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Breast cancer screening in developing countries

Breast cancer screening in developing countries REVIEW I,II, I II III Rene´ Aloı´sio da Costa Vieira, Gabriele Biller, Gilberto Uemura, Carlos Alberto Ruiz, IV Maria Paula Curado I II Programa de Po´ s-Graduac¸a˜o em Oncologia, Hospital de Caˆncer de Barretos, Barretos, SP, BR. Programa de Po´ s-graduac¸a˜o em Obstetricia, Ginecologia e III Mastologia, Faculdade de Medicina de Botucatu – UNESP, Botucatu, SP, BR. Departamento de Obstetricia e Ginecologia, Faculdade de Medicina, IV Universidade de Sao Paulo, Sao Paulo, SP, BR. International Prevention Research Institute, Lyon, France. Developing countries have limited healthcare resources and use different strategies to diagnose breast cancer. Most of the population depends on the public healthcare system, which affects the diagnosis of the tumor. Thus, the indicators observed in developed countries cannot be directly compared with those observed in developing countries because the healthcare infrastructures in developing countries are deficient. The aim of this study was to evaluate breast cancer screening strategies and indicators in developing countries. A systematic review and the Population, Intervention, Comparison, Outcomes, Timing, and Setting methodology were performed to identify possible indicators of presentation at diagnosis and the methodologies used in developing countries. We searched PubMed for the terms ‘‘Breast Cancer’’ or ‘‘Breast Cancer Screening’’ and ‘‘Developing Country’’ or ‘‘Developing Countries’’. In all, 1,149 articles were identified. Of these articles, 45 full articles were selected, which allowed us to identify indicators related to epidemiology, diagnostic intervention (diagnostic strategy, diagnostic infrastructure, percentage of women undergoing mammography), quality of intervention (presentation of symptoms at diagnosis, time to diagnosis, early stage disease), comparisons (trend curves, subpopulations at risk) and survival among different countries. The identification of these indicators will improve the reporting of methodologies used in developing countries and will allow us to evaluate improvements in public health related to breast cancer. KEYWORDS: Breast Neoplasms; Epidemiology; Prevention & Control; Mammography; Mass Screening; Developing Country. Vieira RA, Biller G, Uemura G, Ruiz CA, Curado MP. Breast cancer screening in developing countries. Clinics. 2017;72(4):244-253 Received for publication on September 24, 2016; First review completed on November 16, 2016; Accepted for publication on December 20, 2016 *Corresponding author. E-mail: posgrad@hcancerbarretos.com.br be efficiently promoted. To evaluate the complexity of the ’ INTRODUCTION healthcare system in relation to breast cancer, the ‘‘Breast Breast cancer is a global problem, and 1.7 million new Health Global Initiative’’ (BHGI) (4) has sought to categorize cases are diagnosed per year. Approximately 60% of deaths the organizational levels of countries in relation to breast due to breast cancer occur in developing countries (DCs) (1), cancer. Specifically, at the basic level, breast self-examination whereas in the United States (US), an estimated 249,260 new is encouraged, whereas diagnostic ultrasound and mammo- cases of breast cancer are diagnosed each year, and mortality graphy are available at a limited level. At the increased level, due to this disease is decreasing (2). In contrast, breast cancer patients have access to diagnostic mammography with oppor- in DCs represents one-half of all breast cancer cases and 62% tunistic breast screening, and at the maximum level, the popu- of the deaths (1). In Brazil, it is expected that the incidence of lation undergoes organized screening for breast cancer (4). breast cancer will be about one-fourth that of the US, but this In the US, 70% of women undergo mammographies. This increased incidence is associated with an increase in breast percentage is higher in white women (72.1%), women with a cancer-associated mortality (3). higher level of education (80.1%), women born in the USA Despite advances in medicine, breast cancer is diagnosed (71.6%), and women with health insurance (73.6%) (5). In coun- in the advanced stages in countries with limited resources tries with budgetary limits, the percentage of cancer diagnosis because early detection, diagnosis, and treatment cannot in the presence of a palpable mass (6) and adherence strategies based on self-breast examination are being discussed (7). The prognosis for breast cancer is considered good. The Copyright & 2017 CLINICS – This is an Open Access article distributed under the terms of the Creative Commons License (http://creativecommons.org/licenses/by/ survival rate is on the order of 73% in developed countries 4.0/) which permits unrestricted use, distribution, and reproduction in any and 57% in DCs. In the US, the 5-year survival rate is medium or format, provided the original work is properly cited. 89.7% (8, 9). Although the incidence of breast cancer is No potential conflict of interest was reported. lower in DCs, the mortality/incidence ratio is higher (8). Due DOI: 10.6061/clinics/2017(04)09 to economic and logistical constraints, a limited organized 244 CLINICS 2017;72(4):244-253 Screening in developing countries da Costa Vieira RA et al. network is aimed at the early diagnosis of breast cancer in full by two researchers (GB and RACV). Eighteen articles in DCs. Mammographic screening is not a reality, which were excluded because they were review articles on screen- is reflected in the high number of patients diagnosed at an ing strategies in DCs; 7 articles were excluded because they advanced stage. exclusively addressed underdeveloped countries; 3 articles It is difficult to compare or evaluate the health systems of were excluded because they were published in the 1990s and DCs, and it is also difficult to evaluate their improvement. were superseded by subsequent publications with different Based on this condition, it is important to consider indicators data; 27 articles were excluded for various reasons. Thus, that indirectly reflect the status and evolution of public health the 45 articles that were reviewed included numerical data systems related to breast cancer screening and diagnosis. It is regarding diagnostic methodology and tumor presentation a challenge to identify possible indicators associated with the at diagnosis. We included observational studies, prevalence diagnosis of early breast cancer because these populations studies and prevalence review articles. A summary of the lack real indirect indicators related to breast cancer screening results is shown in Figure 1. and indicators that can evaluate progressive improvements to We attempted to use the systematic review elements the healthcare system or that can compare healthcare systems formatting structure, PICOTS (Population- Intervention- among DCs. The identification of these indicators and the Comparator- Outcome- Timing- Setting) (10, 11), associating subsequent comparisons are the purpose of this study. elements suggested by the BHGI for DCs (4), and quality criteria to be used in mammographic screening (12). A Microsoft Excel table was generated, which identified the ’ MATERIALS AND METHODS PMID, first author, main results and potential indicators This study consists of an integrative systematic review based based on the PICOTS structure. We then attempted to group on a systematic search methodology to evaluate possible indi- studies according to subject matter, taking into account items cators related to methods of breast cancer screening and that reflected a possible health indicator, the methodology diagnosis in DCs. According to the Brazilian National Ethics used for breast cancer diagnosis, or items that reflected the Committee resolution 466, systematic reviews do not need to characteristics of breast cancer patients in DCs (Table 1). be evaluated by an Ethics Committee. Study methodologies The results observed for each item were then described to were not evaluated, but rather, publications that discussed this better understand the characteristics of mammographic subject were examined. screening and possible outcomes observed in DCs. The PubMed database was searched using the keywords ‘‘Breast Cancer ’’ or ‘‘Breast Cancer Screening’’ and ‘‘Develop- ’ RESULTS ing Country’’ or ‘‘Developing Countries’’. This search returned 1,149 articles published between April 1974 to September 30th, Based on PICOTS, where the scenario (Setting) is breast 2015. cancer diagnosis in DCs, a lack of controlled studies (Study After reading the titles and abstracts, we identified 100 design) was observed. We identified 45 articles consisting of potential articles discussing breast cancer indicators and 7 reviews and 38 original articles. These articles are presen- screening characteristics. All 100 identified articles were read ted in Table 1. In the intervention factor (I), we observed Figure 1 - PRISMA records flow diagram. 245 Screening in developing countries CLINICS 2017;72(4):244-253 da Costa Vieira RA et al. Table 1 - Indirect indicators related to breast cancer diagnosis in DCs. PICOT Factor Indicator Population Breast cancer Epidemiological Incidence of breast cancer Intervention Methodology or Diagnosis Diagnostic strategy methodology diagnostic condition National Guidelines; Screening age range Mammography infrastructure; % of population coverage % of mammographies performed Structuring of network with screening rounds Quality Form of presentation of symptoms at diagnosis Time to diagnosis % of early-stage cases (CS 0, CS 0+1, localized/regional disease) Comparator Control Trend curves/temporal data Vulnerable subpopulations Comparison among countries Outcome Final outcome Survival Mortality/incidence ratio Survival according to staging CS = clinical stage. factors relating to diagnosis and factors relating to diagnostic 58.2% had heard of BSEs (23). In Bangladesh, 41% of women quality. We present the individual results of each factor. did not know what breast cancer is, 71% did not know what screening is, and 96% did not know what a BSE is (36). Some studies cite referral services that attenuate these prob- Population lems and the use of breast ultrasound as an alternative method The incidence per 100,000 people differed, ranging from for the diagnosis of palpable lesions (37). One study describes 9.5 in Nigeria (13) to 65 in the Fuji islands (14) and 92.2 in four mammogram machines serving 7 million women (37), French Polynesia (14). Regional variations were also obser- and another states that only working women had access to ved, but the incidence was generally lower in DCs than in mammography (38). In fact, regions lacking public mammo- developed countries (13, 14). Noteworthy regional reviews graphy service have also been described (39). Therefore, diag- are available for Arab countries (13, 15, 16), Asia (14, 17) and nostic mammography rates are approximately 0.5% (33, 40). Latin America (18). Other reports describe slightly better situations, including diagnostic mammography, population campaigns, and Intervention/Diagnosis opportunistic mammography. A study from Jordan reports 14 mammography centers, with 7% of the population having Diagnostic strategy methodology/guidelines.Inmany mammograms and 17.9% having undergone screening (26). centers, breast self-examination (BSE) (19) and clinical breast In Mexico, 22% (24) of the population receives regular mam- examination (CBE) are keys to diagnosis when mammo- mograms. Positive educational interventions (41), isolated graphic diagnosis is not feasible (19, 20), but many women are regional experiences of the first round of mammographic screen- unaware of BSE and CBE (21). Furthermore, difficulties in ing (27, 42), and structured locations where only a minority of promoting education related to BSE have been cited (15), with patients are diagnosed late (43, 44) have been reported. approximately 3% (22) to 24% of women administering a BSE (21, 23) and 12.5% undergoing a CBE (15). In countries lacking government recommendations regard- Percentage of women undergoing mammography.A ing mammography, the recommended starting age for routine study conducted in Jamaica reported that 11.4% of women mammography varies widely, with starting ages of 25, 40, had undergone a mammography at least 5 years ago (45). or 50 years of age and upper limits of 64, 70, or 75 years In areas where mammography is opportunistically avai- of age; both annual or biennial repetition are suggested (16, lable, 42.1% of women aged 40-69 years had never had a 18, 24-27). mammogram (42), and these women are usually less educa- ted and of a lower socioeconomic class (46). Diagnostic infrastructure. A total of 5% of all world- wide expenditure on breast cancer screening takes place in Intervention/quality DCs. This limitation in resources and the many competing priorities mean that conducting mammography and provid- ing effective treatment are difficult (28) and that most tumors Presentation of symptoms at diagnosis. In the absence are consequently diagnosed at the advanced stages. Because of screening strategies, clinical examination leads to diag- breast cancer is often a fatal disease in some countries (29), nosis, and palpable tumors have been reported to represent screening and treatment are not considered cost-effective 90 to 100% of all cases at diagnosis (33, 36, 44, 47). This pro- (30). In addition, many countries lack a national program portion decreases to 26% after opportunistic mammographic (31-33) because national protocols regarding the appropriate screening (48). age range for mammography are not available (34). These The size of invasive tumors can also be used to evaluate conditions lead to a lack of information about the importance disease, and the average sizes in Singapore and Malaysia of mammography. Similarly, BSE and CBE can be used as are 2.2 cm and 3.0 cm, respectively (49). A review evaluating diagnostic and screening methods (35), but this strategy may tumor characteristics in Asia and Africa reveals tumors aver- not be employed at the public health level. In Nigeria, 75.6% aging 3.3 cm in Tunisia, and 4.8 cm in Sudan and Nigeria. of studied women had never performed a BSE, and only In Pakistan, 80% of tumors are larger than 2 cm (50, 51). 246 CLINICS 2017;72(4):244-253 Screening in developing countries da Costa Vieira RA et al. Time between the finding of a breast abnormality or observed differences in diagnosis rates between DCs and examination and diagnosis. Because of both technology- developed countries (53, 57). Localized disease represents based inefficiency and problems with access, few patients 25.2% of the tumors in Egypt, 27.8% in Saudi Arabia, 52.0% undergo treatment in well-equipped centers that feature in Germany and 62.3% in the US (53). protocols. Limited technology, economic reasons, and nutri- The TNM staging system is more often used in articles tional problems lead to maintenance of the disease’s pre- related to DCs. When only invasive disease is evaluated, valence (20). Furthermore, this equipment may be available stage I tumor staging rates were below 5% in India, the Phil- but in insufficient numbers to serve the entire population ippines, and Nigeria, but the rates exceeded 30% in South quickly. Therefore, a long time can elapse between a clinical Korea and Taiwan (50, 51, 53). Based on three reviews (50, 51, complaint and the start of treatment. In better structured 53), we compared the percentage of clinical stage I patients areas, limited equipment and diagnostic flow in the public and data from the Human Development Index (13, 58); we network leads to delays in diagnosis, which reportedly range chose the year 2008 as a reference because that was the from 1 to 3 (52), 8 (53) and 10 months (33). These delays publication year of the articles reviewed. Only one publica- are inversely proportional to the degree of organization of tion was selected by country, and we chose only countries the healthcare system (54). Generally, the delay is less than with an estimated HDI. Data were entered and plotted using 1 month in developed countries and more than 2.5 months in IBM SPSS Statistics 20 for Mac (Armonk, New York, NY). DCs (53). We observed a linear relationship (R = 0,526) related to HDI and clinical stage, as a high HDI was associated with a higher rate of clinical stage I disease, and a lower HDI was Percentage of cases diagnosed at an early stage.In associated with lower rate (Figure 2). general, the rate of patients diagnosed with carcinoma in situ is low, ranging from 1% in India (17) and Pakistan (55) to Comparisons 7.4% in Iran (56). Considering early stage as clinical stage (CS) 0 and I, the rate of individuals diagnosed with early-stage tumors varies and is 5% in India (17), 10% in Pakistan (55), Trend curves/temporal data. Studies demonstrating and 13.9% in Iran (56). In Brazil, the introduction of a temporal changes indirectly show changes in the healthcare regional screening program resulted in an increase in tumors system. For example, a study in Egypt showed that the loca- diagnosed during the early stage from 14.5% to 43.2% (42). lized and metastatic disease rates were 14.8% and 14.0% The infrastructure of Hong Kong differs and resulted in in 1999, respectively, whereas they were 20.8% and 11.9%, detection rates of 13% for CS 0 and 47% for early-stage respectively, in 2008. This change may be attributed to disease (17). A study conducted in Malaysia compared improvements in the local healthcare system (59). Similarly, a women selected with mammographic screening and diag- study of a Lebanese hospital showed a small improvement in nostic mammography and found respective CS 0 diagnosis the early diagnosis rate (CS 0 + I), which was 23.8% from rates of 23.0% and 2.6% and respective early-stage cancer 1990-1995 but changed to 25.8% from 2008-2013 (25). A study diagnosis rates of 53.8% and 27.0% (48). conducted in Iran did not show temporal changes in the The localized/regional/metastatic staging methodology early-stage diagnoses between 1994-1997 and 2006-2009, is not used as frequently in publications in DCs, but we which were 13% and 13.9%, respectively (56). Figure 2 - Scatter plot comparing the Human Development Index and the percentage of clinical stage I cases selected by country. PA = Porto Alegre; SA = Saudi Arabia; SP = Sa˜o Paulo. 247 Screening in developing countries CLINICS 2017;72(4):244-253 da Costa Vieira RA et al. Subpopulations in the same country. A study conduc- 50% in many countries (14, 18, 64). Moreover, the per capita ted in Iran compared women of different socioeconomic income directly correlates with incidence and inversely correlates classes; the BSE, CBE and mammography rates were 4.1%, with mortality (65), reflecting late diagnoses, poor healthcare 5.6% and 4.8%, respectively, among the poorest women and and high mortality (66) in DCs. In many countries, incidence 83.9%, 90.3% and 87.4%, respectively, among women of a (14) and mortality tended to increase (1, 18, 67), whereas mor- higher socioeconomic class (60). Similarly, black people in tality tended to decrease in high-income countries (67). South Africa had lower rates of localized staging (5%) at Moreover, the survival rate was 11% higher in Singapore diagnosis compared with whites (31%), a fact that reflects than in Malaysia. However, differences in tumor size at socioeconomic differences relating to diagnostic access (57, 61). diagnosis, clinical stage at diagnosis, and treatment were also observed, all of which contributed to a higher survival rate of Singaporean patients (49). Comparisons among countries. Because of limitations of organized databases in DCs, studies on this subject are also limited. In Brazil, comparing a hospital records series ’ DISCUSSION with Surveillance, Epidemiology and End Results (SEER) data, Brazilian patients were younger, demonstrated a longer This study is a literature review that describes potential medical history, presented with larger tumors and were less indicators related to the diagnosis of breast cancer in develop- likely to have clinical stage I disease (10.2% x 50.1%), which ing countries. Based on this study type, we opted to use the were all reflected by the lower overall survival rate of 19.6 methodology of systematic reviews, using PRISMA and percentage points and a cancer specific survival of 26.9 per- PICOTS, to evaluate possible ways that the health systems centage points. This effect almost disappeared when compar- in DCs can be assessed. It was not possible to perform a meta- ing overall survival by stage [Figure 3 (62)], which suggests analysis with odds ratios and forest plots because a meta- that the difference may have been due to the excessive num- analysis requires case-control or randomized studies, which ber of patients diagnosed at the early stage in the US (46). are not often published in DCs. Because we found observa- tional studies, prevalence studies and prevalence review Outcome/Survival. Despite the lower incidence rates, articles, we opted to perform an integrative systematic review. 45% of worldwide breast cancer cases and 54% of deaths due The studies were summarized by topic according to the to breast cancer worldwide occur in DCs (63). The mortality/ PRISMA criteria for selection. We identified potential indica- incidence ratio reflects the structure of these countries better tors (Table 1) that can be used to compare differences and to than simple numeric mortality data, and this ratio exceeds evaluate improvement in public health systems. Figure 3 - Survival according to the SEER study (blue) and a Brazilian Oncologic Hospital (HCB, green). (a) Overall survival (OS); (b) cancer- specific survival (SS); (c) overall survival selected by clinical stage (CS) at diagnosis. Unpublished Figure (ref 62) authorized by the Authors. 248 CLINICS 2017;72(4):244-253 Screening in developing countries da Costa Vieira RA et al. BSEs and CBEs have long been considered to be important Currently, many studies arguing against and in favor of methodologies to be implemented at the population level. mammographic screening are available. Decreases in the size However, scientific evidence regarding the effectiveness of of diagnosed lesions, decreases in breast cancer mortality, CBEs or BSEs in reducing mortality from breast cancer is longer lifespans, an acceptable overdiagnosis level (1-10%), currently lacking. Randomized studies carried out in China and the frequency of carcinoma in situ all support the use of (68) and Russia (69) have led to a loss in support for BSEs as mammographic screening (12, 75, 80). Conversely, partial an early detection method because the breast cancer mor- evaluations of systematic reviews (80), discussions about the tality rates did not differ between women who performed actual decline in advanced stage tumors in the US (81), and BSEs and those who did not. In this context, women are the rate of overdiagnosis (31%) (81) do not support the use of encouraged to be alert to any changes in the breast, and CBEs mammographic screening. Moreover, although some studies are part of this awareness and may lead the woman to a show that lives are indeed saved by mammographic screen- diagnostic evaluation. According to the Brazilian Society for ing, the number of survivors is low (82, 83). In general, stu- Mastology, BSEs/CBEs in isolation are not encouraged but dies of doctors who see patients support the use of screening are always associated with the use of mammography, espe- (75, 77), whereas studies performed by epidemiologists argue cially in women over 40. againstthis typeofscreening(81),and suggestthatwomen The sensitivity of breast self-examination (BSE) is low (20 should be well informed regarding mammographic screening to 30%), and it is not associated with a decrease in mortality. and aware of the pros and cons (82, 83). This fact is especially Mammography has a sensitivity of 63 to 95% (37), and it relevant in developed countries, where high income and educa- is the only exam that has been demonstrated to be related tion levels characterize much of the population. to a decrease in mortality. Its sensitivity increases with the In countries with extremely limited public health resources, presence of palpable lumps and decreases in dense breasts. infectious diseases are the main public health problem. The Approximately 10%-30% of breast cancers are not detected extent to which these diseases are controlled to increase life by mammography because of many possible factors such as expectancy changes disease profiles. The age distribution of dense parenchyma, obscure lesions, poor positioning, per- the population affects the incidence of cancer, with a decrease ception error, incorrect interpretations, subtype tumors, slow in age at diagnosis being observed in some countries (37). In growing tumors, the presence of interval carcinomas and DCs, most of the population earns a low income. Therefore, smaller-sized tumors (70). Based on these factors, the woman healthcare usually depends on government actions and public must perform a regular evaluation by BSE and/or undergo health infrastructure. Healthcare provision is related to the a clinical breast evaluation by a healthcare professional. Together, availability of resources, and many diseases compete for these these exams must be considered in the diagnostic evaluation in resources. Public health practices are linked to national guide- addition to a breast ultrasound insymptomatic women(71). lines and available methodologies, which are associated with Breast cancer screening by mammography is the best public education processes and the availability of public net- secondary prevention methodology for the population; it work demand absorbency. Therefore, not only tumor-related serves as a disease intervention measure and promotes early or epidemiological criteria but also account resource avail- detection in the asymptomatic phase. Specifically, screening ability are important when evaluating the age range for substantially reduces the morbidity and mortality due to late screening strategies because data in DCs are generally limited diagnosis. The HIP study (Health Insurance Plan) was the and rely on studies conducted in developed countries. Thus, first to demonstrate a reduction in breast cancer mortality strategies are lacking, and BSEs are used as a screening (30%) as a result of mammographic screening. In the 2006 strategy, whereas ultrasound is used as a diagnostic strategy. and 2009 Cochrane reviews, the reduction was approxi- In DCs, mammograms are not performed primarily because mately 15%. In the last review (2013), which only evaluated of barriers in the healthcare system, which are affected by the randomized studies, they did not observe a reduction in following: the accessibility of health services, unsatisfactory mortality, but a reduction on the order of 25% was found medical adherence due to public healthcare system limitations, when observational studies were included; and when group- the cost of tests, and difficulty in implementing follow-up ing all studies together, this reduction was 19% (72). The tests (5, 84). The evaluation of factors relating to the health- greater likelihood of reducing breast cancer mortality in care system and non-adherence to mammogram screening several developed countries can be attributed to screening guidelines is complex because such evaluations lack a specific programs and the evolution of adjunct therapy (73), (74). indicator. The cultural context is interwoven with the infrastruc- More recent studies have questioned these figures, arguing ture, the limitation of trained personnel, and the effective that this reduction is on the order of 8%, but these studies stratification of examinations up to the point of diagnosis, were conducted in developed countries and many metho- which should be quick, comprehensive, and effective. Never- dological problems were questioned (75). theless, this effect can be assessed by evaluating mammo- Screening primarily reduces mortality in women between graphy available to the public, population coverage, and the 50 and 69-74 years of age, with less dramatic results in percentage of mammography exams performed. In this con- women who are 40-49 years of age. Thus, mammography text, access to mammography refers to the presence of this should be performed on a large scale at the population level technology, the ease of the general population’saccess toit, the for this age group to reduce breast cancer mortality. The quality of the tests performed, and the possibility of perfor- Brazilian Society of Mastology suggests that the starting ming additional tests focused on biopsy and differential age should be 40 years (76), which was also suggested by diagnosis. Logistical and technological limitations delay tests the American Cancer Society until 2015 (77). In 2016, this prior to diagnosis, result in low population coverage, and gene- suggestion was changed to age 45 (78). EUSOMA (12), the rally limit access to regular mammograms. DCs report difficul- US Preventive Services Task Force (79) and the Brazilian ties with respect to mammography screening in women, while Ministry of Health (42) suggest that organized population developed countries discuss the practice of mammography for screening commence at age 50. specific ages, as 57.2% of the women aged 50 to 74 in the 249 Screening in developing countries CLINICS 2017;72(4):244-253 da Costa Vieira RA et al. US (85) undergo regular mammography. In addition, the stage II (4.7 pp at 5-years and 6.6 pp at 10-years; p=0.001) qualities of breast cancer screening methods and accreditation disease. However, these differences were associated with the programs are reported in developed countries (12, 86, 87). This quality of mortality data, the loss of follow-up information, fact reflects the clinical stage at diagnosis, as early clinical stage as well as differences in treatment protocols and molecular disease (EC 0 and I) represents 5% of all tumors in India (17) subtypes, which renders it difficult to make comparisons and 50.9% in Europe (86). In DCs, tumors are usually palpable, among countries (62). large, and not at an early clinical stage at the time of diagnosis If we consider that mammographic screening and early (Figure 2). Conversely, tumors diagnosed only by mammogra- diagnosis are not related to an increase in the survival, as phy are infrequent, and the incidence of carcinoma in situ is shown in some randomized studies, we must not forget that low. For example, carcinoma in situ varies and was 0.1% in these studies were performed in developed countries, where African registries, 1% in India, 11.4% in Europe, 16% in North favorable conditions are present for diagnosis and treatment. America and approximately 4.5%inother regionsofthe world In reality, the opposite conditions are present in DCs, a fact (9, 17, 86). that reflects the lower rate of early diagnosis and poor sur- Although tumors smaller than 2 cm can be detected by vival. It is therefore important to have a progressive structur- clinical examination, they must be superficial, and the great ing of public health systems. To evaluate this condition, we majority of these tumors that are detected by mammography found possible indicators that can be reported and that can be are smaller than 2 cm (88). Technology is associated with a used in future studies performed in DCs (Table 1). local infrastructure and is based on mammograms, ultra- The identification of subpopulations or analysis based on sound, biopsy (open or core biopsy) and pathology. This socioeconomic conditions helps to understand the context reflects the lower percentage of early breast cancers detected of a population that is more dependent on the public health- in DCs. The HDI shows the association of PIB per capita and care system. Similarly, the observation of temporal data the life expectancy, which may indirectly reflect the health allows us to evaluate progress relating to the structuring of system. People have a socioeconomic dependence on public the public healthcare system. Limitations in diagnosis and health systems, and therefore, the public health system is treatment lead to a high mortality/incidence ratio (74); speci- not a choice but may be the only option for many women. To fically, diagnosis is delayed, and many treatments are not evaluate the clinical stage at diagnosis, the TNM staging performed based on protocols (20). system is a standard and acceptable approach. We observed When using the PICOTS methodology for diagnostic tests different frequencies of stages based on clinical stage 0 to IV (11), the Timing (T) and Setting (S) are observed, but studies (five categories) or clinical stage I to IV (four categories). The of these factors were not available. Therefore, we present evaluation of the percentage of cases at clinical stage 0 would general aspects (PICO; Table 1). Some review articles on the be based primarily on mammography-detected tumors, but subject were included in the overall review, but they were these data were not reported in all the included studies. If we not selected in the 45 articles that determined the indicators use the four categories listed above, we must pay attention because they do not show potential indicators. to clinical stage I. Tumors larger than 2 cm are frequently Two aspects should be emphasized in this study. In the palpable and clinically detectable. Based on this observation, initial evaluation, the search was conducted using keywords we generated Figure 2 and chose data from clinical stage I to that are associated with case-control studies. This search IV, as data related to clinical stage 0 were insufficient. We revealed 4 publications, but none of these publications observed a linear relationship of the HDI and clinical stage, included possible indicators, which led us to review gene- as a high HDI was associated with a higher rate of clinical ral articles to identify possible indicators. Furthermore, the stage I, while a lower HDI was associated with lower clinical separation between DCs and underdeveloped countries stage I (Figure 2). presented another problem. The literature evaluated lacks a In terms of survival, patients with early-stage disease clear separation between the two, despite the possibility of exhibit excellent survival rates, whereas patients with meta- using World Bank classifications (90). Therefore, underdevel- stasis at the time of diagnosis have limited survival. Dif- oped countries could not be excluded from the evaluation. ferences in survival are primarily due to differences in Limitations of the present study include the following: clinical stage at the time of diagnosis and the ability to only 1 database was used; the evaluation of articles was provide adjunct therapy at the population level, which is not based on the level of evidence but rather on available reflected in the 5-year survival rates in different countries data, which we attempted to systematically evaluate; and (89). The CONCORD study evaluated population-based comparisons of all indicators in developed countries were cancer registries from 2005-2009 and estimated the 5-year not reported. The objective was to identify potential indi- survival rate after observing lower survival rates in South cators identified by a systematic methodology. Consequently, Africa (53%), Mongolia (57%), India (60%) and higher indirect indicators that can be used in DCs were identified, survival rates in North America and Oceania (84-89%). which elucidated the conditions relating to breast cancer Its study showed that differences in the 5-year cancer diagnosis in DCs. The systematic identification and descrip- specific-survival were dependent on the country (9). After tion of these indicators will facilitate comparisons among a comparison of the SEER database with an institutional countries, the evaluation of public services, and the evalua- Brazilian database adjusted by the same characteristics, a tion of outcomes of the progressive structuring of healthcare similar 10-year global survival rate was observed according systems. to clinical stage, which reminds us to consider the influence Currently, the validity of mammographic screening and of the percentage of early clinical stage cases on the overall mammography is under discussion, but such discussions are survival, and the importance of long-term follow-up. In this carried out in countries with structured healthcare systems publication, the cancer-specific survival was not discussed, that allow for diagnosis and treatment, irrespective of who and differences were observed in patients with clinical stage I absorbs the costs of this process. A better understanding of the (3.6 at 5-years and 13.0% at 10-years; p=0.001) and clinical alternate reality, that is, comparisons between limited public 250 CLINICS 2017;72(4):244-253 Screening in developing countries da Costa Vieira RA et al. healthcare systems in terms of technology or access to mam- 13. Mehdi I, Monem EA, Al Bahrani BJ, Al Kharusi S, Nada AM, Al Lawati J, et al. Age at diagnosis of female breast cancer in Oman: Issues and mography, will enable us to better understand the benefits of implications. South Asian J Cancer. 2014;3(2):101-6, http://dx.doi.org/ this diagnostic modality and mammographic screening. 10.4103/2278-330X.130442. Mammographic screening is proved to be beneficial when 14. Youlden DR, Cramb SM, Yip CH, Baade PD. Incidence and mortality of female breast cancer in the Asia-Pacific region. Cancer Biol Med. 2014; it is performed in an organized and regular manner in the 11(2):101-15. form of a national public health policy or when the per capita 15. 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Breast cancer screening in developing countries

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Pubmed Central
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Copyright © 2017 CLINICS
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1807-5932
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10.6061/clinics/2017(04)09
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Abstract

REVIEW I,II, I II III Rene´ Aloı´sio da Costa Vieira, Gabriele Biller, Gilberto Uemura, Carlos Alberto Ruiz, IV Maria Paula Curado I II Programa de Po´ s-Graduac¸a˜o em Oncologia, Hospital de Caˆncer de Barretos, Barretos, SP, BR. Programa de Po´ s-graduac¸a˜o em Obstetricia, Ginecologia e III Mastologia, Faculdade de Medicina de Botucatu – UNESP, Botucatu, SP, BR. Departamento de Obstetricia e Ginecologia, Faculdade de Medicina, IV Universidade de Sao Paulo, Sao Paulo, SP, BR. International Prevention Research Institute, Lyon, France. Developing countries have limited healthcare resources and use different strategies to diagnose breast cancer. Most of the population depends on the public healthcare system, which affects the diagnosis of the tumor. Thus, the indicators observed in developed countries cannot be directly compared with those observed in developing countries because the healthcare infrastructures in developing countries are deficient. The aim of this study was to evaluate breast cancer screening strategies and indicators in developing countries. A systematic review and the Population, Intervention, Comparison, Outcomes, Timing, and Setting methodology were performed to identify possible indicators of presentation at diagnosis and the methodologies used in developing countries. We searched PubMed for the terms ‘‘Breast Cancer’’ or ‘‘Breast Cancer Screening’’ and ‘‘Developing Country’’ or ‘‘Developing Countries’’. In all, 1,149 articles were identified. Of these articles, 45 full articles were selected, which allowed us to identify indicators related to epidemiology, diagnostic intervention (diagnostic strategy, diagnostic infrastructure, percentage of women undergoing mammography), quality of intervention (presentation of symptoms at diagnosis, time to diagnosis, early stage disease), comparisons (trend curves, subpopulations at risk) and survival among different countries. The identification of these indicators will improve the reporting of methodologies used in developing countries and will allow us to evaluate improvements in public health related to breast cancer. KEYWORDS: Breast Neoplasms; Epidemiology; Prevention & Control; Mammography; Mass Screening; Developing Country. Vieira RA, Biller G, Uemura G, Ruiz CA, Curado MP. Breast cancer screening in developing countries. Clinics. 2017;72(4):244-253 Received for publication on September 24, 2016; First review completed on November 16, 2016; Accepted for publication on December 20, 2016 *Corresponding author. E-mail: posgrad@hcancerbarretos.com.br be efficiently promoted. To evaluate the complexity of the ’ INTRODUCTION healthcare system in relation to breast cancer, the ‘‘Breast Breast cancer is a global problem, and 1.7 million new Health Global Initiative’’ (BHGI) (4) has sought to categorize cases are diagnosed per year. Approximately 60% of deaths the organizational levels of countries in relation to breast due to breast cancer occur in developing countries (DCs) (1), cancer. Specifically, at the basic level, breast self-examination whereas in the United States (US), an estimated 249,260 new is encouraged, whereas diagnostic ultrasound and mammo- cases of breast cancer are diagnosed each year, and mortality graphy are available at a limited level. At the increased level, due to this disease is decreasing (2). In contrast, breast cancer patients have access to diagnostic mammography with oppor- in DCs represents one-half of all breast cancer cases and 62% tunistic breast screening, and at the maximum level, the popu- of the deaths (1). In Brazil, it is expected that the incidence of lation undergoes organized screening for breast cancer (4). breast cancer will be about one-fourth that of the US, but this In the US, 70% of women undergo mammographies. This increased incidence is associated with an increase in breast percentage is higher in white women (72.1%), women with a cancer-associated mortality (3). higher level of education (80.1%), women born in the USA Despite advances in medicine, breast cancer is diagnosed (71.6%), and women with health insurance (73.6%) (5). In coun- in the advanced stages in countries with limited resources tries with budgetary limits, the percentage of cancer diagnosis because early detection, diagnosis, and treatment cannot in the presence of a palpable mass (6) and adherence strategies based on self-breast examination are being discussed (7). The prognosis for breast cancer is considered good. The Copyright & 2017 CLINICS – This is an Open Access article distributed under the terms of the Creative Commons License (http://creativecommons.org/licenses/by/ survival rate is on the order of 73% in developed countries 4.0/) which permits unrestricted use, distribution, and reproduction in any and 57% in DCs. In the US, the 5-year survival rate is medium or format, provided the original work is properly cited. 89.7% (8, 9). Although the incidence of breast cancer is No potential conflict of interest was reported. lower in DCs, the mortality/incidence ratio is higher (8). Due DOI: 10.6061/clinics/2017(04)09 to economic and logistical constraints, a limited organized 244 CLINICS 2017;72(4):244-253 Screening in developing countries da Costa Vieira RA et al. network is aimed at the early diagnosis of breast cancer in full by two researchers (GB and RACV). Eighteen articles in DCs. Mammographic screening is not a reality, which were excluded because they were review articles on screen- is reflected in the high number of patients diagnosed at an ing strategies in DCs; 7 articles were excluded because they advanced stage. exclusively addressed underdeveloped countries; 3 articles It is difficult to compare or evaluate the health systems of were excluded because they were published in the 1990s and DCs, and it is also difficult to evaluate their improvement. were superseded by subsequent publications with different Based on this condition, it is important to consider indicators data; 27 articles were excluded for various reasons. Thus, that indirectly reflect the status and evolution of public health the 45 articles that were reviewed included numerical data systems related to breast cancer screening and diagnosis. It is regarding diagnostic methodology and tumor presentation a challenge to identify possible indicators associated with the at diagnosis. We included observational studies, prevalence diagnosis of early breast cancer because these populations studies and prevalence review articles. A summary of the lack real indirect indicators related to breast cancer screening results is shown in Figure 1. and indicators that can evaluate progressive improvements to We attempted to use the systematic review elements the healthcare system or that can compare healthcare systems formatting structure, PICOTS (Population- Intervention- among DCs. The identification of these indicators and the Comparator- Outcome- Timing- Setting) (10, 11), associating subsequent comparisons are the purpose of this study. elements suggested by the BHGI for DCs (4), and quality criteria to be used in mammographic screening (12). A Microsoft Excel table was generated, which identified the ’ MATERIALS AND METHODS PMID, first author, main results and potential indicators This study consists of an integrative systematic review based based on the PICOTS structure. We then attempted to group on a systematic search methodology to evaluate possible indi- studies according to subject matter, taking into account items cators related to methods of breast cancer screening and that reflected a possible health indicator, the methodology diagnosis in DCs. According to the Brazilian National Ethics used for breast cancer diagnosis, or items that reflected the Committee resolution 466, systematic reviews do not need to characteristics of breast cancer patients in DCs (Table 1). be evaluated by an Ethics Committee. Study methodologies The results observed for each item were then described to were not evaluated, but rather, publications that discussed this better understand the characteristics of mammographic subject were examined. screening and possible outcomes observed in DCs. The PubMed database was searched using the keywords ‘‘Breast Cancer ’’ or ‘‘Breast Cancer Screening’’ and ‘‘Develop- ’ RESULTS ing Country’’ or ‘‘Developing Countries’’. This search returned 1,149 articles published between April 1974 to September 30th, Based on PICOTS, where the scenario (Setting) is breast 2015. cancer diagnosis in DCs, a lack of controlled studies (Study After reading the titles and abstracts, we identified 100 design) was observed. We identified 45 articles consisting of potential articles discussing breast cancer indicators and 7 reviews and 38 original articles. These articles are presen- screening characteristics. All 100 identified articles were read ted in Table 1. In the intervention factor (I), we observed Figure 1 - PRISMA records flow diagram. 245 Screening in developing countries CLINICS 2017;72(4):244-253 da Costa Vieira RA et al. Table 1 - Indirect indicators related to breast cancer diagnosis in DCs. PICOT Factor Indicator Population Breast cancer Epidemiological Incidence of breast cancer Intervention Methodology or Diagnosis Diagnostic strategy methodology diagnostic condition National Guidelines; Screening age range Mammography infrastructure; % of population coverage % of mammographies performed Structuring of network with screening rounds Quality Form of presentation of symptoms at diagnosis Time to diagnosis % of early-stage cases (CS 0, CS 0+1, localized/regional disease) Comparator Control Trend curves/temporal data Vulnerable subpopulations Comparison among countries Outcome Final outcome Survival Mortality/incidence ratio Survival according to staging CS = clinical stage. factors relating to diagnosis and factors relating to diagnostic 58.2% had heard of BSEs (23). In Bangladesh, 41% of women quality. We present the individual results of each factor. did not know what breast cancer is, 71% did not know what screening is, and 96% did not know what a BSE is (36). Some studies cite referral services that attenuate these prob- Population lems and the use of breast ultrasound as an alternative method The incidence per 100,000 people differed, ranging from for the diagnosis of palpable lesions (37). One study describes 9.5 in Nigeria (13) to 65 in the Fuji islands (14) and 92.2 in four mammogram machines serving 7 million women (37), French Polynesia (14). Regional variations were also obser- and another states that only working women had access to ved, but the incidence was generally lower in DCs than in mammography (38). In fact, regions lacking public mammo- developed countries (13, 14). Noteworthy regional reviews graphy service have also been described (39). Therefore, diag- are available for Arab countries (13, 15, 16), Asia (14, 17) and nostic mammography rates are approximately 0.5% (33, 40). Latin America (18). Other reports describe slightly better situations, including diagnostic mammography, population campaigns, and Intervention/Diagnosis opportunistic mammography. A study from Jordan reports 14 mammography centers, with 7% of the population having Diagnostic strategy methodology/guidelines.Inmany mammograms and 17.9% having undergone screening (26). centers, breast self-examination (BSE) (19) and clinical breast In Mexico, 22% (24) of the population receives regular mam- examination (CBE) are keys to diagnosis when mammo- mograms. Positive educational interventions (41), isolated graphic diagnosis is not feasible (19, 20), but many women are regional experiences of the first round of mammographic screen- unaware of BSE and CBE (21). Furthermore, difficulties in ing (27, 42), and structured locations where only a minority of promoting education related to BSE have been cited (15), with patients are diagnosed late (43, 44) have been reported. approximately 3% (22) to 24% of women administering a BSE (21, 23) and 12.5% undergoing a CBE (15). In countries lacking government recommendations regard- Percentage of women undergoing mammography.A ing mammography, the recommended starting age for routine study conducted in Jamaica reported that 11.4% of women mammography varies widely, with starting ages of 25, 40, had undergone a mammography at least 5 years ago (45). or 50 years of age and upper limits of 64, 70, or 75 years In areas where mammography is opportunistically avai- of age; both annual or biennial repetition are suggested (16, lable, 42.1% of women aged 40-69 years had never had a 18, 24-27). mammogram (42), and these women are usually less educa- ted and of a lower socioeconomic class (46). Diagnostic infrastructure. A total of 5% of all world- wide expenditure on breast cancer screening takes place in Intervention/quality DCs. This limitation in resources and the many competing priorities mean that conducting mammography and provid- ing effective treatment are difficult (28) and that most tumors Presentation of symptoms at diagnosis. In the absence are consequently diagnosed at the advanced stages. Because of screening strategies, clinical examination leads to diag- breast cancer is often a fatal disease in some countries (29), nosis, and palpable tumors have been reported to represent screening and treatment are not considered cost-effective 90 to 100% of all cases at diagnosis (33, 36, 44, 47). This pro- (30). In addition, many countries lack a national program portion decreases to 26% after opportunistic mammographic (31-33) because national protocols regarding the appropriate screening (48). age range for mammography are not available (34). These The size of invasive tumors can also be used to evaluate conditions lead to a lack of information about the importance disease, and the average sizes in Singapore and Malaysia of mammography. Similarly, BSE and CBE can be used as are 2.2 cm and 3.0 cm, respectively (49). A review evaluating diagnostic and screening methods (35), but this strategy may tumor characteristics in Asia and Africa reveals tumors aver- not be employed at the public health level. In Nigeria, 75.6% aging 3.3 cm in Tunisia, and 4.8 cm in Sudan and Nigeria. of studied women had never performed a BSE, and only In Pakistan, 80% of tumors are larger than 2 cm (50, 51). 246 CLINICS 2017;72(4):244-253 Screening in developing countries da Costa Vieira RA et al. Time between the finding of a breast abnormality or observed differences in diagnosis rates between DCs and examination and diagnosis. Because of both technology- developed countries (53, 57). Localized disease represents based inefficiency and problems with access, few patients 25.2% of the tumors in Egypt, 27.8% in Saudi Arabia, 52.0% undergo treatment in well-equipped centers that feature in Germany and 62.3% in the US (53). protocols. Limited technology, economic reasons, and nutri- The TNM staging system is more often used in articles tional problems lead to maintenance of the disease’s pre- related to DCs. When only invasive disease is evaluated, valence (20). Furthermore, this equipment may be available stage I tumor staging rates were below 5% in India, the Phil- but in insufficient numbers to serve the entire population ippines, and Nigeria, but the rates exceeded 30% in South quickly. Therefore, a long time can elapse between a clinical Korea and Taiwan (50, 51, 53). Based on three reviews (50, 51, complaint and the start of treatment. In better structured 53), we compared the percentage of clinical stage I patients areas, limited equipment and diagnostic flow in the public and data from the Human Development Index (13, 58); we network leads to delays in diagnosis, which reportedly range chose the year 2008 as a reference because that was the from 1 to 3 (52), 8 (53) and 10 months (33). These delays publication year of the articles reviewed. Only one publica- are inversely proportional to the degree of organization of tion was selected by country, and we chose only countries the healthcare system (54). Generally, the delay is less than with an estimated HDI. Data were entered and plotted using 1 month in developed countries and more than 2.5 months in IBM SPSS Statistics 20 for Mac (Armonk, New York, NY). DCs (53). We observed a linear relationship (R = 0,526) related to HDI and clinical stage, as a high HDI was associated with a higher rate of clinical stage I disease, and a lower HDI was Percentage of cases diagnosed at an early stage.In associated with lower rate (Figure 2). general, the rate of patients diagnosed with carcinoma in situ is low, ranging from 1% in India (17) and Pakistan (55) to Comparisons 7.4% in Iran (56). Considering early stage as clinical stage (CS) 0 and I, the rate of individuals diagnosed with early-stage tumors varies and is 5% in India (17), 10% in Pakistan (55), Trend curves/temporal data. Studies demonstrating and 13.9% in Iran (56). In Brazil, the introduction of a temporal changes indirectly show changes in the healthcare regional screening program resulted in an increase in tumors system. For example, a study in Egypt showed that the loca- diagnosed during the early stage from 14.5% to 43.2% (42). lized and metastatic disease rates were 14.8% and 14.0% The infrastructure of Hong Kong differs and resulted in in 1999, respectively, whereas they were 20.8% and 11.9%, detection rates of 13% for CS 0 and 47% for early-stage respectively, in 2008. This change may be attributed to disease (17). A study conducted in Malaysia compared improvements in the local healthcare system (59). Similarly, a women selected with mammographic screening and diag- study of a Lebanese hospital showed a small improvement in nostic mammography and found respective CS 0 diagnosis the early diagnosis rate (CS 0 + I), which was 23.8% from rates of 23.0% and 2.6% and respective early-stage cancer 1990-1995 but changed to 25.8% from 2008-2013 (25). A study diagnosis rates of 53.8% and 27.0% (48). conducted in Iran did not show temporal changes in the The localized/regional/metastatic staging methodology early-stage diagnoses between 1994-1997 and 2006-2009, is not used as frequently in publications in DCs, but we which were 13% and 13.9%, respectively (56). Figure 2 - Scatter plot comparing the Human Development Index and the percentage of clinical stage I cases selected by country. PA = Porto Alegre; SA = Saudi Arabia; SP = Sa˜o Paulo. 247 Screening in developing countries CLINICS 2017;72(4):244-253 da Costa Vieira RA et al. Subpopulations in the same country. A study conduc- 50% in many countries (14, 18, 64). Moreover, the per capita ted in Iran compared women of different socioeconomic income directly correlates with incidence and inversely correlates classes; the BSE, CBE and mammography rates were 4.1%, with mortality (65), reflecting late diagnoses, poor healthcare 5.6% and 4.8%, respectively, among the poorest women and and high mortality (66) in DCs. In many countries, incidence 83.9%, 90.3% and 87.4%, respectively, among women of a (14) and mortality tended to increase (1, 18, 67), whereas mor- higher socioeconomic class (60). Similarly, black people in tality tended to decrease in high-income countries (67). South Africa had lower rates of localized staging (5%) at Moreover, the survival rate was 11% higher in Singapore diagnosis compared with whites (31%), a fact that reflects than in Malaysia. However, differences in tumor size at socioeconomic differences relating to diagnostic access (57, 61). diagnosis, clinical stage at diagnosis, and treatment were also observed, all of which contributed to a higher survival rate of Singaporean patients (49). Comparisons among countries. Because of limitations of organized databases in DCs, studies on this subject are also limited. In Brazil, comparing a hospital records series ’ DISCUSSION with Surveillance, Epidemiology and End Results (SEER) data, Brazilian patients were younger, demonstrated a longer This study is a literature review that describes potential medical history, presented with larger tumors and were less indicators related to the diagnosis of breast cancer in develop- likely to have clinical stage I disease (10.2% x 50.1%), which ing countries. Based on this study type, we opted to use the were all reflected by the lower overall survival rate of 19.6 methodology of systematic reviews, using PRISMA and percentage points and a cancer specific survival of 26.9 per- PICOTS, to evaluate possible ways that the health systems centage points. This effect almost disappeared when compar- in DCs can be assessed. It was not possible to perform a meta- ing overall survival by stage [Figure 3 (62)], which suggests analysis with odds ratios and forest plots because a meta- that the difference may have been due to the excessive num- analysis requires case-control or randomized studies, which ber of patients diagnosed at the early stage in the US (46). are not often published in DCs. Because we found observa- tional studies, prevalence studies and prevalence review Outcome/Survival. Despite the lower incidence rates, articles, we opted to perform an integrative systematic review. 45% of worldwide breast cancer cases and 54% of deaths due The studies were summarized by topic according to the to breast cancer worldwide occur in DCs (63). The mortality/ PRISMA criteria for selection. We identified potential indica- incidence ratio reflects the structure of these countries better tors (Table 1) that can be used to compare differences and to than simple numeric mortality data, and this ratio exceeds evaluate improvement in public health systems. Figure 3 - Survival according to the SEER study (blue) and a Brazilian Oncologic Hospital (HCB, green). (a) Overall survival (OS); (b) cancer- specific survival (SS); (c) overall survival selected by clinical stage (CS) at diagnosis. Unpublished Figure (ref 62) authorized by the Authors. 248 CLINICS 2017;72(4):244-253 Screening in developing countries da Costa Vieira RA et al. BSEs and CBEs have long been considered to be important Currently, many studies arguing against and in favor of methodologies to be implemented at the population level. mammographic screening are available. Decreases in the size However, scientific evidence regarding the effectiveness of of diagnosed lesions, decreases in breast cancer mortality, CBEs or BSEs in reducing mortality from breast cancer is longer lifespans, an acceptable overdiagnosis level (1-10%), currently lacking. Randomized studies carried out in China and the frequency of carcinoma in situ all support the use of (68) and Russia (69) have led to a loss in support for BSEs as mammographic screening (12, 75, 80). Conversely, partial an early detection method because the breast cancer mor- evaluations of systematic reviews (80), discussions about the tality rates did not differ between women who performed actual decline in advanced stage tumors in the US (81), and BSEs and those who did not. In this context, women are the rate of overdiagnosis (31%) (81) do not support the use of encouraged to be alert to any changes in the breast, and CBEs mammographic screening. Moreover, although some studies are part of this awareness and may lead the woman to a show that lives are indeed saved by mammographic screen- diagnostic evaluation. According to the Brazilian Society for ing, the number of survivors is low (82, 83). In general, stu- Mastology, BSEs/CBEs in isolation are not encouraged but dies of doctors who see patients support the use of screening are always associated with the use of mammography, espe- (75, 77), whereas studies performed by epidemiologists argue cially in women over 40. againstthis typeofscreening(81),and suggestthatwomen The sensitivity of breast self-examination (BSE) is low (20 should be well informed regarding mammographic screening to 30%), and it is not associated with a decrease in mortality. and aware of the pros and cons (82, 83). This fact is especially Mammography has a sensitivity of 63 to 95% (37), and it relevant in developed countries, where high income and educa- is the only exam that has been demonstrated to be related tion levels characterize much of the population. to a decrease in mortality. Its sensitivity increases with the In countries with extremely limited public health resources, presence of palpable lumps and decreases in dense breasts. infectious diseases are the main public health problem. The Approximately 10%-30% of breast cancers are not detected extent to which these diseases are controlled to increase life by mammography because of many possible factors such as expectancy changes disease profiles. The age distribution of dense parenchyma, obscure lesions, poor positioning, per- the population affects the incidence of cancer, with a decrease ception error, incorrect interpretations, subtype tumors, slow in age at diagnosis being observed in some countries (37). In growing tumors, the presence of interval carcinomas and DCs, most of the population earns a low income. Therefore, smaller-sized tumors (70). Based on these factors, the woman healthcare usually depends on government actions and public must perform a regular evaluation by BSE and/or undergo health infrastructure. Healthcare provision is related to the a clinical breast evaluation by a healthcare professional. Together, availability of resources, and many diseases compete for these these exams must be considered in the diagnostic evaluation in resources. Public health practices are linked to national guide- addition to a breast ultrasound insymptomatic women(71). lines and available methodologies, which are associated with Breast cancer screening by mammography is the best public education processes and the availability of public net- secondary prevention methodology for the population; it work demand absorbency. Therefore, not only tumor-related serves as a disease intervention measure and promotes early or epidemiological criteria but also account resource avail- detection in the asymptomatic phase. Specifically, screening ability are important when evaluating the age range for substantially reduces the morbidity and mortality due to late screening strategies because data in DCs are generally limited diagnosis. The HIP study (Health Insurance Plan) was the and rely on studies conducted in developed countries. Thus, first to demonstrate a reduction in breast cancer mortality strategies are lacking, and BSEs are used as a screening (30%) as a result of mammographic screening. In the 2006 strategy, whereas ultrasound is used as a diagnostic strategy. and 2009 Cochrane reviews, the reduction was approxi- In DCs, mammograms are not performed primarily because mately 15%. In the last review (2013), which only evaluated of barriers in the healthcare system, which are affected by the randomized studies, they did not observe a reduction in following: the accessibility of health services, unsatisfactory mortality, but a reduction on the order of 25% was found medical adherence due to public healthcare system limitations, when observational studies were included; and when group- the cost of tests, and difficulty in implementing follow-up ing all studies together, this reduction was 19% (72). The tests (5, 84). The evaluation of factors relating to the health- greater likelihood of reducing breast cancer mortality in care system and non-adherence to mammogram screening several developed countries can be attributed to screening guidelines is complex because such evaluations lack a specific programs and the evolution of adjunct therapy (73), (74). indicator. The cultural context is interwoven with the infrastruc- More recent studies have questioned these figures, arguing ture, the limitation of trained personnel, and the effective that this reduction is on the order of 8%, but these studies stratification of examinations up to the point of diagnosis, were conducted in developed countries and many metho- which should be quick, comprehensive, and effective. Never- dological problems were questioned (75). theless, this effect can be assessed by evaluating mammo- Screening primarily reduces mortality in women between graphy available to the public, population coverage, and the 50 and 69-74 years of age, with less dramatic results in percentage of mammography exams performed. In this con- women who are 40-49 years of age. Thus, mammography text, access to mammography refers to the presence of this should be performed on a large scale at the population level technology, the ease of the general population’saccess toit, the for this age group to reduce breast cancer mortality. The quality of the tests performed, and the possibility of perfor- Brazilian Society of Mastology suggests that the starting ming additional tests focused on biopsy and differential age should be 40 years (76), which was also suggested by diagnosis. Logistical and technological limitations delay tests the American Cancer Society until 2015 (77). In 2016, this prior to diagnosis, result in low population coverage, and gene- suggestion was changed to age 45 (78). EUSOMA (12), the rally limit access to regular mammograms. DCs report difficul- US Preventive Services Task Force (79) and the Brazilian ties with respect to mammography screening in women, while Ministry of Health (42) suggest that organized population developed countries discuss the practice of mammography for screening commence at age 50. specific ages, as 57.2% of the women aged 50 to 74 in the 249 Screening in developing countries CLINICS 2017;72(4):244-253 da Costa Vieira RA et al. US (85) undergo regular mammography. In addition, the stage II (4.7 pp at 5-years and 6.6 pp at 10-years; p=0.001) qualities of breast cancer screening methods and accreditation disease. However, these differences were associated with the programs are reported in developed countries (12, 86, 87). This quality of mortality data, the loss of follow-up information, fact reflects the clinical stage at diagnosis, as early clinical stage as well as differences in treatment protocols and molecular disease (EC 0 and I) represents 5% of all tumors in India (17) subtypes, which renders it difficult to make comparisons and 50.9% in Europe (86). In DCs, tumors are usually palpable, among countries (62). large, and not at an early clinical stage at the time of diagnosis If we consider that mammographic screening and early (Figure 2). Conversely, tumors diagnosed only by mammogra- diagnosis are not related to an increase in the survival, as phy are infrequent, and the incidence of carcinoma in situ is shown in some randomized studies, we must not forget that low. For example, carcinoma in situ varies and was 0.1% in these studies were performed in developed countries, where African registries, 1% in India, 11.4% in Europe, 16% in North favorable conditions are present for diagnosis and treatment. America and approximately 4.5%inother regionsofthe world In reality, the opposite conditions are present in DCs, a fact (9, 17, 86). that reflects the lower rate of early diagnosis and poor sur- Although tumors smaller than 2 cm can be detected by vival. It is therefore important to have a progressive structur- clinical examination, they must be superficial, and the great ing of public health systems. To evaluate this condition, we majority of these tumors that are detected by mammography found possible indicators that can be reported and that can be are smaller than 2 cm (88). Technology is associated with a used in future studies performed in DCs (Table 1). local infrastructure and is based on mammograms, ultra- The identification of subpopulations or analysis based on sound, biopsy (open or core biopsy) and pathology. This socioeconomic conditions helps to understand the context reflects the lower percentage of early breast cancers detected of a population that is more dependent on the public health- in DCs. The HDI shows the association of PIB per capita and care system. Similarly, the observation of temporal data the life expectancy, which may indirectly reflect the health allows us to evaluate progress relating to the structuring of system. People have a socioeconomic dependence on public the public healthcare system. Limitations in diagnosis and health systems, and therefore, the public health system is treatment lead to a high mortality/incidence ratio (74); speci- not a choice but may be the only option for many women. To fically, diagnosis is delayed, and many treatments are not evaluate the clinical stage at diagnosis, the TNM staging performed based on protocols (20). system is a standard and acceptable approach. We observed When using the PICOTS methodology for diagnostic tests different frequencies of stages based on clinical stage 0 to IV (11), the Timing (T) and Setting (S) are observed, but studies (five categories) or clinical stage I to IV (four categories). The of these factors were not available. Therefore, we present evaluation of the percentage of cases at clinical stage 0 would general aspects (PICO; Table 1). Some review articles on the be based primarily on mammography-detected tumors, but subject were included in the overall review, but they were these data were not reported in all the included studies. If we not selected in the 45 articles that determined the indicators use the four categories listed above, we must pay attention because they do not show potential indicators. to clinical stage I. Tumors larger than 2 cm are frequently Two aspects should be emphasized in this study. In the palpable and clinically detectable. Based on this observation, initial evaluation, the search was conducted using keywords we generated Figure 2 and chose data from clinical stage I to that are associated with case-control studies. This search IV, as data related to clinical stage 0 were insufficient. We revealed 4 publications, but none of these publications observed a linear relationship of the HDI and clinical stage, included possible indicators, which led us to review gene- as a high HDI was associated with a higher rate of clinical ral articles to identify possible indicators. Furthermore, the stage I, while a lower HDI was associated with lower clinical separation between DCs and underdeveloped countries stage I (Figure 2). presented another problem. The literature evaluated lacks a In terms of survival, patients with early-stage disease clear separation between the two, despite the possibility of exhibit excellent survival rates, whereas patients with meta- using World Bank classifications (90). Therefore, underdevel- stasis at the time of diagnosis have limited survival. Dif- oped countries could not be excluded from the evaluation. ferences in survival are primarily due to differences in Limitations of the present study include the following: clinical stage at the time of diagnosis and the ability to only 1 database was used; the evaluation of articles was provide adjunct therapy at the population level, which is not based on the level of evidence but rather on available reflected in the 5-year survival rates in different countries data, which we attempted to systematically evaluate; and (89). The CONCORD study evaluated population-based comparisons of all indicators in developed countries were cancer registries from 2005-2009 and estimated the 5-year not reported. The objective was to identify potential indi- survival rate after observing lower survival rates in South cators identified by a systematic methodology. Consequently, Africa (53%), Mongolia (57%), India (60%) and higher indirect indicators that can be used in DCs were identified, survival rates in North America and Oceania (84-89%). which elucidated the conditions relating to breast cancer Its study showed that differences in the 5-year cancer diagnosis in DCs. The systematic identification and descrip- specific-survival were dependent on the country (9). After tion of these indicators will facilitate comparisons among a comparison of the SEER database with an institutional countries, the evaluation of public services, and the evalua- Brazilian database adjusted by the same characteristics, a tion of outcomes of the progressive structuring of healthcare similar 10-year global survival rate was observed according systems. to clinical stage, which reminds us to consider the influence Currently, the validity of mammographic screening and of the percentage of early clinical stage cases on the overall mammography is under discussion, but such discussions are survival, and the importance of long-term follow-up. In this carried out in countries with structured healthcare systems publication, the cancer-specific survival was not discussed, that allow for diagnosis and treatment, irrespective of who and differences were observed in patients with clinical stage I absorbs the costs of this process. A better understanding of the (3.6 at 5-years and 13.0% at 10-years; p=0.001) and clinical alternate reality, that is, comparisons between limited public 250 CLINICS 2017;72(4):244-253 Screening in developing countries da Costa Vieira RA et al. healthcare systems in terms of technology or access to mam- 13. Mehdi I, Monem EA, Al Bahrani BJ, Al Kharusi S, Nada AM, Al Lawati J, et al. Age at diagnosis of female breast cancer in Oman: Issues and mography, will enable us to better understand the benefits of implications. South Asian J Cancer. 2014;3(2):101-6, http://dx.doi.org/ this diagnostic modality and mammographic screening. 10.4103/2278-330X.130442. Mammographic screening is proved to be beneficial when 14. Youlden DR, Cramb SM, Yip CH, Baade PD. Incidence and mortality of female breast cancer in the Asia-Pacific region. Cancer Biol Med. 2014; it is performed in an organized and regular manner in the 11(2):101-15. form of a national public health policy or when the per capita 15. 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World J Surg. 2007;31(5):1031-40, http:// mographic screening may be more beneficial in DCs than dx.doi.org/10.1007/s00268-005-0585-9. what is observed in developed countries. This structuring 18. Robles SC, Galanis E. Breast cancer in Latin America and the Caribbean. Rev Panam Salud Publica. 2002;11(3):178-85, http://dx.doi.org/10.1590/ can be evaluated using indicators relating to diagnostic qua- S1020-49892002000300007. lity or methodology, and this study identified these indi- 19. Aro AR, de Koning HJ, Absetz P, Schreck M. Two distinct groups of cators. These indicators will facilitate the evaluation of the non-attenders in an organized mammography screening program. Breast Cancer Res Treat. 2001;70(2):145-53, http://dx.doi.org/10.1023/A:1012 improvement in health systems related to breast cancer and will allow comparisons among countries. This will provide 20. Agarwal G, Ramakant P. Breast Cancer Care in India: The Current Sce- us with a better understanding of the real impact of mam- nario and the Challenges for the Future. Breast Care. 2008;3(1):21-7, http://dx.doi.org/10.1159/000115288. mographic screening in DCs. 21. Obaji N, Elom H, Agwu U, Nwigwe C, Ezeonu P, Umeora O. Awareness and Practice of Breast Self-Examination among Market Women in Aba- kaliki, South East Nigeria. Ann Med Health Sci Res. 2013;3(1):7-12, ’ AUTHOR CONTRIBUTIONS http://dx.doi.org/10.4103/2141-9248.109457. 22. Al-Sharbatti SS, Shaikh RB, Mathew E, Salman Al-Biate MA. Breast self Vieira RA participated in the study design, article selection, data analysis examination practice and breast cancer risk perception among female and writing of the manuscript. Biller G participated in the article selection university students in Ajman. Asian Pac J Cancer Prev. 2013;14(8):4919-23, and data analysis. Uemura G participated in the data analysis and dis- http://dx.doi.org/10.7314/APJCP.2013.14.8.4919. cussion. Ruiz CA participated in the data analysis and discussion. Curado 23. Amoran OE, Toyobo OO. Predictors of breast self-examination as cancer MP participated in the study design and discussion. All authors read and prevention practice among women of reproductive age-group in a rural town in Nigeria. Niger Med J. 2015;56(3):185-9, http://dx.doi.org/ approved the final written version of the manuscript. 10.4103/0300-1652.160362. 24. Knaul FM, Nigenda G, Lozano R, Arreola-Ornelas H, Langer A, Frenk J. Breast cancer in Mexico: a pressing priority. Reprod Health Matters. ’ REFERENCES 2008;16(32):113-23, http://dx.doi.org/10.1016/S0968-8080(08)32414-8. 25. Chahine G, El Rassy E, Khazzaka A, Saleh K, Rassy N, Khalife N, et al. 1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. 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