Possible Logistic and Sociodemographyc Factors on BreastCancer Screening in Turkey: Lessons from a Women’sHealth Project in Mersin Province

Huseyin Abali & Alper Ata & Gozde Gokçe &

Huseyin Gokçe

Published online: 6 October 2011# Springer Science+Business Media, LLC 2011

Abstract Mortality from breast cancer is decreasing partlyowing to early detection. In Mersin province in our country,local health authorities launched an education program onsexual diseases and breast cancer early detection for womenover 15 years of age. After the educational session, clinicalbreast examination was offered by a nurse or physician, andif suspicious they were recommended to apply a specialistfor further examination. Here, we report the results on thosewomen with abnormal clinical breast examination. In thissecond project, socio-demographic variables were investi-gated such as educational level and place of living,parameters to measure the success of previous project,

whether they followed the recommendation themselves,whether mammograms were reported in accordance withBreast Imaging Reporting and Data System (BIRADS). Of3,793 women recruited, mean age was 42.2 years, 42.3%were younger than 40.0 years. Majority (88.5%) weremarried, graduate of primary school (60.6%), without a job(91.2%), and inhabiting in the province (38.7%). Of thepopulation, 98.1% believe in the importance of screening inthe treatment of breast cancer. According to 70.3%,monthly breast self-examination enables early detection,33.5% believe that clinical breast examination detectscancer early, and 35.5% think that annual mammographycan detect it early. Among 2,183 women 40 years of age orover, 41.5% had mammography at once before participatingin the first project. Breast self-examination was beingcarried out by 56.6% on a monthly basis. After an abnormalbreast examination, 86.4% applied to hospitals for specialistexamination. Reasons for declining to seek for furtherexamination among 410 women answering were as follows:42.0% did not accept, 27.0% did not know it wasimportant, 16.6% because of economical reasons, and5.0% were too shy to be examined. Being older, beingmarried, being the graduate of primary and secondaryschool, residing in rural areas, having a mammogrampositively affected the decision in univariate analyses (p<0.05). All but educational level (p=0.059) remainedsignificant in multivariate analysis. Mammography wasreported in accordance with BIRADS in only 45 (1.2%).Awareness of population on breast cancer early detectioncan be raised through education. Generally, women followprofessional recommendation from professionals. Mam-mography reporting among radiologist in accordance withBIRADS is rare. Successful early detection of breast cancermay be obtained by public education together withimproving detection methods.

H. AbaliDepartment of Internal Medicine Division of Medical Oncology,Baskent University School of Medicine,Ankara, Turkey

A. AtaDepartment of Internal Medicine Division of Medical Oncology,Mersin University School of Medicine,Mersin, Turkey

G. GokçeDepartment of Nursing,Dokuz Eylul University Faculty of Health Sciences,Izmir, Turkey

H. GokçeHead of Health Education, Provincial Health Administration,Mersin, Turkey

H. Abali (*)Adana Uygulama ve Arastirma Merkezi,Kisla Saglik Yerleskesi, Baskent Üniversitesi Tip Fakültesi,Ic Hastaliklari Medikal Onkoloji BD,Kazim Karabekir M. 4227 Sk No: 27,01120, Yüregir, Adana, Turkeye-mail: habali1970@yahoo.com

J Canc Educ (2012) 27:347–352DOI 10.1007/s13187-011-0270-7

Keywords Breast cancer . Early detection . Screening .

Education

Introduction

With an incidence of almost 30 in 100,000 population,breast cancer is a significant health problem in Turkey [1].Its incidence and the mortality has been decreasing in USAowing to screening and early detection [2], where almost70% of women over 40 years of age undergo mammographicscreening. Mammographic screening is recommended bymany professional organizations for women over 40 years ofage since it decreases the mortality from breast cancer. Thereis no clear evidence that Breast Self-Examination (BSE)detects breast cancer early, but it generally recommended byguidelines since it may raise awareness of the breasts whichmay facilitate detection of interval cancers [3]. Unfortunately,breast cancer screening in developing countries is far frombeing satisfactory. In our country, a nationwide organizationcalled KETEM (Kanser Erken Teşhis, Tarama ve EğitimMerkezi: Cancer Early Detection and Education Center) hasrecently been launched by Ministry of Health and began toscreen for some cancers [4].

In Mersin province in Turkey, provincial health authority,supported by the governor, launched a program to educatewomen over 15 years of age on sexully transmitted diseasesand breast cancer by giving lectures and showing a breast self-examination video. Attending women were offered clinicalbreast examination by a physician or nurse after the educationalsession. Those with abnormal breast examination were advisedto apply to larger hospitals and centers for mammography. Theresults of the education program was published elsewhere [5].

In the second phase of education program, those womenwith an abnormal breast examination were contacted andclinical examination by general surgeon and then mam-mography or breast ultrasonography, depending on age,was advised if they had not done so already.

We think that publishing our experience we learnt from thesecond phase will be of important value for the promotion ofbreast cancer screening and early detection in Turkey andcountries with similar socio-demographic structure.

Materials and Methods

In Mersin, a province on south coast of Turkey withalmost 1,600,000 inhabitants, around 439,000 womenover 14 years of age had been reached by 35 health-teams from local health administration from 1 January2006 and 30 June 2008. Those teams, consisted of 34physicians and 348 nurse–midwives were trained forwomen's health, breast cancer, breast examinations, and

for screening methods to detect breast cancer before theproject began.

The subjects were informed about breast cancer, its clinicalfindings, screening, and other diagnostic methods by audio-visual methods. Importance of screening and early diagnosiswas stressed with focus on BSE. A short video clip was alsopresented, demonstrating breast self-examination. Subsequentto the dissemination of the information, each subject wasoffered a detailed clinical breast examination (CBE) and ageneral examination as a screening method by the authorizedhealth personnel. Of all the subjects who participated, data of77,934 were described and materials and methods werepresented in detail elsewhere [5].

Of all, 51,706 (66.0%) women agreed to receive CBE.Women with an abnormal CBE, like a suspected mass, wereadvised to apply to clinical centers for further evaluation withspecialist examination, mammography, and breast ultrasound.

In this second project, 3,793 women with an abnormalbreast finding as result of CBE after education werecontacted. They were asked to fill in a questionnaire formmainly about their demographics, whether they followedthe recommendation and questions evaluating the efficacyof previous education. Mammography and general surgeonexamination were also arranged for them if they had nothad done already so. Results of mammography, whetherthey were reported in accordance with Breast ImagingReporting and Data System (BIRADS) and whether theyhad a diagnosis of breast cancer after were also recorded.

Statistical Analysis

Continuous variables were expressed as mean and 95%confidence intervals and ordinal data as median and inter-quartile range, if not stated otherwise. For dichotomousvariables, chi-square test was used to determine the differencebetween the groups, and for continuous variables Student's ttest was used for independent groups. Logistic regressionanalysis was performed for multivariate analysis ofdichotomous variables. Statistical significance was acceptedas a p value of equal to or less than 0.05. Data were analyzedusing Statistical Package for Social Sciences (SPSS 15.0).

Results

Mean age of 3,793 women recruited was 42.2 years, theyoungest and the oldest being 15 and 88 years, respectively.Of them, 1,610 (42.3%) were younger than 40, 45 (1.2%),over 69 years; and the remaining 2,138 (56.5%) between 40and 69 years of age. Majority (3,355, 88.5%) were married,graduate of primary school (2,299, 60.6%), without a job(3,460, 91.2%), and inhabiting in the province (1,466, 38.7%).Demographic data were presented in Table 1 in detail.

348 J Canc Educ (2012) 27:347–352

On the form, their health behaviors were also recorded:majority were non-smokers (2,996, 79.0%). Of them,97.8% were having at least one serving of fresh vegetablesand fruits a day, and only 596 (15.7%) reported to beexercising on a regular basis. The mean age at the firstmenarche was 13.4 years (13.4–13.5 years), age at firstpregnancy 21.3 years (21.0–21.4 years) and median numberof births 3.0 (2.0). A great majority of 3,400 women(89.6%) breast-fed for a mean time of 5 months (4.9–5.1 months). Birth control pills were used by 1,031 (27.2%)for mean time of 27.8 months (25.7–29.9 months).

We also tried to measure level of information on breastcancer screening and early diagnosis in the study populationafter the previous project and after being classified assuspicious breast examination. By doing that, we tried tounderstand how successful the previous educational sessionswere. Of the population, 3,722 (98.1%) believe in theimportance of screening in the treatment of breast cancer.According to 2,668 (%70.3), monthly breast self-examinationenables early detection, while only 1,271 (33.5%) believesthat clinical breast examination by health care provider detectsit early. Only 1,346 (35.5%) thinks that annual mammographyafter 40 years of age can detect it early (Fig. 1).

Data on whether they had mammogram before partici-pating the project were collected in 2,183 women who are40 years of age or over, and 41.5% had mammography atleast once in their life time.

Main focus of the previous education was that “breastcancer can be detected at early stages by breast self-

examination.” Of the population, 2,987 (78.8%) think thatthey know how to do a breast self-examination. However,only 1,793 (56.6%) of the responding 2,992 women statedthat they perform breast self-examination on a monthly basis.

After abnormal breast examination, what the percentageof women sought for professional medical examinationmay be the good sign of whether they are caring forthemselves. Of them, 3,277 (86.4%) applied to hospitals forspecialist examination. While the remaining 516 (13.6%)did not seek for further medical examination, mammogramwas obtained in 2,444 (64.4%), breast ultrasound in 491(12.9%), no further examination than breast examination thespecialist in 318 (8.4%). Among 516, 410 answered a

Table 1 Key demographic fea-tures of the study population

*Unless explained otherwise

N=3,793 Percent,* %

Mean age (years, minimum–maximum) 42.2 15–88

Age groups

15–39 years 1,610 42.4

40+ years 2,183 57.6

Educational status

Illiterate 590 15.6

Can read and write only 350 9.2

Primary and secondary school 2,299 60.6

Lise 417 11.0

University 137 3.6

Marital status

Married 3,335 88.5

Single 167 4.4

Divorced 271 7.1

Place of the longest inhabitation (n=2,327)

Urban 1,247 53.6

Rural 1,080 46.4

Smoker 797 21.0

Mean age at menarche (95% CI, years) 13.4 13.4–13.5

Mean age at the first pregnancy (95% CI, years) 21.3 21.1–21.4

70.30%

33.50% 35.50%

0.00%

10.00%

20.00%

30.00%

40.00%

50.00%

60.00%

70.00%

80.00%

Percent believing in early detection

BSE CBE Mammography

Fig. 1 Percent of participating individuals who think that BSE, CBE,and mammography can detect breast cancer early

J Canc Educ (2012) 27:347–352 349

question on why they did not seek for further medicalexamination: 172 (42.0%) did not accept, 93 (27.0%) didnot know it was important, 68 (16.6%) because of economicalreasons, and 21 (5.0%) were too shy to be examined.

Table 2 summarizes the socio-economical factors affect-ing the behavior of applying for further medical examina-tion, which is the ultimate indicator of someone's healthconsciousness. Being older, being married, being thegraduate of primary and secondary school, residing in ruralareas, and having a mammogram positively affected inunivariate analyses. All but educational level (p=0.059)remained significant in multivariate analysis (Table 2).

One striking finding was that mammography was reportedin accordance with BIRADS in only 45 (1.2%) women.

Discussion

Screening mammography is the best method to diagnosebreast cancer in early stages by detecting microcalfications,not detected by BSE. In Turkey, there has been no fullyfunctional nationwide breast cancer screening program towhich women is invited, yet. Mammography with normal

BSE is paid by the government if women apply to KETEM.To the best of our knowledge, we do not know whatpercentage of women receive biannual mammography.

In our study, we tried to understand the level ofinformation of women on breast cancer early detection,their health behavior pattern on factors like smoking andbreast feeding, degree that they had been affected from theprevious educational project, factors affecting the decisionto follow recommendation by a health care provider. Ourstudy population comprised of mostly nonsmoker, marriedfemales of 15–69 years of age range (over 57% are over40), who are housewives, generally graduate of primaryschool, residing in small towns and villages. Of thesubjects, a majority thinks that the breast cancer can bedetected early with some precautions, and follows therecommendations of health care provider. Among womenwho are 40 years old or over, 41.5% had at least onemammography in their lifetime. Unfortunately, almost nomammography was reported in accordance with BIRADS.

Almost all (98.1%) thinks that believes the importanceof breast cancer screening and over 70.0% thinks that BSEenables early detection; figures every health care providerhappy to see. Of our population, 56.6% reported to perform

Table 2 Socio-economicalfactors on health behavior(applying fo furtherexamination)

Illiterate goup contains boththose who cannot read and writeand those who can only read andwrite, primary school groupcontains primary and secondaryschool graduates

Pri primaryaLogistic regression analysis

Applying for furtherexamination, N (%)

Chi-square Multivariatep value p valuea

Age (years) <0.001 <0.001

<40 (n=1,301) 1,301 (80.8)

≥40 (n=1,976) 1,976 (90.5)

Marital status 0.033 0.032

Single (n=438) 364 (83.1)

Married (n=2,913) 2,913 (86.8)

Educationa 0.006 0.059

Illiterate (n=940) 791 (84.1)

Pri school (n=2,299) 2,019 (87.8)

Lise+(n=554) 467 (84.3)

Employment 0.262

Holding a job (n=333) 281 (84.4)

House wife (n=3,460) 2,996 (86.6)

Health ınsurance <0.001 0.04

Present (n=2,637) 2,330 (88.4)

Absent (n=1,156) 947 (81.9)

The longest Inhabitation 0.001 <0.001

Town or village (n=1,080) 938 (86.9)

Small city (n=1,247) 1,109 (88.9)

Central province (1,466) 1,230 (83.9)

Time of previous mamogram <0.001 <0.001

Never (n=2,536) 2,036 (80.3)

<1 year (n=648) 645 (99.5)

>1 year (n=609) 596 (97.9)

350 J Canc Educ (2012) 27:347–352

BSE on a monthly basis regularly. In a study from thewestern part of Turkey on women applying to healthcenters for other reasons, 37.9% ever heard about breastcancer, 37.1% heard about BSE, and 24.8% had mammog-raphy within 2 years [6]. In the same study, BSE rate was10–40%. In a larger study on over 600 women aged 20–70 years of age—a similar population to ours, similarfigures were obtained [7]. About 25.0–42.7% had at leastone mammogram in their lifetime in Turkey, indicated bytwo studies [7, 8]. Although not comparable directly, higherinformation and consciousness level in our study is found.In our study, rate of having at least one mammogram beforethe first project among those women 40 years of age orover is 41.5%, which is over 70.0% in developed nations[9]. Our figures seem much better than previously pub-lished studies in our country on more or less a similarpopulation. Except for mammography utilization rate, thismay be explained by the fact that our study population hadan abnormal breast examination, meaning that they aresomewhat sensitized to breast cancer early detection.However, it is highly probable that the education theyreceived could have contributed significantly, which sup-ported by our finding that only 35.5% thinks mammographydetects breast cancer in early stages as opposed to 70.0%figure of BSE. It must be remembered that the previouseducation project focused on BSE, rather than clinical breastexamination or mammography (Fig. 1). Therefore, it isevident from our findings that public awareness can easilybe raised through public education. This observation isfurther supported by other studies in Turkey [10, 11].

As health care providers, our ultimate goal is to promotehealth in the community. Education must lead to a behavioralchange ultimately, which is developing an attitude. It is notenough just to know. That is, people should apply to healthcenters for screening. We therefore examined the factorsaffecting whether or not applying to a hospital or doctor afterhaving an abnormal breast examination. We found that beingolder than 40 years of age, being married, having a healthinsurance, residing in a small city or town, having amammogram positively affected the decision in univariateanalyses (Table 2). All remained independent factors inmultivariate analyses except for education.

Of the women not applying to hospitals, 42.0% did notaccept further examination, 16.6% said “I did not know itwas important,” 16.6% could not go to hospital foreconomical reasons, 5.0% was too shy to go. We do notknow why they did not accept, but “did not know it wasimportant” can be explained by ignorance. In our country,almost everybody is covered by insurance. Therefore,economical reason mostly related to cost of travel.

Apart from target population, facilities in a country mustbe enough in number and quality to screen breast cancer.We do not know the exact number of mammography

devices in Turkey to the best of our knowledge. Ministry ofHealth of Turkish Republic launched a cancer screeningprogram (KETEM) in majority of provinces in the country.Each center has mammography device. A rather recentlypublished study analyzed the quality of devices in Turkey.They concluded that there are many mammography devicesnot registered by Turkish Atomic Energy Commission(therefore there is no external quality control); there areserious deficiencies the in quality of devices and radiologisteducation [12]. Mammography device availability inTurkey is one of the lowest among other countries [13].Mammography device availability affects breast cancerscreening performance in a particular country [13]. In ourstudy, we did not study the quality of mammography devices,but analyzed the reports obtained. Unfortunately, only 1.2%were reported in accordance with BIRADS, which indicates aserious deficiency in mammography reporting. To the best ofour knowledge, there is no nationwide mammographyreporting education for radiologists in Turkey.

In conclusion, for a successful screening for breastcancer in Turkey, we have to know socio-demographicfeatures of population in order to understand at whichpoints breast cancer screening may fail. Education raisesthe awareness and probably screening yield. We also haveto know mammography devices and their quality assess-ments. On the other hand, radiologists must report mammo-grams in line with BIRADS. Since our populationcharacteristics are similar, our results may be generalizableto neighboring countries.

Acknowledgment We would like to thank Mersin GovernorHüseyin Aksoy and his wife Hulya Aksoy for their endless supportfor women's health project in Mersin.

References

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM.GLOBOCAN 2008, Cancer Incidence and Mortality Worldwide:IARC CancerBase No. 10 [Internet]. Lyon, France: InternationalAgency for Research on Cancer; 2010, http://globocan.iarc.fr,http://www.cancer.org/Research/CancerFactsFigures/cancer-facts-figures-2008, Accessed 05 November 2010

2. Hamphry LL, Helfand M, Chan BK, Woolf SH (2002) Breastcancer screening: a summary of the evidence for the U.S.Preventive Services Task Force. Ann Intern Med 137:347–360

3. National Comprehensive Cancer Network Guidelines (2011)Breast Cancer Screening and Diagnosis, version 1. 2011. http://www.nccn.org/professionals/physician_gls/pdf/breast-screening.pdf. Accessed 7 June 2011

4. KETEM anasayfa: http://ketem.org/ketem_nedir.php. Accessed 05November 2010

5. Hayran M, Abali H, Kilickap S, Aksoy H, Kemik A, Gokce H,Gokdemir H, Toplar S, Kaya D, Isbir GG (2010) Socio-demographic parameters in screening for breast cancer: lessonsfrom a population-based women's health project held in aprovince in Turkey. J BUON 15:726–731

J Canc Educ (2012) 27:347–352 351

6. Secginli S, Nahcivan NO (2006) Factors associated with breastcancer screening behaviours in a sample of Turkish women: aquestionnaire survey. Int J Nurs Stud 43:161–171

7. Sadikoglu G, Ozcakir A, Dogan F, Gokgoz S, Bilgel N (2010)Mammography utilization among Turkish Women. Asian Pac J ofCancer Prev 11:377–381

8. Organization for Economic Co-operation and Development (2007)OECDHealth Data. http://www.ecosante.org Accessed 01 April 2008

9. Secginli S, Nahcivan NO (2010) The effectiveness of a nurse-delivered breast health promotion program on breast cancerscreening behaviours in non-adherent Turkish women: a randomizedcontrolled trial. Int J Nurs Stud 2010. doi:10.1016/j.ijnurstu.2010.05.016

10. Budakoglu I, Maral I, Ozdemir A, Bumin A (2007) The effectivenessof training for breast cancer and breast self-examination in womenaged 40 and over. J of Cancer Educ 22:108–111

11. Wadler BM, Judge CM, Prout M, Allen JD, Geller AC (2011)Improving breast cancer control via the use of communityhealth workers in South Africa: a critical review. J of Oncol.doi:10.1155/2011/150423

12. Voyvoda N, Ozdemir A, Gultekin S (2007) Mammography deviceuse in Turkey, and quantity and quality analysis of mammographyeducation. Diagn Interv Radiol 13:129–133

13. Autier P, Ouakrim DA (2008) Determinants of the number ofmammography units in 31 countries with significant mammographyscreening. Br J of Cancer 99:1185–1190

352 J Canc Educ (2012) 27:347–352