ANTICANCER RESEARCH 34: 5057-5066 (2014)

Implementation of a Clinical Quality Control Program in a Mammography Screening Service of

SILVIA MARIA PRIOLI DE SOUZA SABINO1, THIAGO BUOSI SILVA1, ANAPAULA HIDEMI UEMA WATANABE1, KARI SYRJÄNEN2,3, ANDRÉ LOPES CARVALHO2 and EDMUNDO CARVALHO MAUAD1

1Department of Cancer Prevention, Barretos Cancer Hospital, Barretos, Brazil; 2Teaching and Research Institute, Barretos Cancer Hospital, Barretos, Brazil; 3Department of Oncology & Radiotherapy, Turku University Hospital, Turku, Finland

Abstract. Aim: To evaluate the effect of a clinical quality detection remains one of the cornerstones in the fight against control program on the final quality of a mammography breast cancer mortality (3). The quality of mammography is screening service. Materials and Methods: We conducted directly related to the capacity for detecting an abnormality. retrospective assessment of the clinical quality of 5,000 While screening mammography without adequate quality mammograms taken in a Mammography Screening Program control reaches a sensitivity of 66%, an adequately controlled between November 2010 and September 2011, following the screening mammography has sensitivity up to 85-90% (4, 5). implementation of a Clinical Quality Control Program based Optimal quality of the mammography image is essential on the European Guidelines. Results: Among the 105,000 for successful diagnosis of breast cancer (6, 7). This includes evaluated quality items, there were 8,588 failures (8.2%) - 1.7 both the (i) technical criteria associated with the assessment failures per examination. Altogether, 89% of the failures were of the mammography and workstations through well- associated with positioning. The recall rate due to a technical established periodic tests (8), and (ii) clinical criteria error reached a maximum of 0.5% in the early phase of the involving the review of the produced films, mammographic observation period and subsequently stabilized (0.09%). compression, exposure, artifacts and image definition (5, 6, Conclusion: The ongoing education and monitoring combined 8, 9), all affecting the accuracy of mammography (5, 6). with personalized training increased the critical thinking of Thus, correct positioning as well as physical and technical the involved professionals, reducing the technical failures and parameters, like adequate contrast, are absolutely necessary unnecessary exposure of patients to radiation, with to obtain high-quality mammographic images. In substantial improvement in the final quality of mammography. consequence, the radiography technician must follow the positioning standards to maximize the amount of tissue Breast cancer remains the leading cause of cancer mortality covered by the image (10). among women worldwide (1), with the highest incidence in The evaluation of the clinical criteria of mammography developed countries. However, mortality rates in developing image quality is controversial and subjective, being hampered countries also show an increased trend due to a lack of by variations in the individual perception of the observers (11). resources for implementation of organized screening As an attempt to develop a rigorous standardized system, programs, accurate diagnosis and effective treatment (2). several models have been proposed, including the American Mammography is the only radiological examination that College of Radiology (ACR) (12) and the European allows for systematic detection of breast cancer, as early Commission (European Guidelines) (13). According to the World Health Organization (WHO), developing countries display an array of difficulties when it comes to access radiological services like large gaps in image quality and also Correspondence to: Silvia Maria Prioli de Souza , MD, MSc, deficiencies in radiological services (14). In 2006, the Department of Cancer Prevention, Barretos Cancer Hospital, Brazilian press reported that 60% of the mammographic Barretos, Brazil, Rua Antenor Duarte Villela, 1331 - Bairro Dr. examinations conducted by the National Cancer Institute of Paulo Prata, Barretos, SP, 14784-400, Brazil. Tel/Fax: +55 1733216600 (ext. 7051), e-mail: [email protected] Brazil (INCA) (including public health systems and private clinics) exhibited some degree of failures, such as errors in the Key Words: Breast cancer, mammography, quality control, screening radiation dosage, equipment calibration, positioning of the programs, in-service training, mobile units. patients and image interpretation (15).

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With desire to improve the quality of the services and Table I. The use of digital and analog mammography equipment in the expertise based on the European model of population-based mammography screening of Barretos Cancer Hospital, Fundação Pio organized screening, the Barretos Cancer Hospital acquired XII. knowledge about European screening and especially the City (State) Unit type Number Equipment technology quality assurance program and training of its screening professionals. These experiences encouraged us to start in Barretos (SP) Fixed 3 Digital 2009 a clinical quality control program of their screening Mobile (MU2) 1 Analog mammography based on the European Guidelines. Mobile (MU5) 1 Analog (SP) Fixed 1 Digital The aim of this study was to evaluate the quality of the Fixed 1 Digitalized Analog (CR) mammographic images produced in one mammographic Mobile (MU4) 2 Analog screening service, during the implementation of a clinical Araçatuba (SP) Mobile (MU6) 2 Digital quality control program. Juazeiro (BA) Fixed 1 Analog Mobile 1 Analog

Materials and Methods Where: BA=Bahia State; CR=computed radiography; MU=Mobile Unit; SP= State. Materials. We conducted an observational study based on retrospective data collection on the clinical quality of mammograms performed in a Mammography Screening Program at the Pio XII Foundation - Barretos Cancer Hospital between 2010 and 2011. The clinical quality of the mammogram was evaluated using nominal study sample comprised a series of 5,000 mammograms performed qualitative variables according to the standardization of the by the same group of radiology technicians during implementation of European Guidelines (13), and divided into two categories: (i) the Clinical Quality Control Program. Excluded from the study were failures associated with positioning or (ii) failures associated with all tests performed for women with very large breasts, those who the equipment. The collected data were compiled into a database underwent breast-conserving surgery or mastectomy, as well as the developed within the computer system of the Barretos Cancer images with limitations in the evaluation of the proposed indicators. Hospital. The evaluation was subdivided into items associated with The authors ensure that this study was been carried out in cranio-caudal and medio-lateral oblique views and, in the equipment accordance with The Code of Ethics of the World Medical category, the evaluated items included those associated with the Association (Declaration of Helsinki) for experiments involving performer equipment that could interfere with the final quality of humans. This project was evaluated by the Ethics Committee in mammography in both views (Table II). Research of the Barretos Cancer Hospital and assessment was Each item was categorized as "conformity" or "non-conformity", approved under protocol number 573/2012. based on the two views in both lateral sides. Only the items in “non- conformity” were annotated using this software. The quality control Methods. The target group undergoing re-education since November program identified the unit that performed the examination, the 2010 comprised of 33 radiography technicians who performed radiology technician responsible and the committed failures. mammographies for women participating in the Mammography Therefore, it was possible to distinguish the types of non- Screening Program at the Pio XII Foundation - Barretos Cancer conformities (technical or equipment) in each work unit, associated Hospital. with each type of equipment, analog, digitized analog or digital. The Clinical Quality Control Program was supervised by a The analysis of the number of errors was performed monthly. multidisciplinary team comprising (i) a radiologist specialized in Based on the chart of the statistical process control (software R mammography, responsible for assessing the clinical quality control version 2.15.2, Link or Supplier) (18), which influences the items, (ii) a physicist dedicated to technical quality control, (iii) individual performance relative to the group average in the period. three technical supervisors of the practical training (to specifically The radiology technicians showing average failures above individual correct the failures of the technical group) and (iv) a statistician. limits, calculated in proportion to the volume of the tests analyzed, All radiology technicians involved in the program received were summoned to new training (Figure 1). theoretical and practical training in mammography and executed The failure types of the radiology technicians necessitating to their activities in 3 fixed units and 5 mobile units (MU) equipped repeat training were identified and personalized, and targeted with 13 mammography systems (6 digital and 7 analog systems) corrective actions were employed in specific practical trainings with (Table I). Approximately 20% of the production from each unit was technical supervisors. The training lasted an average duration of 15 sampled daily through systematic random sampling. This value was hours and the physician in charge monitored the production. After defined as the sample size calculation based on the volume of the correction of the presented failures, the radiology technicians were production of each unit (16). authorized to continue their work. The X-ray films from the analog units were forwarded and The radiology technicians from the units of the Pio XII immediately assessed, while the digital exams were assessed using Foundation - Barretos Cancer Hospital received individualized an archiving and image distribution system - PACS (Picture assessments of their non-compliance and development during the Archiving and Communication System) (17), within 24 hours after period, a continuing education program and a monthly recycling in completion. After identification of the pattern of the breast the fixed unit of Barretos was offered. When necessary, corrective composition, i.e., the proportion of fibroglandular tissue in relation intervention was performed through the dedicated physician in the to fat tissue, according to the BI-RADS™ classification (12), the mobile units; thus, any problems in these units were resolved in the

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Figure 1. The control chart demonstrating technical performance of the radiology technicians related to the volume and compared to the group in the same period. The average failures of each technician are represented by a dot. The dotted line depicts how much each technician will fail and still maintain a technical performance within the acceptable range. The points above the dotted line indicate the radiology technicians whose performance was outside the accepted range and who were referred for further training.

Table II. Types of positioning-related failures and performer-technical failures assessed by the Clinical Quality Control Program (according to European Guidelines).

Category View Evaluated item

Positioning Cranio-caudal Nipple in profile and centered Lateral and medial portions of breasts correctly shown Presence of the pectoral muscle Absence of skin folds Symmetry Medio-lateral oblique Nipple in profile and parallel to the film All the breast tissue clearly shown Pectoral muscle to nipple level Pectoral muscle relaxed Absence of skin folds and axilla Absence of minor pectoral muscle Visualization of infra-mammary angle Symmetry Equipment Cranio-caudal and Definition Medio-lateral oblique Optical density Contrast Noise Artifacts Identification

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Figure 2. The distribution of the failures according to failure type and mammography unit.

Table III. Frequency of equipment failures by the type of equipment.

Failure Analog Equipment Digitized analog equipment Digital Equipment p-Value n (%) n (%) n (%)

Optical Density 128 (15.3%) 3 (9.7%) 5 (11.9%) <0.01 Definition 9 (1.1%) 21 (67.7%) 27 (64.3%) 0.1 Contrast 33 (3.9%) 2 (6.4%) 0 (0%) <0.01 Noise 0 (0%) 2 (6.4%) 9 (21.4%) <0.01 Artifact 668 (79.6%) 3 (9.7%) 1 (2.4%) <0.01

Total 839 (100%) 31 (100%) 42 (100%)

shortest possible time. During the study period, the rates of repeated In total, 2,851 results were obtained from the digital exams examinations and recalls due to a technical error (12, 13, 19) of the (57.02%), 1,968 results were derived from analog exams of units were recorded. This study was conducted using a single expert the radiographic films (39.36%) and the remaining 181 results observer to avoid bias due to inter-observer variation, inherent to represented digitized analog exams (3.62%). the subjectivity of the clinical quality assessment. In the overall evaluation of the 5,000 mammograms, 1,119 Statistical analyses. The data were subjected to exploratory analysis (22.3%) results were in conformity, 2,545 (51%) results had through descriptive statistics, using mean, absolute and percentage less than two failures, while 1,336 (26.7%) showed three to frequencies, and graphs. nine failures. Altogether, 8,588 (8.2%) failures were identified, with an average of 1.69 failures per examination. Results Out of all failures, 7,676 (89%) were associated with the positioning of the breast during the examination and 912 Altogether, from the 5,000 consecutive mammograms (11%) failures were associated with the equipment. Fixed submitted to clinical quality control program between units of Barretos, as well as MU2 and MU5 exhibited the November 2010 and September 2011, 105,000 quality items lowest average failure rate associated with positioning, were evaluated, related to both the positioning and equipment. ranging between 1.2 and 1.4 failures/exam, whereas the fixed

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Figure 3. Distribution of positioning-related failures.

units of Barretos, fixed units of Jales with digital equipment Failures in breast positioning. Among the 7,676 non- (fixed Jales D) and MU6 exhibited the lowest equipment- conformities associated with breast positioning during related failures, ranging between 0 and 0.03 failures/exam. mammography, 3,316 (43%) were observed in the cranio- The highest rate of failures in both positioning (between 2.6 caudal view and 4,356 (57%) were found in the medio-lateral and 3 failures/exam) and the equipment (between 0.6 and 0.9 oblique view. The absence of major pectoral muscle in the failures/exam) were observed at the units of Juazeiro, Bahia. cranio-caudal view was the single most frequent failure, The distribution of the failure types by the mammography representing 2,547 (33%) of the errors. The second most units is shown in Figure 2. frequent error was the lack of adequate opening of the infra- mammary angle, with 1,846 (24%) non-conformities, followed Technical failures. The 912 non-conformities associated with by incorrect positioning of the breast above the nipple line the equipment failure were analyzed in more detail and 673 (14.2 %) (Figure 3). (69.9%) of those were attributed to the presence of artifacts Also the correct positioning of each evaluated item was in the image, followed by 137 (15%) variations in optical recorded. The major pectoral muscle was sampled correctly density, 58 (6.4%) losses in definition, 37 (4.1%) losses in in cranio-caudal view in 49.2% of the patients; it was contrast, 31 (3.4%) mis-identifications and 12 (1.3%) properly positioned on the nipple line in 78.2% of the indications of image noise. Evaluation of these non- examinations, while the infra-mammary angle was correctly conformities according to the type of equipment revealed a viewed in 63.1% of the mammograms (Table IV). The predominance of the failures in analog equipment, with 839 average number of non-conformities for each radiology (93%) non-conformities. The digitized analog equipment technician was cyclic during the study period, showing bi- (CR) and digital analysis registered only 4% and 3% failures, monthly or quarterly peaks, while the variation of the respectively. Correlation of the type of failure with the overall group failures leveled off along with the realized equipment determined, using the Kruskal-Wallis test, showed examinations. the highest prevalence of failures for artifacts in analog equipment (79.6%), definition problems in digitized analog Repetition and recall rates. The repetition rate of the (67.7%) and digital (64.3%) equipment (Table III). examinations increased from 1.6% to 6.6% between

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Figure 4. Monthly variation in the repetition rates.

Table IV. Success rate related to mammographic positioning.

View Evaluated item Adequately done (%)

Cranio-caudal Nipple in profile and centered 98.5 Lateral and medial portions of breasts rightly shown 96.2 Presence of the pectoral muscle 49.2 Absence of skin folds 97.2 Symmetry 97.0 Medio-lateral oblique Nipple in profile and parallel to the film 98.2 All the breast tissue clearly shown 99.8 Pectoral muscle to nipple level 78.2 Pectoral muscle relaxed 90.1 Absence of skin folds and axilla 95.4 Absence of minor pectoral muscle 96.6 Visualization of infra-mammary angle 63.1 Symmetry 98.4 Identification 98.5

November 2010 and February 2011, with a decline in Discussion subsequent months, stabilizing between 3 and 4%, as shown in Figure 4. The recall rates due to a technical error ranged Potential causes of false negative mammographies include (i) from 0.05% to 0.3%, showing a decline of 0.47% between dense parenchyma obscuring the lesion, (ii) subtle features of November 2010 and February 2011 (i.e., a decrease from malignancy, (iii) slow growth of the lesion, (iv) perception 0.5% to 0.03%), and stabilizing at an average level of 0.09% error, (v) incorrect interpretation of a suspect finding and (vi) (Figure 5). failing of positioning or examination technique (20). An

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Figure 5. Monthly variation in the recall rates due to technical error.

adequate quality of mammography is essential for the accurate professionals to improve the quality of radiography (14). A diagnosis of breast cancer (4, 5). However, controlling the major problem in developing countries, however, is the quality of mammography is a greater challenge than in any qualification of all the professionals involved in organized other field of radiology (9) which makes it imperative to adopt radiological services. a continuous and rigorous quality-monitoring process in all Resources for education and training are important for mammographic screening programs. implementation and sustainability of a radiological service, INCA (Brazil) in association with the Brazilian College of which can be used to educate local health care providers to Radiology (CBR) and the National Agency for Sanitary improve the quality of the service (24). Furthermore, Surveillance (ANVISA), with 53 services of the Unified specialized and qualified labor requires time and financial Health System (SUS) conducted a pilot study on quality investment. The training of Brazilian radiology technicians for control in mammography between 2007 and 2008 (21). It the performance of mammography is conducted as a part of was disclosed that the quality of 30% of the mammographic generalist training which includes 18 months of a technical examinations was below the satisfactory standards, with an course without qualification specific to mammography, as index three-times higher than the percentage of failures compared with the 4 years required to graduate with accepted by WHO guidelines (21). Despite its extreme mammography specialization in many of the developed importance, the quality certification of the mammography countries. This inadequate training of radiology technicians is services by the Brazilian College of Radiology and well-illustrated by the results of an audit (in 2009) by an Diagnostic Imaging (CBR), in which the examinations and independent European organization, emphasizing that the first medical reports are subjected to a rigorous evaluation, was thing to be tackled is the high number of recalls due to not mandatory and is currently available in only 5.7% (183) technical and positioning problems. of the 3,200 mammography services available in Brazil (22). To minimize the impact of the deficient technical training The availability of good-quality radiological services on mammography quality, a multi-disciplinary team worldwide is worrying, particularly in low- and middle- comprising of radiologists, physicists and radiology income countries (LMC). According to WHO, 3.5 to 4.7 technicians should be integrated to address the technical and billion individuals worldwide have difficulties to access the clinical criteria of the examination. This team should radiology services due the lack of progress in LMCs (23). immediately act in the resolution of failures with corrective The medical imaging services in these countries continue actions on equipment and plan systematic activities that facing several difficulties, most importantly the lack of promote continuous quality control through personnel resources to structure the services and a weak or inexistent training, equipment renewal and monitoring the quality of infrastructure for training and education of the different the units over time for the maintenance of the established

5063 ANTICANCER RESEARCH 34: 5057-5066 (2014) standards and the participation of the units in national maintenance of the cassettes, intensifying screens and programs of accreditation. Similar actions are taken in processors, inherent to analog technology. The technical non- developed countries, such as the Netherlands (25) and Japan conformities represented 11% of the observed failures, (26), which have training centers and mammography quality primarily reflecting the use of analog mammographic monitoring. Typically, the technical team or radiologist, who equipment (93%), such as presence of artifacts in the image is inadequately-trained for this purpose, intuitively assesses and changes in optical density. the clinical quality of the mammography, and preventive and The learning curve of the radiology technicians was corrective actions are not generally endorsed. Thus, it is demonstrated through the analysis of the variations in necessary to develop programs in which the criteria repetition and recall rates due to technical errors. During the associated with the final quality of the mammogram first quarter after implementation of the program, a significant produced are systematically analyzed to support the practical increase in the repetition rates of the radiology technicians training for radiology technicians. (without request by the radiologist) was observed, indicating During this study, the analysis of the sample control charts an arousal of a critical sense of the technical team concerning disclosed the need for additional training only for technicians the quality items associated with positioning and equipment. who committed an average of 2 or more failures per test. In addition, there was a substantial reduction in the number of Thus, according to these criteria, the majority of the recalls by the radiologists due to technical errors that were evaluated examinations (73%) did not prompt the not previously observed because these failures were corrected radiographer for training. In this study, the mammography during the examination. In the subsequent months, a decrease units exhibited significant changes in their average number in the repetition rates was observed, associated with the of non-conformities. The units located more distant from the stabilization of the exam quality i.e., the quality standard was headquarters of the program and from the practical training achieved in the first image acquisitions not requiring unit exhibited nearly three-times more failures than the other repositioning for correctness. At this stage, the repetition rate units. These data suggest that the proximity to the training reached the levels acceptable by the European Guidelines center is important to provide more effective correction of (13). Moreover, the rates of recall for technical error remained the failures, likely reflecting the daily opportunities to low, reaching the averages acceptable by the European communicate with those responsible for the program as well Guidelines (13). as the possibility to participate in monthly practical training These results were achieved through careful monitoring, with technical supervisors, which is offered only sporadically continuous training and constant personalized technical for the more remote units. training, because the technical performance of individual Most of the recorded failures were associated with the technicians oscillated over time, with the failures peaking positioning of the breast for examination, which is consistent happening again almost bi-monthly or quarterly. However, with the published literature (5, 9, 27). Positioning failures are stabilization occurred in the continuous training group, with operator-dependent and closely associated with the occurrence the failures of a radiology technician being compensated of interval cancers (5). The cranio-caudal view showed the through the hit of another technician and, consequently, the highest number of positioning-related non-conformities (with suitability of the overall service quality. a number of items evaluated), of which the main item, i.e., sampling of the major pectoral muscle, was adequately Conclusion performed 20% more often than reported by Cardeñosa (28) and 50% more often than in the study of Bassett (29). With the apparent increase in breast cancer cases also in the The breast density is an important variable in any evaluation developing countries, it is necessary to conduct studies to of the clinical quality of the picture, which potentially affects evaluate the quality of the mammography screening programs. the detection of lesions and reduces the sensitivity of The results presented in the present study demonstrate that mammography (5, 30, 31). The pattern of the breast density continuous education and monitoring associated with might also influence the perception of the image due to the personalized training promoted critical thinking of the reduction of the contrast associated with variations in exposure technicians, reducing the waste of resources and unnecessary and compression (27, 32). Further studies are required to exposure of the patients to radiation, with a consequent evaluate the potential association between the quality of improvement of the final quality of mammography services mammographic positioning and breast density. offered in a Breast Cancer Screening Program. The Artifacts were observed in 13% of the images, but most personalized education proposed in this study leads to high- of these errors had a characteristic, easily-detectable quality results similar to those constantly achieved in developed appearance. The units producing these failures were countries that could also be used as a managing tool for quality immediately notified for corrective measures. The low in mammography in different and in similar frequency of artifacts reflects the care associated with the developing countries.

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