were identified. A total of 109 of the respondents (66.5%) who were surveyed stated that they did not know about KETEMs. The number of 55 participants (33.5%) stated that they had prior knowledge. While the 96 participants (88%) from the group who did not know about KETEM were not diagnosed with screening, 13 (12%) were diagnosed with screening. Thirty-eight participants (69.1%) in the group who had knowledge about KETEM were diagnosed through screening, and 17 (30.9%) were diagnosed without participating in the screening program. When the data were evaluated, it was found that having knowledge of KETEM made a significant difference in its relationship with screening and diagnosis (p = 0.003, p < 0.05).

In this study, data on the KETEM admission rates of 164 patients were obtained. Nine of the 30 patients who have been diagnosed with the scan (30%) have applied to KETEM, whereas 21 (70%) have not applied to KETEM. Ten of the 134 patients who did not receive a diagnosis by scanning, (7.46%) had applied to KETEM, whereas 124 (92.54%) did not apply to KETEM. As a result, a significant relationship was found between the two groups in terms of KETEM application rate (p = 0.002, p < 0.05).

The relationship between the knowledge of 164 patients about KETEM and their application to KETEM was examined. While 17 of the 19 patients who applied to KETEM were aware of KETEM (89.5%), two patients stated that they were unaware of KETEM’s (10.5%). While 38 (26.2%) patients who did not apply to KETEM had information about KETEMs, 107 (73.8%) stated that they did not know. A high level of statistical significance was found between the group that had information about KETEM in terms of the KETEM application rate and the group that did not (p = 0.000, p < 0.05).

A total of 30 of the 164 people who participated in the study were diagnosed with cancer through the screening program, and this rate was found to be 18.2%.

Discussion

The breast cancer is the most common type of cancer in women (Azamjah et al., 2019; Şencan & Keskinkılıç, 2017). Although breast cancer death rates are declining in most high-income countries, incidence and mortality rates are increasing rapidly, especially in developing countries (DeSantis et al., 2015; Rivera-Franco & Leon-Rodriguez, 2018; Sharma, 2019). This increase has been associated with lifestyle changes (early menarche, birth after 35 years, changes in reproductive functions such as less breastfeeding, recent menopause, etc.), dietary habits (obesity, inactivity, etc.), increasing population growth, aging, and opportunistic surveillance (Porter, 2008). An increase may have been observed with improved access to medical care over time. The reported incidence of breast cancer in Turkey increased from 24/100,000 in 1993 to 50/100,000 in 2017 (Özmen et al., 2019).

The effects of screening programs applied to breast cancer on mortality have been investigated in different studies. In an analysis conducted by Schopper and de Wolf (2009), the decrease in breast cancer mortality in women over 50 years of age was reported as 16%–36% in different screening programs.

According to the findings of a study conducted on 20,000 breast cancer patients in Turkey by Özmen et al. (2019), the median age of diagnosis of breast cancer patients in Turkey was 51 (14–97). The 45–49 age group was the most densely populated group at 16.5%. The mean age at menarche was 13.4 ± 1.0. It was stated that 33.9% of the patients had a family history of cancer, and 15.8% had a family history of breast cancer. In the study, the mean tumor diameter was 2.5 ± 1.7 cm, and the median tumor size was 2 cm (0.1–25 cm). Tumor diameter was observed to be significantly larger in younger patients (< 40 years) (mean diameter 2.8; median diameter 2.5 cm; p < 0.001).

In the study, the group between the ages of 45–49 was found to be 15.2%. The median age was 52 in those diagnosed with screening and 54.5 in those who were not diagnosed with screening. The percentage of patients with a family history of cancer was found to be 54.8%. The mean size of the tumor was observed as 3.1 ± 0.1 cm. It can be said that the breast cancer diagnostic variables of the participants in the two studies were similar.

In studies on the Bahçeşehir Breast Cancer Screening Program by Ozkan Gurdal et al. (2021), one of the first organized community-based long-term screening studies on breast cancer in Turkey, 8758 women were screened through KETEMs. While breast cancer was detected in 130 women, the mean age was 53.3 ± 7.8 years. In the study, a significant correlation was found between the tumor size of the women diagnosed through KETEM at the time of diagnosis and the tumor size in the National Breast Cancer Registry Data Group.

In the data groups, there was no statistically significant difference found in tumor sizes between the group diagnosed by screening and the group not diagnosed by screening.

In the same study, patients who had been diagnosed through KETEM were identified earlier, with higher levels of breast protection surgery, smaller tumor sizes, fewer axillary nodal involvements, lower histological grades, and higher DCIS ratios (p = 0.001) (Ozkan Gurdal et al., 2021). Upon comparing the T, N, and M stages of cancer between the two groups in the current investigation, no significant difference was found.

The Bahçeşehir Scanning Program found that the 64.7% of cancers in women aged between 40 and 49, and 93% of cancers in women aged between 40 and 44 were detected in the first scan. The detection rate in the first two rounds of screening for tumors detected by screening was 86.4%. This high prevalence of breast cancer in women under 50 years of age, especially between the ages of 40 and 44, indicates the importance of at least one random screening after age 40, especially in countries that cannot implement a population-based screening program. Other studies about KETEM’s also stated the importance of the first scan age (Duffy et al., 2020; Gocgun et al., 2015; Gultekin et al., 2018).

In a similar study conducted in Istanbul Moda, when mammography and BSE behaviors were examined, the 53.6% of women had mammography in the last two years. It has been observed that the frequency of mammography increases as education and economic levels increase. In the research group, it was determined that the two most important factors positively affecting mammography screening were the education of women and their economic status (Demir Yildirim & Ozaydin, 2014).

Previous studies have also reported a relationship between low educational status, low reading ability, and insufficient breast cancer screening knowledge. It was mentioned that a high literacy rate affects women’s ability to access written cancer screening materials, benefit from the instructions given during the clinic visit, and apply for health insurance to obtain preventive screening (Akdoğan Gemici et al., 2020; Bulut et al., 2021; Davis et al., 1996; Özmen et al., 2016; Üçüncü et al., 2018).

Study Limitations

A limitation of this study had to do with the small number of participants. A limitation of this study was the small sample size, which may limit the generalizability of the findings to all Turkish women. Furthermore, the age range of participants is very wide, and the mean age of participants higher than that of most other studies which have explored breast cancer screening program awareness and personal and environmental risk factors on breast cancer. During the period that the survey was conducted, the patients who applied to the chemotherapy unit and the oncology clinic were examined. The survey’s time constraints and the low variability of chemotherapy patients have prevented the number of participants from increasing. Due to a lack of data, the impact of the descriptive characteristics of patients (Table 2) has not been accurately examined. There could be no generalizations since the sample does not reflect all Turkish women.

Table 2.

Descriptive Characteristics of the Patients

Variables Statistics
Smoking, n (%)
Not smoking
Smoking
128 (78)
36 (22)
Alcohol, n (%)
Not drinking
Drinking
157 (95.7)
7 (4.3)
Oral contraceptive use, n (%)
Have used
Have not used
37 (22.6)
127 (77.4)
Menopausal state, n (%)
Yes
No
129 (78.6)
35 (21.4)
BMI (kg/m2), ± SD
M (minimum–maximum)		 28.39 ± 5.81
27.47 (16.41–49.31)
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Note: % = percent of rows; BMI = body mass index; M = median; SD = standard deviation.

Conclusions and Recommendations

The present study observed that as the level of education increased, knowledge about KETEMs and KETEM applications increased. As the level of education increased, women’s approaches to knowledge, attitude, and early diagnosis of breast cancer were found to have increased positively.

The study observed a lack of knowledge and the inadequacy of screening programs for women diagnosed with breast cancer. We believe that the introduction and dissemination of KETEMs is critical for early cancer detection through screening, and that relevant studies should be conducted to raise awareness of screening programs.

Footnotes

Ethics Committee Approval: This study was conducted at İzmir Katip Çelebi Üniversitesi Atatürk Eğitim Araştırma Hastanesi between September 2021 and March 2022. The study was approved by the T.C İzmir Katip Çelebi Üniversitesi Girişimsel Olmayan Araştırmalar Etik Kurulu (Protokol No: 2021-GOKAE-0529).

Informed Consent: Verbal and written consent was obtained from all participants.

Peer-review: Externally peer-reviewed.

Author Contributions: Design – M.E.K., B.B.K.; Supervision – B.B.K.; Data Collection and/or Processing – M.E.K., S.Ö., G.K., Y.A., B.T.K.; Analysis and/or Interpretation – M.E.K.; Literature Search – M.E.K.; Writing Manuscript – M.E.K., S.Ö., G.K., Y.A., B.T.K.

Acknowledgements: We extend our deepest gratitude to the patients who participated in this study, without whom this research would not have been possible. We also thank the clinical staff at the chemotherapy unit and the oncology policlinic for their assistance in the study. We express our sincere thanks to those who supported us by conducting the survey despite the heavy workload at the polyclinic. Furthermore, we are grateful to Dr. Elif Kaymaz for her invaluable assistance in the field of statistics.

Conflict of Interest: The authors have no conflict of interest to declare.

Funding: The authors declared that this study has received no financial support.

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