- Email: [email protected]
Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis
Radiography xxx (2016) 1e6
Contents lists available at ScienceDirect
Radiography journal homepage: www.elsevier.com/locate/radi
Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis S. Moran a, b, *, H. Warren-Forward c a b c
BreastScreen NSW Hunter New England, Australia University of Newcastle, Australia Discipline of Medical Radiation Sciences, University of Newcastle, NSW, Australia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 24 October 2015 Received in revised form 20 February 2016 Accepted 26 February 2016 Available online xxx
Introduction: Globally, the role of the radiographer is changing; some countries have developed advanced roles with specific scopes of practice. Other countries, like Australia, are in the process of this change. This paper demonstrates the abilities of Australian radiographers in mammogram screen reading, highlighting some of their specific difficulties with different lesion types. Method: Six experienced radiographers participated in a prospective study, screen reading 2000 mammograms each between 2010 and 2011. This paper looks at the results of those same women at biennial re-screen. Analysis of the results included validation of normal results by negative follow-up screens and new cancers at biennial review; there is also analysis on the types of lesions detected and missed. Results: After biennial review, three cancers in 2013/2014 had been marked as abnormal by one radiographer two years prior, which increased her sensitivity from 64% to 85%. Sensitivity for the radiologists decreased from the assumed 100% to 95%. Radiographers appeared to be skilled in detection of calcifications and architectural distortions but had difficulty with non-specific densities. Conclusion: This study demonstrates the potential for Australian radiographers to enhance the accuracy of screen reading programs. Crown Copyright © 2016 Published by Elsevier Ltd on behalf of The College of Radiographers. All rights reserved.
Keywords: Radiographers Screen reading Accuracy Advanced practice Lesion type Tissue density
Introduction The Australian health care system has a high standard of care and quality of service, but it is struggling to meet the everincreasing demands of an ageing population.1 The increase in service demand will be dependent on a reduced health workforce, which will exacerbate the enormous pressure that some health workers are presently subject to; this in turn increases the risk of clinical error.1,2 In the radiography profession there are some areas where the skills of radiographers could be better utilised, and one of these areas is mammography. Screening programs historically have struggled with a shortage of radiologists3e5 and with radiographer recruitment and retention.1,2
* Corresponding author. 27 King St, Stockton, NSW 2295, Australia. Tel.: þ61 2 49201143, þ61 0427 201147 (mobile). E-mail address: [email protected] (S. Moran).
Other countries such as the USA and some European countries have established advanced practice roles with specific scopes of practice including mammography screen reading.6e8 A change in career structure was well received by the radiography profession in the UK; they have a four tier system incorporating radiographer assistants, radiographer practitioners, advanced practice radiographers and at the highest level, consultant radiographers.6 The Australian Inter-Professional Advisory Team (IPAT) released a document in 2012 which recommended that the Australian Institute of Radiography (AIR) create a framework for a status of Advanced Practitioner within the radiography profession.9 An advanced practitioner would be able to fulfil some of the duties normally undertaken by radiologists; this would also help alleviate the radiologist workload.6,10 In the field of screening mammography, some of the skills identified as possible advanced practice roles include mammogram screen reading and interventional techniques (biopsies and hookwire localisations).11 The scope of radiographers in the UK has widened over the last decade12 and
http://dx.doi.org/10.1016/j.radi.2016.02.007 1078-8174/Crown Copyright © 2016 Published by Elsevier Ltd on behalf of The College of Radiographers. All rights reserved.
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007
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radiographers in the UK now report and provide services independently from radiologists, providing high quality care through excellent clinical practice and leadership.13,14 With the AIR now poised to redesign the structure of professional radiography, Australian radiographers have shown that they are prepared to undertake further study to increase their knowledge, preferring to enhance their careers via clinical roles rather than managerial positions.15,16 Research into the capabilities of Australian mammography radiographers is ongoing, with four retrospective studies published within the last five years.17e20 The first Australian prospective study was completed in 2013, and has resulted in two papers; the first one reports on the performance results of six radiographers in a BreastScreen Australia (BSA) program, comparing their results with those of the radiologists.21 The cancers detected during the study were all biopsy-proven and women returned to screening at that time were assumed to be cancer-free. Follow-up was needed to measure whether any second round cancers had been indicated by the radiographers during the exercise. This paper presents the final results, after biennial follow-up and also investigates the types of lesions and breast tissue that was prevalent in the mammograms read and cancers missed by the radiographers. Methodology Ethics approval was provided by both the University of Newcastle and Hunter New England Area Health (HREC H-352-1206). Participants Six experienced radiographers participated in a prospective study, between 2010 and 2013. The radiographers were aged between 45 and 65 years and had worked in mammography for a minimum of 10 years. The radiographers read 2000 mammograms each, as this number is the annual minimum required for radiologists in BSA as detailed in Appendix P of the National Accreditation Standards (NAS).22 Most radiographers aimed to read a set amount per month (100e200) but this varied according to other commitments. All mammograms were read using a Sectra digital Picture Archiving System (PACS) with 10 megapixel Barco monitors. This equipment was in the normal screen reading area used by the radiologists, with appropriate lighting and viewing conditions. There were approximately 16 radiologists with a minimum of 10 years screen reading experience during this time, 6 of these also participated in assessment clinics. They read all mammograms available and at times that were convenient for them (usual practice), from local and remote sites. Further information on the method and resources used for this trial are detailed in a previous paper with the first stage results.21 The radiographers' results were compared to the combined radiologist outcome, as a reference standard to assess performance criteria. If a radiographer reported a lesion as ‘suspicious’ and it had not been recalled by the radiologists, it was referred to the designated radiologist for his opinion. This occurred twice. An author-developed in-house training package on image assessment23 had been made available to the radiographers between a pilot and full retrospective study, between 2007 and 200917,18; no formal training was provided.
outcomes of the women suggested ‘recall’ by the radiographer readers in 2010/2011. This was to determine whether the radiographers had detected any abnormality at that time which had not been recalled by the radiologists, but proved to be a cancer. There were 48 cancers detected in this group of women; all other negative 2010/2011 results were validated to be normal in 2013/2014 with the exception of three which are discussed in results. Difficulties of detection The images in this study included considerable variety of breast sizes, volumes and breast density; all these factors impact on the efficacy of, and level of difficulty associated with, screen reading accuracy.24,25 The lesions recalled also ranged from very subtle to very obvious, which meant that each radiographer's level of difficulty was different. This final stage analyses the different lesions and types of tissue within which those lesions were situated, ranging from mostly fatty to dense glandular tissue. The density of the breast tissue was subjectively viewed by the lead author, using guidance from the Breast Imaging Reporting Data System (BIRADS).26 Density of the tissue was categorised into one of four types: A. B. C. D.
Predominantly fatty Scattered fibro-glandular elements Heterogeneously dense Extremely dense
Lesions are classified into 6 categories using the Australian BreastScreen Information System (BIS):
Circumscribed mass with or without calcification Stellate lesion Architectural distortion Calcifications Non-specific density Other (may include skin lesions, lymph nodes)
Results In the first stage results, the number of mammograms assessed by individual radiographers varied slightly, depending on availability and a number of excluded images (technical recalls and symptomatic letters), resulting in 9348 individual mammograms. The majority (9197) of these women returned in 2013 (Fig. 1). There had been 61 women with cancers detected in 2011 so those women
Follow-up methodology Follow up on the 9348 women screened in 2010/2011 was conducted at rescreen between September 2012 and December 2013. In particular, the database was checked for all cancers detected. The principal researcher also checked the biennial
Figure 1. Follow up in 2013 of mammograms read in 2010/2011.
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007
S. Moran, H. Warren-Forward / Radiography xxx (2016) 1e6
did not return for a screen; they had surgery and treatment and were followed up more closely by specialist doctors. There were 90 women whose results could not be followed up in 2013; this was due to a variety of reasons, including withdrawal from the programme (20), women who did not respond to reminder letters for their rescreen (26) and women who did not get a reminder letter to return because they were out of the target age group (44).
Cancer detection
3
Table 1 Final summary of diagnostic accuracies.
T1 T2 T3 T4 T5 T6 All (median) Radiologists (median)
Cancer detection is the primary focus of all BreastScreen programmes. The cancers detected by radiographers ranged from 10/ 19 or 53% (T6) to 12/12 or 100% (T4) of cancers detected by the radiologists. These were all histology proven cancers, after recall assessment and biopsy. There were 48 (new) cancers detected in the women (n ¼ 9197) in 2013 (Fig. 1). Three of these cancers had been indicated as a recall for assessment by radiographer T3 in 2011. The cancers were detected in the same side and site that T3 had called. If these three cancers had been detected in 2011, the combined radiologist sensitivity would have reduced to 95% (Fig. 2). Radiographer T3 sensitivity would have increased from 64% to 85%, and radiographer T2 sensitivity would have dropped from 82% to 64% as she had returned to screening, two of those three women. None of the other radiographers had assessed these mammograms, and so there was no change in their sensitivities. The change in specificity was minimal, due to the very high number of non-cancers.
Sensitivity
Specificity
Accuracy
PPV
NPV
55% 64% 85% 100% 85% 53% 73% 95%
97% 91% 91% 95% 98% 95% 94% 96%
97% 91% 91% 95% 98% 95% 94% 96%
9% 5% 6% 10% 19% 11% 8% 12%
100% 100% 100% 100% 100% 100% 100% 100%
Figure 3. Classification of lesions.
Difficulties of detection Accuracy A table of diagnostic accuracies (Table 1) demonstrates the final outcomes of this trial. Accuracy is a combination of the correctly classified true and false positives and negatives, and is affected by disease prevalence, increasing as prevalence decreases. The prevalence of breast cancer is low in the screening population and therefore the diagnostic accuracy is relatively high, ranging from 91 to 98% for radiographers and 95e97% for radiologists. Positive predictive value (PPV) is defined, in this study, as the proportion of women recalled for assessment who have breast cancer, and is associated with the recall rate of each reader. PPV for the radiologists was 12%; Radiographer T5 had an exceptional PPV rate of 19%, while radiographers T1, T4 and T6 had rates of 9%, 10% and 11% respectively (Table 1). Negative predictive value (NPV) represents the proportion of women asked to return to routine rescreen who did not have breast cancer. In this screening cohort, cancers detected were 6.5 per 1000, so the number of women returned to routine rescreen that do not have a cancer is very high (rounded to 100% in Table 1).
Fig. 3 demonstrates what types of lesions were missed by the radiographers. The most common malignant lesion in this cohort was the stellate lesion (21) and the least common was architectural distortion (5) with the rest evenly distributed between calcifications, masses and densities. The missed cancers by the radiographers totalled 21; of these, there were 3 calcifications (calcs), 3 mass lesions, 9 non-specific densities (nsd), and 6 stellate lesions, but there was excellent perception (100%) of architectural distortion (arch dist). The mix of tissue types for the cancers read by each radiographer makes it clear that the majority of cancers were detected in heterogeneously dense tissue, even though the majority of women (88%) were within (at that time) the target age group of 50e69 years (Fig. 4). Table 2 describes the total number of cancers detected and missed calls by radiographers, according to the type of lesion, and density of breast tissue. Eight of the nine non-specific densities that were missed by radiographers were in dense to extremely dense tissue. Radiographer T1 was the only radiographer to miss calcifications (Fig. 5); one was in fatty tissue, while the other two were in dense parenchyma (Table 2). Radiographers T2 and T3 had a mixture of missed lesions, but both detected all their calcifications and only missed one stellate lesion (Fig. 5). There were no cancers missed by radiographer T4; she had mostly stellate and mass lesions to read. Radiographer T5 detected all calcifications in her cohort, missing one non-specific density and one stellate lesion. Radiographer T6 missed all 5 of the non-specific densities (Fig. 5), most of which were in heterogeneously dense tissue (Table 2). Discussion
Figure 2. Change of sensitivities in 2013 (RS ¼ radiologist reference standard).
Two main factors determine the diagnostic accuracy of mammogram interpretation; the first is the technical quality of the image and the second depends on the proficiency and competence
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007
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Figure 4. Types of tissue per radiographer cancers. Figure 5. Types of lesions per radiographer-read cancers.
of the reader, who needs to be able to recognise and correctly interpret the information.27 Sensitivity is the ability of the reader to detect the disease when it is present, and specificity is the ability to return a normal result in the absence of the disease. Assessment of each mammogram results in a ‘recall’ or ‘rescreen’ finding. Five of the six radiographers in this study achieved higher specificity than sensitivity; this suggests that the radiographers have good recognition of ‘normal’ breast tissue. The wide range of sensitivity performance of radiographers in the current study is difficult to explain; all the radiographers had between 10 and 20 years mammography experience. Inherent aptitude for tasks can vary, as can a person's focus and concentration vary at different times. Three radiographers demonstrated sensitivities comparable to that of formally trained radiographers in studies by Haiart & Henderson and Wivell,28,29 and markedly higher than novice radiographers in other studies.20,30e32 The specificity in the current cohort of radiographers is higher than other reported studies, this is largely explained by the radiographers participating in a prospective study, where the number of cancers is low (61 cancers out of 10,000 women in the present study). Possibly some participants were particularly conscious of avoiding excess recalls, which would account for both higher specificities and lower sensitivities. In many other studies, the radiographers were assessed reading retrospective mammograms with a larger number of positive (cancer) findings; which can depress the specificity. In addition, larger numbers of mammograms read appear to demonstrate increased specificity, due in large part to mass screening statistics.33 Some lesions are more obvious than others and this also plays a part in the difficulty of perception and analysis. The majority of missed cancers were non-specific densities and stellate lesions, while the majority of calcifications and masses, and all the architectural distortions were detected. A similar trial by Wivell et al. demonstrated that their (formally trained) radiographers detected significantly more calcifications (p < 0.01) than radiologists and had comparable detection rates for masses and architectural distortion.29 A more recent trial
in Mexico reported that radiographers trained in image interpretation detected the majority of calcifications, and all mass lesions as well as architectural distortion, while missing 75% of asymmetry.34 A trial in the USA by Sumkin et al. reported the largest disagreement between technologists and radiologists occurred in cases of asymmetry or architectural distortion.35 BSA reports that approximately 20 DCIS lesions are detected per 10,000 women screened (all ages, biennial).36 There were 12 calcification lesions detected in this study, which is a little lower than expected in a study of 9348 mammograms. The other lesions have been considered ‘invasive’ lesions due to the fact that BSA does not classify them separately in the monitoring reports; there were 49 invasive lesions detected, which is higher than the reported 43e44 per 10,000.36 The cancers in this study consisted of fewer calcifications and more invasive-type lesions than would be typically expected; however, the (untrained) radiographers in the current study demonstrated results consistent with other studies.29,34,35 The majority of lesions missed by the radiographers were detected in dense glandular tissue. This knowledge may be used to focus formal training for screen reading, concentrating on the lesion types most commonly not visualised or perceived, and the difficulties of perception within dense tissue. The low sensitivity rates of three participants (T1, T2 and T6) can be partly explained by the high percentage of glandular tissue and the types of lesions they were observing. Since Wolfe characterised patterns of breast density, it has been accepted that there is a link between breast density and increased risk of breast cancer37,38; dense breast tissue results in reduced sensitivity of mammography due to ‘masking’ of abnormalities.25 Radiographer T5 combined a high sensitivity and specificity with a low recall rate, for an outstanding result. Radiographer T4 also demonstrated excellent sensitivity, high specificity with a recall rate just above that of the radiologists.
Table 2 Detected and missed cancers, by lesion classification and tissue density. Tissue type
Fatty Scattered Heterogeneous Very dense Total cancers
Calcifications
Mass lesions
Non-spec den
Stellate
Arch dist
Cancers
Missed
Cancers
Missed
Cancers
Missed
Cancers
Missed
Cancers
Missed
1 3 5 3 12
1 0 1 1 3
1 1 8 1 11
0 1 2 0 3
1 2 8 1 12
1 0 7 1 9
6 7 7 1 21
2 2 2 0 6
0 1 4 0 5
0 0 0 0 0
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007
S. Moran, H. Warren-Forward / Radiography xxx (2016) 1e6
Previous studies in Canada and the Netherlands have demonstrated that radiographer assessments can significantly increase the cancer detection of breast screening programs.30,31 Radiographer T3 detected three lesions in 2011 that resulted in cancer diagnosis two years later; this suggests that a strategy of radiologist review of radiographer-reported abnormalities could prove to be beneficial. Radiographers T4 and T5 both demonstrated comparable cancer detection and recall rates to the radiologists. Positives of the research The radiographer participants commented on the fact that the challenge of screen reading emphasized to them the importance of good positioning and compression; they became more aware, when undertaking mammograms, how a lack of good compression can impact on diagnostic accuracy. The undertaking of this trial increased the knowledge, skills and interest of all participants. Information on the types of lesions most commonly overlooked by radiographers may be a useful contribution to training programs for radiographers and may strengthen the evidence base in the future. Limitations to the research The main limitation of this research is the small number of radiographers that participated in the study (n ¼ 6). Another limitation was that the study was conducted in a single Australian BreastScreen Centre which restricts the generalisability of results. The density measures were conducted by the principal researcher and may reflect subjective bias. There may have been interval cancers among the 90 women who did not return to the program, therefore only incident cancers have been studied, which provides only relative (not true) sensitivities. Due to the low number of cancers in the current cohort, it was not possible to apply more stringent statistical analysis, and the authors acknowledge that any analysis performed is significantly underpowered. Again, when comparing differences between the types of cancers missed and breast density, the numbers were too small to apply any significance testing. However, the radiographer performance on average in this study is comparable to other published research.29,34,35 Conclusion Advanced practice roles in mammography screening have been slower to evolve in Australia than in the UK; this may be partially explained by the fact that the shortage of radiologists has not been as dire as that in the UK and also highlights the inflexibility of interprofessional boundaries within our health care system.39,40 Indeed, radiographers in the UK have a very clearly defined career progression and are now competent in many aspects of clinical practice.12,41 There are many radiographers in Australia who are extremely experienced and keen to extend their skills into mammography image interpretation. Properly trained and competency-assessed radiographers could complement the radiology workforce in BSA such that the effects of radiologist shortages on program performance could be alleviated. Other potential advantages of this role development have been identified. Overall program quality would have to be protected by ensuring that screen-reading radiographers were appropriately backfilled for their mammography role, as well as being properly respected and rewarded. Now is the time for Australia to follow the lead of the USA, Europe and the UK who have shown proven success in advanced practice, by providing acknowledgement and accreditation for advanced practitioners in mammogram screen reading.
5
Conflict of interest statement None reported. Acknowledgements The authors would like to acknowledge the Cancer Institute NSW for the award of a Research Innovation Grant (GO189638) which allowed payment to the participants for their time to undertake this study. Thanks also go to the radiographer participants, for the hard work and enthusiasm they demonstrated over a long, timeconsuming trial period. References 1. Commonwealth of Australia. BreastScreen Australia evaluation e review of infrastructure and capacity e April 2009. 2009. Barton ACT. 2. Smith T. Advanced practice e profession-led and patient-focused. Radiographer 2009;56(3):4e5. 3. Kelly A. Breast screens delayed: radiologist shortage cuts services. Newcastle Herald June 28, 2004;2004. Sect. 11. 4. Brooks P, Lapsley H, Butt D. Medical workforce issues in Australia: “tomorrow's doctors e too few, too far”. Med J Aust 2003;179:206e8. 5. Duckett S. Health workforce design for the 21st century. Aust Health Rev 2005;29:201e10. 6. Department of Health. Radiography skill mix. A report on the four tier service delivery model. 2003. London, UK. 7. Anderson C, Brecht J, Heron K, Simpson E, Buxton AJ. A review of formal and informal radiographer reporting/opinion. Radiogr 2006;53:29e33. 8. Brealey S, King D, Hahn S, et al. The costs and effects of introducing selectively trained radiographers to an A&E reporting service: a retrospective controlled before and after study. Br J Radiol 2005;78:499e505. 9. Ian Freckleton. Advanced practice in radiography and Radiation therapy: a report from the interprofessional advisory team. Australian Institute of Radiography; 2012. 10. Johansen LW, Brodersen J. Reading screening mammograms e attitudes among radiologists and radiographers about skill mix. Eur J Radiol 2011;80:325e30. 11. National Health Service. Role development and skill mix in breast screening: a guide to new roles. National Trainers Forum. 2007. 12. Price RC, Le Masurier SB. Longitudinal changes in extended roles in radiography: a new perspective. Radiography 2007;13:18e29. 13. Snaith B, Hardy M, Lewis EF. Radiographer reporting in the UK: a longitudinal analysis. Radiography 2015;21:119e23. 14. Rees Z. Consultant breast radiographers: where are we now?: an evaluation of the current role of the consultant breast radiographer. Radiography 2014;20: 121e5. 15. Moran S, Warren-Forward H. Assessment of the willingness of radiographers in mammography to accept new responsibilities in role extension: part one e quantitative analysis. Radiography 2011;17:270e4. 16. Moran S, Taylor J, Warren-Forward H. Assessment of the willingness of Australian radiographers in mammography to accept new responsibilities in role extension: part two e qualitative analysis. Radiography 2013;19:130e6. 17. Moran S, Warren-Forward H. A retrospective pilot study of the performance of mammographers in interpreting screening mammograms. Radiographer 2010;57:12e9. 18. Moran S, Warren-Forward H. A retrospective study of the performance of radiographers in interpreting screening mammograms. Radiography 2011;17: 126e31. 19. Holt JJ, Pollard K. Radiographers' ability to perceive and classify abnormalities on mammographic images e results of a pilot project. Radiographer 2010;57: 8e14. 20. Debono J, Poulos A, Houssami N, Turner R, Boyages J. Evaluation of radiographers' mammography screen-reading accuracy in Australia. J Med Radiat Sci 2015;62:15e22. 21. Moran S, Warren-Forward H. Can Australian radiographers assess screening mammograms accurately? First stage results from a four year prospective study. Radiography 2015. http://dx.doi.org/10.1016/j.radi.2015.11.005 [in press]. 22. National Accreditation Standards. 2008. Accessed at, www.breastscreen.info.au. 23. Moran S, Warren-Forward H. Development of a training package to increase the performance of radiographers in assessing screening mammograms. Radiographer 2011;58:10e3. 24. Boyd NF, Guo H, Martin LJ, et al. Mammographic density and the risk and detection of breast cancer. N Engl J Med 2007;356:227e36. 25. Carney PA, Miglioretti DL, Yankaskas BC, Kerlikowske K, Rosenberg R. Individual and combined effects of age, breast density and hormone replacement therapy use on the accuracy of screening mammography. Ann Intern Med 2003;138:168e75.
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007
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26. Sickles EA, D'Orsi C, Bassett L. ACR BIRADS Mammography. Reston, VA: American College of Radiology; 2013. 27. Reed W. Mammography interpretation: factors influencing the assessment of accuracy and the perception of abnormality. Radiographer 2005:23e5. 28. Haiart DC, Henderson J. A comparison of interpretation of screening mammograms by a radiographer, a doctor and a radiologist: results and implications. Br J Clin Pract 1991;45:43e5. 29. Wivell G, Denton ERE, Eve CB, Inglis JC, Harvey I. Can radiographers read screening mammograms? Clin Radiol 2003;58:63e7. 30. Duijm LEM, Groenewoud JH, Fracheboud J, de Koning HJ. Additional double reading of screening mammograms by radiologic technologists: impact on screening performance parameters. J Natl Cancer Inst 2007;99:1162e70. 31. Tonita JM, Hillis JP, Lim CH. Medical radiologic technologist review: effects on a population-based breast cancer screening program. Radiology 1999;211: 529e33. 32. Mucci B, Lawson S, Athey G, Scarisbrick G. Radiographers as readers in breast screening: experience with a ‘red dot’ method. Breast 1997;6:183e5. 33. Moran S, Warren-Forward H. The diagnostic accuracy of radiographers assessing screening mammograms: a systematic review. Radiography 2015.
34. Torres-Mejia G, Smith RA, de la Luz Carranza-Flores M, et al. Radiographers supporting radiologists in the interpretation of screening mammography: a viable strategy to meet the shortage in the number of radiologists. BMC Cancer 2015:15. 35. Sumkin JH, Klaman HM, Graham M, et al. Prescreening mammography by technologists: a preliminary assessment. Am J Roentgenol 2003;180:253e6. 36. AIHW. BreastScreen Australia monitoring report 2010e2011. Canberra: A.I.H.W; 2013. 37. Wolfe JN. Breast patterns as an index of risk for developing breast cancer. Am J Roentgenol 1976;126:1130e7. 38. Checka CM, Chun JE, Schnabel FR, Lee J, Toth H. The relationship of mammographic density and age: implications for breast cancer screening. Am J Roentgenol 2012;198:W292e5. 39. Smith T, Lewis S. Opportunities for role development for medical imaging practitioners in Australia: part 2 e mechanisms for change. Radiographer 2003;50:35e9. 40. Tony Smith. Progress towards advanced practice in Australia, New Zealand and the Western Pacific. Radiography 2008;14:20e3. 41. Price R. All together now? Radiography 2012;18:229.
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007
Contents lists available at ScienceDirect
Radiography journal homepage: www.elsevier.com/locate/radi
Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis S. Moran a, b, *, H. Warren-Forward c a b c
BreastScreen NSW Hunter New England, Australia University of Newcastle, Australia Discipline of Medical Radiation Sciences, University of Newcastle, NSW, Australia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 24 October 2015 Received in revised form 20 February 2016 Accepted 26 February 2016 Available online xxx
Introduction: Globally, the role of the radiographer is changing; some countries have developed advanced roles with specific scopes of practice. Other countries, like Australia, are in the process of this change. This paper demonstrates the abilities of Australian radiographers in mammogram screen reading, highlighting some of their specific difficulties with different lesion types. Method: Six experienced radiographers participated in a prospective study, screen reading 2000 mammograms each between 2010 and 2011. This paper looks at the results of those same women at biennial re-screen. Analysis of the results included validation of normal results by negative follow-up screens and new cancers at biennial review; there is also analysis on the types of lesions detected and missed. Results: After biennial review, three cancers in 2013/2014 had been marked as abnormal by one radiographer two years prior, which increased her sensitivity from 64% to 85%. Sensitivity for the radiologists decreased from the assumed 100% to 95%. Radiographers appeared to be skilled in detection of calcifications and architectural distortions but had difficulty with non-specific densities. Conclusion: This study demonstrates the potential for Australian radiographers to enhance the accuracy of screen reading programs. Crown Copyright © 2016 Published by Elsevier Ltd on behalf of The College of Radiographers. All rights reserved.
Keywords: Radiographers Screen reading Accuracy Advanced practice Lesion type Tissue density
Introduction The Australian health care system has a high standard of care and quality of service, but it is struggling to meet the everincreasing demands of an ageing population.1 The increase in service demand will be dependent on a reduced health workforce, which will exacerbate the enormous pressure that some health workers are presently subject to; this in turn increases the risk of clinical error.1,2 In the radiography profession there are some areas where the skills of radiographers could be better utilised, and one of these areas is mammography. Screening programs historically have struggled with a shortage of radiologists3e5 and with radiographer recruitment and retention.1,2
* Corresponding author. 27 King St, Stockton, NSW 2295, Australia. Tel.: þ61 2 49201143, þ61 0427 201147 (mobile). E-mail address: [email protected] (S. Moran).
Other countries such as the USA and some European countries have established advanced practice roles with specific scopes of practice including mammography screen reading.6e8 A change in career structure was well received by the radiography profession in the UK; they have a four tier system incorporating radiographer assistants, radiographer practitioners, advanced practice radiographers and at the highest level, consultant radiographers.6 The Australian Inter-Professional Advisory Team (IPAT) released a document in 2012 which recommended that the Australian Institute of Radiography (AIR) create a framework for a status of Advanced Practitioner within the radiography profession.9 An advanced practitioner would be able to fulfil some of the duties normally undertaken by radiologists; this would also help alleviate the radiologist workload.6,10 In the field of screening mammography, some of the skills identified as possible advanced practice roles include mammogram screen reading and interventional techniques (biopsies and hookwire localisations).11 The scope of radiographers in the UK has widened over the last decade12 and
http://dx.doi.org/10.1016/j.radi.2016.02.007 1078-8174/Crown Copyright © 2016 Published by Elsevier Ltd on behalf of The College of Radiographers. All rights reserved.
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007
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radiographers in the UK now report and provide services independently from radiologists, providing high quality care through excellent clinical practice and leadership.13,14 With the AIR now poised to redesign the structure of professional radiography, Australian radiographers have shown that they are prepared to undertake further study to increase their knowledge, preferring to enhance their careers via clinical roles rather than managerial positions.15,16 Research into the capabilities of Australian mammography radiographers is ongoing, with four retrospective studies published within the last five years.17e20 The first Australian prospective study was completed in 2013, and has resulted in two papers; the first one reports on the performance results of six radiographers in a BreastScreen Australia (BSA) program, comparing their results with those of the radiologists.21 The cancers detected during the study were all biopsy-proven and women returned to screening at that time were assumed to be cancer-free. Follow-up was needed to measure whether any second round cancers had been indicated by the radiographers during the exercise. This paper presents the final results, after biennial follow-up and also investigates the types of lesions and breast tissue that was prevalent in the mammograms read and cancers missed by the radiographers. Methodology Ethics approval was provided by both the University of Newcastle and Hunter New England Area Health (HREC H-352-1206). Participants Six experienced radiographers participated in a prospective study, between 2010 and 2013. The radiographers were aged between 45 and 65 years and had worked in mammography for a minimum of 10 years. The radiographers read 2000 mammograms each, as this number is the annual minimum required for radiologists in BSA as detailed in Appendix P of the National Accreditation Standards (NAS).22 Most radiographers aimed to read a set amount per month (100e200) but this varied according to other commitments. All mammograms were read using a Sectra digital Picture Archiving System (PACS) with 10 megapixel Barco monitors. This equipment was in the normal screen reading area used by the radiologists, with appropriate lighting and viewing conditions. There were approximately 16 radiologists with a minimum of 10 years screen reading experience during this time, 6 of these also participated in assessment clinics. They read all mammograms available and at times that were convenient for them (usual practice), from local and remote sites. Further information on the method and resources used for this trial are detailed in a previous paper with the first stage results.21 The radiographers' results were compared to the combined radiologist outcome, as a reference standard to assess performance criteria. If a radiographer reported a lesion as ‘suspicious’ and it had not been recalled by the radiologists, it was referred to the designated radiologist for his opinion. This occurred twice. An author-developed in-house training package on image assessment23 had been made available to the radiographers between a pilot and full retrospective study, between 2007 and 200917,18; no formal training was provided.
outcomes of the women suggested ‘recall’ by the radiographer readers in 2010/2011. This was to determine whether the radiographers had detected any abnormality at that time which had not been recalled by the radiologists, but proved to be a cancer. There were 48 cancers detected in this group of women; all other negative 2010/2011 results were validated to be normal in 2013/2014 with the exception of three which are discussed in results. Difficulties of detection The images in this study included considerable variety of breast sizes, volumes and breast density; all these factors impact on the efficacy of, and level of difficulty associated with, screen reading accuracy.24,25 The lesions recalled also ranged from very subtle to very obvious, which meant that each radiographer's level of difficulty was different. This final stage analyses the different lesions and types of tissue within which those lesions were situated, ranging from mostly fatty to dense glandular tissue. The density of the breast tissue was subjectively viewed by the lead author, using guidance from the Breast Imaging Reporting Data System (BIRADS).26 Density of the tissue was categorised into one of four types: A. B. C. D.
Predominantly fatty Scattered fibro-glandular elements Heterogeneously dense Extremely dense
Lesions are classified into 6 categories using the Australian BreastScreen Information System (BIS):
Circumscribed mass with or without calcification Stellate lesion Architectural distortion Calcifications Non-specific density Other (may include skin lesions, lymph nodes)
Results In the first stage results, the number of mammograms assessed by individual radiographers varied slightly, depending on availability and a number of excluded images (technical recalls and symptomatic letters), resulting in 9348 individual mammograms. The majority (9197) of these women returned in 2013 (Fig. 1). There had been 61 women with cancers detected in 2011 so those women
Follow-up methodology Follow up on the 9348 women screened in 2010/2011 was conducted at rescreen between September 2012 and December 2013. In particular, the database was checked for all cancers detected. The principal researcher also checked the biennial
Figure 1. Follow up in 2013 of mammograms read in 2010/2011.
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007
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did not return for a screen; they had surgery and treatment and were followed up more closely by specialist doctors. There were 90 women whose results could not be followed up in 2013; this was due to a variety of reasons, including withdrawal from the programme (20), women who did not respond to reminder letters for their rescreen (26) and women who did not get a reminder letter to return because they were out of the target age group (44).
Cancer detection
3
Table 1 Final summary of diagnostic accuracies.
T1 T2 T3 T4 T5 T6 All (median) Radiologists (median)
Cancer detection is the primary focus of all BreastScreen programmes. The cancers detected by radiographers ranged from 10/ 19 or 53% (T6) to 12/12 or 100% (T4) of cancers detected by the radiologists. These were all histology proven cancers, after recall assessment and biopsy. There were 48 (new) cancers detected in the women (n ¼ 9197) in 2013 (Fig. 1). Three of these cancers had been indicated as a recall for assessment by radiographer T3 in 2011. The cancers were detected in the same side and site that T3 had called. If these three cancers had been detected in 2011, the combined radiologist sensitivity would have reduced to 95% (Fig. 2). Radiographer T3 sensitivity would have increased from 64% to 85%, and radiographer T2 sensitivity would have dropped from 82% to 64% as she had returned to screening, two of those three women. None of the other radiographers had assessed these mammograms, and so there was no change in their sensitivities. The change in specificity was minimal, due to the very high number of non-cancers.
Sensitivity
Specificity
Accuracy
PPV
NPV
55% 64% 85% 100% 85% 53% 73% 95%
97% 91% 91% 95% 98% 95% 94% 96%
97% 91% 91% 95% 98% 95% 94% 96%
9% 5% 6% 10% 19% 11% 8% 12%
100% 100% 100% 100% 100% 100% 100% 100%
Figure 3. Classification of lesions.
Difficulties of detection Accuracy A table of diagnostic accuracies (Table 1) demonstrates the final outcomes of this trial. Accuracy is a combination of the correctly classified true and false positives and negatives, and is affected by disease prevalence, increasing as prevalence decreases. The prevalence of breast cancer is low in the screening population and therefore the diagnostic accuracy is relatively high, ranging from 91 to 98% for radiographers and 95e97% for radiologists. Positive predictive value (PPV) is defined, in this study, as the proportion of women recalled for assessment who have breast cancer, and is associated with the recall rate of each reader. PPV for the radiologists was 12%; Radiographer T5 had an exceptional PPV rate of 19%, while radiographers T1, T4 and T6 had rates of 9%, 10% and 11% respectively (Table 1). Negative predictive value (NPV) represents the proportion of women asked to return to routine rescreen who did not have breast cancer. In this screening cohort, cancers detected were 6.5 per 1000, so the number of women returned to routine rescreen that do not have a cancer is very high (rounded to 100% in Table 1).
Fig. 3 demonstrates what types of lesions were missed by the radiographers. The most common malignant lesion in this cohort was the stellate lesion (21) and the least common was architectural distortion (5) with the rest evenly distributed between calcifications, masses and densities. The missed cancers by the radiographers totalled 21; of these, there were 3 calcifications (calcs), 3 mass lesions, 9 non-specific densities (nsd), and 6 stellate lesions, but there was excellent perception (100%) of architectural distortion (arch dist). The mix of tissue types for the cancers read by each radiographer makes it clear that the majority of cancers were detected in heterogeneously dense tissue, even though the majority of women (88%) were within (at that time) the target age group of 50e69 years (Fig. 4). Table 2 describes the total number of cancers detected and missed calls by radiographers, according to the type of lesion, and density of breast tissue. Eight of the nine non-specific densities that were missed by radiographers were in dense to extremely dense tissue. Radiographer T1 was the only radiographer to miss calcifications (Fig. 5); one was in fatty tissue, while the other two were in dense parenchyma (Table 2). Radiographers T2 and T3 had a mixture of missed lesions, but both detected all their calcifications and only missed one stellate lesion (Fig. 5). There were no cancers missed by radiographer T4; she had mostly stellate and mass lesions to read. Radiographer T5 detected all calcifications in her cohort, missing one non-specific density and one stellate lesion. Radiographer T6 missed all 5 of the non-specific densities (Fig. 5), most of which were in heterogeneously dense tissue (Table 2). Discussion
Figure 2. Change of sensitivities in 2013 (RS ¼ radiologist reference standard).
Two main factors determine the diagnostic accuracy of mammogram interpretation; the first is the technical quality of the image and the second depends on the proficiency and competence
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007
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Figure 4. Types of tissue per radiographer cancers. Figure 5. Types of lesions per radiographer-read cancers.
of the reader, who needs to be able to recognise and correctly interpret the information.27 Sensitivity is the ability of the reader to detect the disease when it is present, and specificity is the ability to return a normal result in the absence of the disease. Assessment of each mammogram results in a ‘recall’ or ‘rescreen’ finding. Five of the six radiographers in this study achieved higher specificity than sensitivity; this suggests that the radiographers have good recognition of ‘normal’ breast tissue. The wide range of sensitivity performance of radiographers in the current study is difficult to explain; all the radiographers had between 10 and 20 years mammography experience. Inherent aptitude for tasks can vary, as can a person's focus and concentration vary at different times. Three radiographers demonstrated sensitivities comparable to that of formally trained radiographers in studies by Haiart & Henderson and Wivell,28,29 and markedly higher than novice radiographers in other studies.20,30e32 The specificity in the current cohort of radiographers is higher than other reported studies, this is largely explained by the radiographers participating in a prospective study, where the number of cancers is low (61 cancers out of 10,000 women in the present study). Possibly some participants were particularly conscious of avoiding excess recalls, which would account for both higher specificities and lower sensitivities. In many other studies, the radiographers were assessed reading retrospective mammograms with a larger number of positive (cancer) findings; which can depress the specificity. In addition, larger numbers of mammograms read appear to demonstrate increased specificity, due in large part to mass screening statistics.33 Some lesions are more obvious than others and this also plays a part in the difficulty of perception and analysis. The majority of missed cancers were non-specific densities and stellate lesions, while the majority of calcifications and masses, and all the architectural distortions were detected. A similar trial by Wivell et al. demonstrated that their (formally trained) radiographers detected significantly more calcifications (p < 0.01) than radiologists and had comparable detection rates for masses and architectural distortion.29 A more recent trial
in Mexico reported that radiographers trained in image interpretation detected the majority of calcifications, and all mass lesions as well as architectural distortion, while missing 75% of asymmetry.34 A trial in the USA by Sumkin et al. reported the largest disagreement between technologists and radiologists occurred in cases of asymmetry or architectural distortion.35 BSA reports that approximately 20 DCIS lesions are detected per 10,000 women screened (all ages, biennial).36 There were 12 calcification lesions detected in this study, which is a little lower than expected in a study of 9348 mammograms. The other lesions have been considered ‘invasive’ lesions due to the fact that BSA does not classify them separately in the monitoring reports; there were 49 invasive lesions detected, which is higher than the reported 43e44 per 10,000.36 The cancers in this study consisted of fewer calcifications and more invasive-type lesions than would be typically expected; however, the (untrained) radiographers in the current study demonstrated results consistent with other studies.29,34,35 The majority of lesions missed by the radiographers were detected in dense glandular tissue. This knowledge may be used to focus formal training for screen reading, concentrating on the lesion types most commonly not visualised or perceived, and the difficulties of perception within dense tissue. The low sensitivity rates of three participants (T1, T2 and T6) can be partly explained by the high percentage of glandular tissue and the types of lesions they were observing. Since Wolfe characterised patterns of breast density, it has been accepted that there is a link between breast density and increased risk of breast cancer37,38; dense breast tissue results in reduced sensitivity of mammography due to ‘masking’ of abnormalities.25 Radiographer T5 combined a high sensitivity and specificity with a low recall rate, for an outstanding result. Radiographer T4 also demonstrated excellent sensitivity, high specificity with a recall rate just above that of the radiologists.
Table 2 Detected and missed cancers, by lesion classification and tissue density. Tissue type
Fatty Scattered Heterogeneous Very dense Total cancers
Calcifications
Mass lesions
Non-spec den
Stellate
Arch dist
Cancers
Missed
Cancers
Missed
Cancers
Missed
Cancers
Missed
Cancers
Missed
1 3 5 3 12
1 0 1 1 3
1 1 8 1 11
0 1 2 0 3
1 2 8 1 12
1 0 7 1 9
6 7 7 1 21
2 2 2 0 6
0 1 4 0 5
0 0 0 0 0
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007
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Previous studies in Canada and the Netherlands have demonstrated that radiographer assessments can significantly increase the cancer detection of breast screening programs.30,31 Radiographer T3 detected three lesions in 2011 that resulted in cancer diagnosis two years later; this suggests that a strategy of radiologist review of radiographer-reported abnormalities could prove to be beneficial. Radiographers T4 and T5 both demonstrated comparable cancer detection and recall rates to the radiologists. Positives of the research The radiographer participants commented on the fact that the challenge of screen reading emphasized to them the importance of good positioning and compression; they became more aware, when undertaking mammograms, how a lack of good compression can impact on diagnostic accuracy. The undertaking of this trial increased the knowledge, skills and interest of all participants. Information on the types of lesions most commonly overlooked by radiographers may be a useful contribution to training programs for radiographers and may strengthen the evidence base in the future. Limitations to the research The main limitation of this research is the small number of radiographers that participated in the study (n ¼ 6). Another limitation was that the study was conducted in a single Australian BreastScreen Centre which restricts the generalisability of results. The density measures were conducted by the principal researcher and may reflect subjective bias. There may have been interval cancers among the 90 women who did not return to the program, therefore only incident cancers have been studied, which provides only relative (not true) sensitivities. Due to the low number of cancers in the current cohort, it was not possible to apply more stringent statistical analysis, and the authors acknowledge that any analysis performed is significantly underpowered. Again, when comparing differences between the types of cancers missed and breast density, the numbers were too small to apply any significance testing. However, the radiographer performance on average in this study is comparable to other published research.29,34,35 Conclusion Advanced practice roles in mammography screening have been slower to evolve in Australia than in the UK; this may be partially explained by the fact that the shortage of radiologists has not been as dire as that in the UK and also highlights the inflexibility of interprofessional boundaries within our health care system.39,40 Indeed, radiographers in the UK have a very clearly defined career progression and are now competent in many aspects of clinical practice.12,41 There are many radiographers in Australia who are extremely experienced and keen to extend their skills into mammography image interpretation. Properly trained and competency-assessed radiographers could complement the radiology workforce in BSA such that the effects of radiologist shortages on program performance could be alleviated. Other potential advantages of this role development have been identified. Overall program quality would have to be protected by ensuring that screen-reading radiographers were appropriately backfilled for their mammography role, as well as being properly respected and rewarded. Now is the time for Australia to follow the lead of the USA, Europe and the UK who have shown proven success in advanced practice, by providing acknowledgement and accreditation for advanced practitioners in mammogram screen reading.
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Conflict of interest statement None reported. Acknowledgements The authors would like to acknowledge the Cancer Institute NSW for the award of a Research Innovation Grant (GO189638) which allowed payment to the participants for their time to undertake this study. Thanks also go to the radiographer participants, for the hard work and enthusiasm they demonstrated over a long, timeconsuming trial period. References 1. Commonwealth of Australia. BreastScreen Australia evaluation e review of infrastructure and capacity e April 2009. 2009. Barton ACT. 2. Smith T. Advanced practice e profession-led and patient-focused. Radiographer 2009;56(3):4e5. 3. Kelly A. Breast screens delayed: radiologist shortage cuts services. Newcastle Herald June 28, 2004;2004. Sect. 11. 4. Brooks P, Lapsley H, Butt D. Medical workforce issues in Australia: “tomorrow's doctors e too few, too far”. Med J Aust 2003;179:206e8. 5. Duckett S. Health workforce design for the 21st century. Aust Health Rev 2005;29:201e10. 6. Department of Health. Radiography skill mix. A report on the four tier service delivery model. 2003. London, UK. 7. Anderson C, Brecht J, Heron K, Simpson E, Buxton AJ. A review of formal and informal radiographer reporting/opinion. Radiogr 2006;53:29e33. 8. Brealey S, King D, Hahn S, et al. The costs and effects of introducing selectively trained radiographers to an A&E reporting service: a retrospective controlled before and after study. Br J Radiol 2005;78:499e505. 9. Ian Freckleton. Advanced practice in radiography and Radiation therapy: a report from the interprofessional advisory team. Australian Institute of Radiography; 2012. 10. Johansen LW, Brodersen J. Reading screening mammograms e attitudes among radiologists and radiographers about skill mix. Eur J Radiol 2011;80:325e30. 11. National Health Service. Role development and skill mix in breast screening: a guide to new roles. National Trainers Forum. 2007. 12. Price RC, Le Masurier SB. Longitudinal changes in extended roles in radiography: a new perspective. Radiography 2007;13:18e29. 13. Snaith B, Hardy M, Lewis EF. Radiographer reporting in the UK: a longitudinal analysis. Radiography 2015;21:119e23. 14. Rees Z. Consultant breast radiographers: where are we now?: an evaluation of the current role of the consultant breast radiographer. Radiography 2014;20: 121e5. 15. Moran S, Warren-Forward H. Assessment of the willingness of radiographers in mammography to accept new responsibilities in role extension: part one e quantitative analysis. Radiography 2011;17:270e4. 16. Moran S, Taylor J, Warren-Forward H. Assessment of the willingness of Australian radiographers in mammography to accept new responsibilities in role extension: part two e qualitative analysis. Radiography 2013;19:130e6. 17. Moran S, Warren-Forward H. A retrospective pilot study of the performance of mammographers in interpreting screening mammograms. Radiographer 2010;57:12e9. 18. Moran S, Warren-Forward H. A retrospective study of the performance of radiographers in interpreting screening mammograms. Radiography 2011;17: 126e31. 19. Holt JJ, Pollard K. Radiographers' ability to perceive and classify abnormalities on mammographic images e results of a pilot project. Radiographer 2010;57: 8e14. 20. Debono J, Poulos A, Houssami N, Turner R, Boyages J. Evaluation of radiographers' mammography screen-reading accuracy in Australia. J Med Radiat Sci 2015;62:15e22. 21. Moran S, Warren-Forward H. Can Australian radiographers assess screening mammograms accurately? First stage results from a four year prospective study. Radiography 2015. http://dx.doi.org/10.1016/j.radi.2015.11.005 [in press]. 22. National Accreditation Standards. 2008. Accessed at, www.breastscreen.info.au. 23. Moran S, Warren-Forward H. Development of a training package to increase the performance of radiographers in assessing screening mammograms. Radiographer 2011;58:10e3. 24. Boyd NF, Guo H, Martin LJ, et al. Mammographic density and the risk and detection of breast cancer. N Engl J Med 2007;356:227e36. 25. Carney PA, Miglioretti DL, Yankaskas BC, Kerlikowske K, Rosenberg R. Individual and combined effects of age, breast density and hormone replacement therapy use on the accuracy of screening mammography. Ann Intern Med 2003;138:168e75.
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007
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S. Moran, H. Warren-Forward / Radiography xxx (2016) 1e6
26. Sickles EA, D'Orsi C, Bassett L. ACR BIRADS Mammography. Reston, VA: American College of Radiology; 2013. 27. Reed W. Mammography interpretation: factors influencing the assessment of accuracy and the perception of abnormality. Radiographer 2005:23e5. 28. Haiart DC, Henderson J. A comparison of interpretation of screening mammograms by a radiographer, a doctor and a radiologist: results and implications. Br J Clin Pract 1991;45:43e5. 29. Wivell G, Denton ERE, Eve CB, Inglis JC, Harvey I. Can radiographers read screening mammograms? Clin Radiol 2003;58:63e7. 30. Duijm LEM, Groenewoud JH, Fracheboud J, de Koning HJ. Additional double reading of screening mammograms by radiologic technologists: impact on screening performance parameters. J Natl Cancer Inst 2007;99:1162e70. 31. Tonita JM, Hillis JP, Lim CH. Medical radiologic technologist review: effects on a population-based breast cancer screening program. Radiology 1999;211: 529e33. 32. Mucci B, Lawson S, Athey G, Scarisbrick G. Radiographers as readers in breast screening: experience with a ‘red dot’ method. Breast 1997;6:183e5. 33. Moran S, Warren-Forward H. The diagnostic accuracy of radiographers assessing screening mammograms: a systematic review. Radiography 2015.
34. Torres-Mejia G, Smith RA, de la Luz Carranza-Flores M, et al. Radiographers supporting radiologists in the interpretation of screening mammography: a viable strategy to meet the shortage in the number of radiologists. BMC Cancer 2015:15. 35. Sumkin JH, Klaman HM, Graham M, et al. Prescreening mammography by technologists: a preliminary assessment. Am J Roentgenol 2003;180:253e6. 36. AIHW. BreastScreen Australia monitoring report 2010e2011. Canberra: A.I.H.W; 2013. 37. Wolfe JN. Breast patterns as an index of risk for developing breast cancer. Am J Roentgenol 1976;126:1130e7. 38. Checka CM, Chun JE, Schnabel FR, Lee J, Toth H. The relationship of mammographic density and age: implications for breast cancer screening. Am J Roentgenol 2012;198:W292e5. 39. Smith T, Lewis S. Opportunities for role development for medical imaging practitioners in Australia: part 2 e mechanisms for change. Radiographer 2003;50:35e9. 40. Tony Smith. Progress towards advanced practice in Australia, New Zealand and the Western Pacific. Radiography 2008;14:20e3. 41. Price R. All together now? Radiography 2012;18:229.
Please cite this article in press as: Moran S, Warren-Forward H, Can Australian radiographers assess screening mammograms accurately? Biennial follow-up from a four year prospective study and lesion analysis, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.007