Abstract
Screening plays an essential role in the reduction of mortality and morbidity of breast cancer, which is one of the most common cancers in women worldwide. The aim of this study was to find out whether the use of health education model and theory-based behavioral interventions is effective in women’s breast cancer screening behavior. Applying different search strategies, we searched electronic databases including PubMed, ScienceDirect, Web of Science, and Scopus without time limit from January 12 to March 11, 2017. Keywords included “Breast neoplasm,” Screening,” “Women,” and “Health Education.” First, screening was conducted based on title, abstract, and full text. Then, the studies were screened according to the selection criteria of our study. The relevant and eligible studies were critically appraised by Delphi checklist. In addition, a meta-analysis of eligible studies was conducted with the random-effect approach. Twenty-six of 8,620 initial studies (with sample size of 10,681 in the intervention group and 8,854 in the control group) were included in the final analysis. The results of the meta-analysis showed that the probability of screening behavior in the intervention group is 1.4 times of that in the control group. Furthermore, subgroup analysis by the type of screening behavior indicates that the probabilities of conducting breast self-examination and mammography in the intervention group are 1.9 and 1.4 times of those in the control group. The health education program has a significant impact on breast cancer screening behaviors, particularly breast self-examination. Thus, given the positive effects of the educational screening programs in women, it is suggested that these programs must be continuously pursued with long-term follow-up and increasing rates of screening behaviors should be monitored.
Introduction
Breast cancer is the most common cancer and the main cause of cancer death in women globally. 1 It is responsible for 23% of all cancers in women so that the annual incidence of breast cancer is 38.1 million cases worldwide. 2 In addition, 502,000 women in the world die from breast cancer every year. 3 According to the American Cancer Society, in the United States, 252,710 new cases of breast cancer were diagnosed in 2017 and 40,610 of them died. 4 Breast cancer had a substantially higher incidence (43.3 per 100,000) and the highest mortality rate (12.9 per 100,000) than any other cancer. 5 The high mortality rate is due to late diagnosis of this disease. If this cancer be diagnosed at an early stage, it can be treated and the screening can be used for its diagnosis. 6 Screening methods include mammography, clinical breast examination, and breast self-examination (BSE). 7 Screening consists of testing women to identify cancers before the appearance of any symptoms. 8 Screening and early diagnosis play a vital role in reducing the mortality of breast cancer. 9 The consequences of delayed or unavailable cancer care are a lower likelihood of survival, greater morbidity of treatment, and higher costs of care, resulting in avoidable deaths from cancer. Early detection improves cancer outcomes by providing care at the first possible step and is consequently a significant public health strategy in all settings.
According to breast cancer screening guideline, BSE every month after the age of 20 years, clinical breast examinations every 3 years at the age of 20 to 39 years, clinical breast examinations and an annual mammogram every year after the age of 40 years are recommended. 10
Studies have revealed that the mortality of women who participated in breast cancer screening programs was reduced to 40%. Despite the importance of screening, a very low percentage of the population do attend the breast cancer screening programs.11,12
Women experience barriers to breast cancer screening. These barriers included fear of breast cancer detection, lower income, fatalistic view of cancer, poor cancer knowledge, lack of time, absence of symptoms, lower perceived susceptibility to breast cancer, embarrassment, and lack of screening recommendation.13–15 Hence, women have to be empowered regarding screening, and educational measures should be taken to promote this behavior among women. An important step is to motivate women to protect themselves against breast cancer, and an important factor for motivation is the health promotion programs, which focus on health education and health behaviors. 16 Therefore, an educational model plays a major role in identifying and addressing educational requirements, starting the program in the right direction, and reducing the unclear and vague parts that may be present in the main content of an educational intervention. 17
Considering that different studies have applied one or more interventions to assess the impact of screening on breast cancer prevention, the purpose of the study is to determine the most effective type of theory-based interventions in this field. Moreover, by this systematic meta-analysis, we will be able to find out if the use of health education model and theory-based behavioral interventions is effective in women’s breast cancer screening behavior.
Materials and Methods
Search Strategy
The electronic search of databases including PubMed, ScienceDirect, Web of Science, and Scopus was conducted without time limit from January 12 to March 11, 2017. The search strategy included key terms: “Breast cancer,” “Breast neoplasm,” “Breast cancers,” “Screening,” “Training Breast self-examination,” “Breast self-examination,” “Clinical Breast Examination,” “Mammography,” “Female,” “Screening,” “Breast Tumor,” “Breast Carcinoma,” “Breast Malignant Tumor,” “Neoplasm,” “Breast,” “Screening behavior,” “Mass screening,” “Cancer early Detection,” “Women,” and “Prevention.” The search strategy for databases is presented in Appendix. This article is designed according to a Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement.
Selection of Studies
After extracting the full text of the articles and removing duplicate studies, according to the selection criteria of our study, the articles were reviewed based on the title, abstract, and full text. In addition, the references of all eligible articles were investigated to identify additional relevant studies. The process of selecting articles was done by two independent researchers. Furthermore, the Google Scholar search engine was applied for gray or additional literature.
The PICOTS-based inclusion criteria to select appropriate articles were as follows:
Types of Studies
We included studies with randomized controlled trials that (a) aimed for behavioral interventions based on theory and model and (b) focused on screening behaviors, including BSE, physician breast examination, and mammography.
Types of Participants
Studies with participants who were 20 years and older, who were without breast cancer, and whose history of breast cancer that apparently was healthy.
Types of Interventions
Behavioral interventions based on the model and theory, focusing on screening behaviors.
Types of Outcomes
The final outcomes were self-examination behavior, clinical examinations, and mammography.
Time
There was no time limitation in our study.
Language
The searches were conducted for the articles that were written in English.
Quality Assessment
After reading full-text articles, two researchers assessed the quality of each study independently using the Delphi checklist. 18
Exclusion Criteria Studies
Exclusion criteria were the studies that have been conducted to screening for breast cancer along with other cancers; studies that have been conducted on women with a history of breast cancer; studies that did not report the outcomes of behavior; and the studies that were aimed to assess the knowledge, attitude, and behavioral intention.
Data Extraction
Data were extracted from each study based on the title, author name, time and place of study, target group, sample size, follow-up, theory or model, study variables, intervention method, and intervention results. Two researchers extracted data independently.
Statistical Analysis
The data analysis was done using the meta-analysis with the random-effect approach. In addition, the results were presented as forest plot and tables, and heterogeneity was evaluated by χ2 test. In addition, the presence of publication bias was assessed by funnel plot.
Results
From the initial search, 8,620 articles were retrieved. Among these articles, 7,972 studies were excluded, as they were duplicates or irrelevant. The remaining 648 articles were reviewed, of which380 studies were excluded because they did not contain intervention. In the next step, 268 articles were carefully reviewed. In the subsequent step, 180 articles were excluded because they did not cover theory base, and only 88 articles were selected theory base. Eventually, 62 studies were excluded because these were not fulfilling the purpose of the study. Thus, a total of 26 studies12,14,19–42 were selected for meta-analysis (Figure 1). Characteristics of the included studies are presented in Table 1.
Flow chart of the systematic review process.
Characteristics of Studies Included in Review.
Abbreviations: HBM, health belief model; TTM, transtheoretical model; PAPM, precaution adoption process model; BSE, breast self-examination; TP, tailored print booklets alone; TC, telephone counseling.
Quality Assessment Results
After determining the related articles, the quality of the articles was evaluated using the Delphi checklist. This checklist evaluated articles based on nine criteria (randomization, allocation concealed, similar in the baseline, eligibility criteria specified, outcome assessor blinded, care provider blinded, patient blinded, variability outcome measures, and intention-to-treat) and considered the maximum score of 9.
Meta-Analysis Results
The results of the meta-analysis show that the probability of screening behavior in the intervention group is 1.4 (95% CI: [1.30, 1.59]) times of that in the control group. In addition, subgroup analysis by the type of screening behavior indicates that probabilities of conducting BSE and mammography in the interventional group are 1.9 (95% CI: [1.06, 3.68]) and 1.4 (95% CI: [1.29, 1.58]) times of those in control group (Figures 2 and 3).
Effectiveness of training mammograms in women. Effectiveness of training breast self-examination in women.

In this study, the overall effect of educational interventions was evaluated in terms of three periods: less than 6 months, 6 to 12 months, and over 12 months. Subgroup analysis of the follow-up period shows that the most effective screening behavior was reported in the period of 6 to 12 months.
Discussion
This study included 26 randomized controlled trial studies, which indicated that educational interventions increased screening behaviors significantly. Health education focuses on influencing and changing individual behavior. 43 Moreover, training plays an important role in raising awareness and consequently promoting screening behavior.
Theoretically-based interventions may be appropriate by identifying key concepts for the target group for behavior change. The positive effects in objective and subjective outcomes may be that while theoretical constructs are targeted in the intervention, theory and model facilitate determining the components of intervention techniques. 44
Our study confirms that behavioral theory-based interventions increase breast cancer screening behaviors.
Among the three methods of screening—mammography, clinical breast examination, and self-breast examination—the most effective method was self-breast examination. In addition, other methods are costly and time-consuming and hence would be the barriers for women to test screening behaviors especially mammography. The BSE is the inexpensive, simplest, and most available method to detect the breast cancer in the earlier stages. In the study by Secginli and Nahcivan, 32 among the three methods of screening, increased behavior was observed for BSE, because other methods required to overcome perceived barriers such as getting a referral from a physician, going to a separate site for the screening, and paying for the procedure.
Subgroup analysis by follow-up period shows that the screening behavior is effective for the period of 6 to 12 months. Therefore, it is recommended that this program must be continuously pursued with long-term follow-up. It seems that in the 6-month follow-up, behavior change has not occurred, and in the 12-month follow-up, the sensitivity of individual has decreased and the behavior will also be disremembered.
To plan the effective intervention programs to promote breast cancer screening, many investigators have attempted to find out the agents that influence women’s behavior for breast cancer screening. The most used model in this survey was the health belief model (HBM). The HBM has been used in many studies as the theoretical framework for understanding breast cancer diagnosis behaviors. According to the HBM, if individuals perceive the disease as a risk for themselves, believe in the consequence regarding the severity of the diseases, and are aware of benefits and barriers of screenings, then the health behavior is expected to appear. 45
In a study by Crane et al. using transtheoretical model, although there were significant differences in attitude and intention, no significant difference was obtained by mammography. This result can indicate that every intention does not lead to behavior, and this relationship depends upon barrier elimination and attracting support on different levels.
Differences were observed among the studies reviewed. One of the most important differences was the sample size, which can affect the results.
Subgroup analysis by the type of screening behavior indicates that BSE was more prevalent than mammography. Moreover, mammography screening has been utilized in more developed countries. One of the reasons for this difference is the cost, and cost elimination resulted in a modest increase in the rate of mammography screening. 46
With any systematic review study, there are a number of sources of bias that impact the results of the meta-analyses. The first one is whether all relevant articles were identified. Although this is unknown, we believe that we have identified the key published articles.
The second source of bias is publication bias. This is a major concern in all of the meta-analysis because studies reporting significant or positive findings are more possible to be published. 47 The third source of bias is heterogeneity. The heterogeneity of the studies was evaluated using the χ2 test. Given the differences in study groups, sample size, ethnicity, and culture distribution of cases, some degrees of heterogeneity are to be expected.
Limitations and Strengths
This systematic review study provides strong evidence on the effectiveness of the theory-based interventions to promote breast cancer screening behavior, especially BSE behavior because this behavior is a skill that does not require cost and equipment.
Thus, it can be promoted through education and increasing the self-efficacy of women. Our review focused on studies that designed to help women to decide and encourage them in participation and adherence to screening.
Our review has several limitations. First, we cannot prevent publication bias, although we performed a comprehensive and complete literature search. The studies that had a low sample size and with meaningless results were to impact our results. Second, several studies had an open intervention design and used unblinded clinical conclusion assessments, which caused lower scores for trial quality. Third, there was a lack of access to full-text articles. Fourth, the evaluation of published articles was only in English. Fourth, in this study, we did not compare the studies that were performed without model and theory. Therefore, it is suggested that this goal should be considered in future studies.
Conclusion
The health education program has an important impact on breast cancer screening behaviors, especially BSE. Training and consulting to the women in the line with encouragement and increasing their skill in performing the self- examination are important stages toward the diagnosis of breast cancer in the earlier stages of the disease. For this reason, informing women about breast cancer, promoting breast awareness, and teaching them how to perform BSE correctly are important. Therefore, considering the positive effect of the educational screening programs in women, it is proposed that these programs must be continually pursued with long-term follow-up and the increasing screening behaviors should be monitored.
Supplemental Material
Supplemental material for Effectiveness of the Theory-Based Educational Interventions on Screening of Breast Cancer in Women: A Systematic Review and Meta-Analysis
Supplemental Material for Effectiveness of the Theory-Based Educational Interventions on Screening of Breast Cancer in Women: A Systematic Review and Meta-Analysis by Saeed Bashirian, Younes Mohammadi, Majid Barati, Leila Moaddabshoar and Mitra Dogonchi in International Quarterly of Community Health Education
Footnotes
Appendix: Search Strategy for All Databases
Breast cancer
“breast cancer” OR “Breast Neoplasm” OR “Breast Neoplasm's” OR “Breast Tumors” OR “Breast Tumor” OR “Malignant Neoplasm of Breast” OR “Malignant Tumor of Breast” OR “Breast Malignant Tumor” OR “Breast Malignant Tumors” OR “Breast Carcinoma” OR “Breast Carcinomas” OR “Human Mammary Neoplasm's” OR “Cancer of the Breast”
Screening
Mammography OR “Breast Self-Examination” OR “Screening behavior” OR “Screening Tests” OR “Mass Screening” OR “training Breast self-examination” OR “Clinical Breast Examination” OR “BSE (Breast Self Examination)” OR “Screening Mammogram” OR “Screening Mammograms” OR diagnosis OR “Mammogram repeat” OR “Cancer Early Detection”
Target group
Woman OR women OR female OR Girl OR “Women Group”
The intervention section and the program
effect* OR control* OR evaluation* OR program* OR “Health education” OR “health promotion” OR “Community Health Education” OR outcome OR “impact training” OR “behavior modification” OR “self care” OR promoting OR promotion OR counseling
Type of study
“randomized controlled trial” OR “controlled clinical trial” OR “randomized controlled trials” OR “random allocation” OR “double-blind method” OR “single-blind method” OR “clinical trial” OR “clinical trials” OR singl* OR doubl* OR tripl* OR mask* OR blind* OR placebo* OR random* OR “research design” OR “comparative study” OR “evaluation studies” OR “prospective studies” OR control* OR volunteer* NOT animal
Implications for Future Research
Our study proposes that effective planning and interventions tailored to the audience’s characteristics can be effective through removing perceived barriers and increasing participation and encouragement of women for performing screening methods. By raising public awareness and early detection of cancer through screening methods, they can play a key role in the reduction of incidence and mortality of cancer.
Acknowledgments
This project has been approved by the Research and Technology Deputy of Hamadan University of Medical Sciences. The authors wish to thank all the interviewers who worked in this study.
Author Contributions
Saeed Bashirian and Majid Barati were involved in conception and design. Mitra Dogonchi and Leila Moaddabshoar contributed to collection and assembly of data. Younes Mohammadi performed data analysis and interpretation. Mitra Dogonchi was involved in Manuscript writing. All authors approved final manuscript.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by Hamadan University of Medical Sciences (Grant Number: 9603091553).
Author Biographies
References
Supplementary Material
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