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Missed Cancers
Laurie Margolies, MD; Wendie A. Berg, MD, PhD, FACR, FSBI
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KEY FACTS

  • Terminology

    • Imaging

      • Clinical Issues

        TERMINOLOGY

        • Definitions

          • Screening mammogram: Testing to detect cancer in women with no signs or symptoms of breast cancer
          • Diagnostic mammogram: Examination performed with monitoring by on-site radiologist
            • Symptoms: Lump, nipple discharge or retraction, change in breast size or shape, skin thickening or retraction
            • Recall from screening for additional imaging or follow-up of abnormality noted on prior breast imaging
          • Missed cancer: Visible in retrospect on prior breast imaging
            • True miss: Suspicious finding at cancer site on review
              • Errors in perception: Finding overlooked
                • Satisfaction of search, technical problems, inherent features of cancer &/or surrounding tissue (poor lesion conspicuity, subtle findings), fatigue, workplace distractions and interruptions
              • Errors in interpretation: Finding seen but dismissed as normal or benign
            • Subthreshold finding: Perceptible finding without characteristics judged as having required further work-up at that time
          • False-negatives (FN) on audits are specifically defined
            • Tissue diagnosis of cancer within screening interval (in USA typically within 365 days) after prior screening reported as negative or benign
              • Or prior diagnostic imaging negative, benign, or probably benign
              • FN even if cancer not visible in retrospect
            • FN even if detected by early next screen
            • If > 1 year (USA, assuming 1-year screening interval suggested) has elapsed since prior examination, it is not FN at audit, even if cancer is visible in retrospect
          • Actionable: Retrospective determination that finding was present on prior examination at site of malignancy that should have prompted further evaluation
            • Retrospective blinded studies found actionable findings on 25-41% prior screening mammograms
              • When normal cases included (2 of 6 studies): 27-29% of missed cancers actionable
            • Retrospective nonblinded studies of screening mammograms found actionable findings in 23-77%
          • Interval cancer: Cancers detected clinically between recommended screenings
            • Time interval varies based on screening recommendations: 12-36 months
            • 10-12% of breast cancers in fatty breasts; > 50% in women with dense breasts
            • Tend to be larger, higher grade; lymph node metastases more likely compared to screen-detected cancers
            • Some interval cancers are missed cancers; others are occult on imaging ("true interval" cancer)

        IMAGING

        • General Features

          • Mammographic Findings

            • Ultrasonographic Findings

              • MR Findings

                • Imaging Recommendations

                  DIFFERENTIAL DIAGNOSIS

                    PATHOLOGY

                    • General Features

                      CLINICAL ISSUES

                      • Presentation

                        • Demographics

                          DIAGNOSTIC CHECKLIST

                          • Consider

                            • Image Interpretation Pearls

                              Selected References

                              1. Clauser P et al: Motion artifacts, lesion type, and parenchymal enhancement in breast MRI: what does really influence diagnostic accuracy? Acta Radiol. 284185118770918, 2018
                              2. Ekpo EU et al: Errors in mammography cannot be solved through technology alone Asian Pac J Cancer Prev. 19(2):291-301, 2018
                              3. Mordang JJ et al: The importance of early detection of calcifications associated with breast cancer in screening. Breast Cancer Res Treat. 167(2):451-58, 2018
                              4. Schreutelkamp IL et al: Breast cancers missed by screening radiologists can be detected by reading mammograms at a distance. Ir J Med Sci. ePub, 2018
                              5. Vreemann S et al: The frequency of missed breast cancers in women participating in a high-risk MRI screening program. Breast Cancer Res Treat. ePub, 2018
                              6. Grubstein A et al: Analysis of false-negative readings of automated breast ultrasound studies. J Clin Ultrasound. 45(5):245-51, 2017
                              7. Lekanidi K et al: Breast screening: what can the interval cancer review teach us? Are we perhaps being a bit too hard on ourselves? Eur J Radiol. 94:13-15, 2017
                              8. Margolies LR et al: The chest radiologist's role in invasive breast cancer detection. Clin Imaging. 50:13-19, 2017
                              9. Mohd Norsuddin N et al: An investigation into the mammographic appearances of missed breast cancers when recall rates are reduced. Br J Radiol. 90(1076):20170048, 2017
                              10. Warren LM et al: Image processing can cause some malignant soft-tissue lesions to be missed in digital mammography images. Clin Radiol. 72(9):799.e1-799.e8, 2017
                              11. Yoon JH et al: Ultrasonographic evaluation of women with pathologic nipple discharge. Ultrasonography. 36(4):310-320, 2017
                              12. Yun SJ et al: Benefit of adding digital breast tomosynthesis to digital mammography for breast cancer screening focused on cancer characteristics: a meta-analysis. Breast Cancer Res Treat. 164(3):557-569, 2017
                              13. Zuckerman SP et al: Imaging with synthesized 2D mammography: differences, advantages, and pitfalls compared with digital mammography. AJR Am J Roentgenol. 209(1):222-29, 2017
                              14. Gubern-Mérida A et al: Automated detection of breast cancer in false-negative screening MRI studies from women at increased risk. Eur J Radiol. 85(2):472-9, 2016
                              15. Hayward JH et al: Improving screening mammography outcomes through comparison with multiple prior mammograms. AJR Am J Roentgenol. 207(4):918-24, 2016
                              16. Korhonen KE et al: Strategies to increase cancer detection: review of true-positive and false-negative results at digital breast tomosynthesis screening. Radiographics. 36(7):1954-65, 2016
                              17. Palazzetti V et al: Analysis of mammographic diagnostic errors in breast clinic. Radiol Med. 121(11):828-33, 2016
                              18. Seo M et al: Features of undiagnosed breast cancers at screening breast mr imaging and potential utility of computer-aided evaluation. Korean J Radiol. 17(1):59-68, 2016
                              19. Wadhwa A et al: Missed breast cancer: what can we learn? Curr Probl Diagn Radiol. 45(6):402-19, 2016
                              20. Geertse TD et al: Value of audits in breast cancer screening quality assurance programmes. Eur Radiol. 25(11):3338-47, 2015
                              21. Song SE et al: Undiagnosed breast cancer: features at supplemental screening US. Radiology. 277(2):372-80, 2015
                              22. Bae MS et al: Breast cancer detected with screening US: reasons for nondetection at mammography. Radiology. 270(2):369-77, 2014
                              23. Uematsu T: Ultrasonographic findings of missed breast cancer: pitfalls and pearls. Breast Cancer. 21(1):10-9, 2014
                              24. Yeh ED et al: Positioning in breast MR imaging to optimize image quality. Radiographics. 34(1):E1-17, 2014
                              25. Evans KK et al: If you don't find it often, you often don't find it: why some cancers are missed in breast cancer screening. PLoS One. 8(5):e64366, 2013
                              26. Hoff SR et al: Breast cancer: missed interval and screening-detected cancer at full-field digital mammography and screen-film mammography-- results from a retrospective review. Radiology. 264(2):378-86, 2012
                              27. Nishikawa RM et al: Clinically missed cancer: how effectively can radiologists use computer-aided detection? AJR Am J Roentgenol. 198(3):708-16, 2012
                              28. Pages EB et al: Undiagnosed breast cancer at MR imaging: analysis of causes. Radiology. 264(1):40-50, 2012
                              29. Obdeijn IM et al: Assessment of false-negative cases of breast MR imaging in women with a familial or genetic predisposition. Breast Cancer Res Treat. 119(2):399-407, 2010
                              30. Schnall MD et al: Diagnostic architectural and dynamic features at breast MR imaging: multicenter study. Radiology. 238(1):42-53, 2006
                              31. Bassett LW et al: Diagnosis of diseases of the breast. 2nd ed. Philadelphia: Elsevier-Saunders. 193-223, 2005
                              32. Wolfe JM et al: Cognitive psychology: rare items often missed in visual searches. Nature. 435(7041):439-40, 2005
                              33. Roubidoux MA et al: Invasive cancers detected after breast cancer screening yielded a negative result: relationship of mammographic density to tumor prognostic factors. Radiology. 230(1):42-8, 2004
                              34. Ikeda DM et al: Analysis of 172 subtle findings on prior normal mammograms in women with breast cancer detected at follow-up screening. Radiology. 226(2):494-503, 2003
                              35. Majid AS et al: Missed breast carcinoma: pitfalls and pearls. Radiographics. 23(4):881-95, 2003
                              36. Birdwell RL et al: Mammographic characteristics of 115 missed cancers later detected with screening mammography and the potential utility of computer-aided detection. Radiology. 219(1):192-202, 2001
                              37. Ganott MA et al: Analysis of false-negative cancer cases identified with a mammography audit. Breast J. 5(3):166-175, 1999
                              38. Siegle RL et al: Rates of disagreement in imaging interpretation in a group of community hospitals. Acad Radiol. 5(3):148-54, 1998
                              39. Nodine CF et al: Nature of expertise in searching mammograms for breast masses. Acad Radiol. 3(12):1000-6, 1996
                              40. Harvey JA et al: Previous mammograms in patients with impalpable breast carcinoma: retrospective vs blinded interpretation. 1993 ARRS President's Award. AJR Am J Roentgenol. 161(6):1167-72, 1993
                              41. Bird RE et al: Analysis of cancers missed at screening mammography. Radiology. 184(3):613-7, 1992
                              Related Anatomy
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                              Related Differential Diagnoses
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                              References
                              Tables

                              Tables

                              KEY FACTS

                              • Terminology

                                • Imaging

                                  • Clinical Issues

                                    TERMINOLOGY

                                    • Definitions

                                      • Screening mammogram: Testing to detect cancer in women with no signs or symptoms of breast cancer
                                      • Diagnostic mammogram: Examination performed with monitoring by on-site radiologist
                                        • Symptoms: Lump, nipple discharge or retraction, change in breast size or shape, skin thickening or retraction
                                        • Recall from screening for additional imaging or follow-up of abnormality noted on prior breast imaging
                                      • Missed cancer: Visible in retrospect on prior breast imaging
                                        • True miss: Suspicious finding at cancer site on review
                                          • Errors in perception: Finding overlooked
                                            • Satisfaction of search, technical problems, inherent features of cancer &/or surrounding tissue (poor lesion conspicuity, subtle findings), fatigue, workplace distractions and interruptions
                                          • Errors in interpretation: Finding seen but dismissed as normal or benign
                                        • Subthreshold finding: Perceptible finding without characteristics judged as having required further work-up at that time
                                      • False-negatives (FN) on audits are specifically defined
                                        • Tissue diagnosis of cancer within screening interval (in USA typically within 365 days) after prior screening reported as negative or benign
                                          • Or prior diagnostic imaging negative, benign, or probably benign
                                          • FN even if cancer not visible in retrospect
                                        • FN even if detected by early next screen
                                        • If > 1 year (USA, assuming 1-year screening interval suggested) has elapsed since prior examination, it is not FN at audit, even if cancer is visible in retrospect
                                      • Actionable: Retrospective determination that finding was present on prior examination at site of malignancy that should have prompted further evaluation
                                        • Retrospective blinded studies found actionable findings on 25-41% prior screening mammograms
                                          • When normal cases included (2 of 6 studies): 27-29% of missed cancers actionable
                                        • Retrospective nonblinded studies of screening mammograms found actionable findings in 23-77%
                                      • Interval cancer: Cancers detected clinically between recommended screenings
                                        • Time interval varies based on screening recommendations: 12-36 months
                                        • 10-12% of breast cancers in fatty breasts; > 50% in women with dense breasts
                                        • Tend to be larger, higher grade; lymph node metastases more likely compared to screen-detected cancers
                                        • Some interval cancers are missed cancers; others are occult on imaging ("true interval" cancer)

                                    IMAGING

                                    • General Features

                                      • Mammographic Findings

                                        • Ultrasonographic Findings

                                          • MR Findings

                                            • Imaging Recommendations

                                              DIFFERENTIAL DIAGNOSIS

                                                PATHOLOGY

                                                • General Features

                                                  CLINICAL ISSUES

                                                  • Presentation

                                                    • Demographics

                                                      DIAGNOSTIC CHECKLIST

                                                      • Consider

                                                        • Image Interpretation Pearls

                                                          Selected References

                                                          1. Clauser P et al: Motion artifacts, lesion type, and parenchymal enhancement in breast MRI: what does really influence diagnostic accuracy? Acta Radiol. 284185118770918, 2018
                                                          2. Ekpo EU et al: Errors in mammography cannot be solved through technology alone Asian Pac J Cancer Prev. 19(2):291-301, 2018
                                                          3. Mordang JJ et al: The importance of early detection of calcifications associated with breast cancer in screening. Breast Cancer Res Treat. 167(2):451-58, 2018
                                                          4. Schreutelkamp IL et al: Breast cancers missed by screening radiologists can be detected by reading mammograms at a distance. Ir J Med Sci. ePub, 2018
                                                          5. Vreemann S et al: The frequency of missed breast cancers in women participating in a high-risk MRI screening program. Breast Cancer Res Treat. ePub, 2018
                                                          6. Grubstein A et al: Analysis of false-negative readings of automated breast ultrasound studies. J Clin Ultrasound. 45(5):245-51, 2017
                                                          7. Lekanidi K et al: Breast screening: what can the interval cancer review teach us? Are we perhaps being a bit too hard on ourselves? Eur J Radiol. 94:13-15, 2017
                                                          8. Margolies LR et al: The chest radiologist's role in invasive breast cancer detection. Clin Imaging. 50:13-19, 2017
                                                          9. Mohd Norsuddin N et al: An investigation into the mammographic appearances of missed breast cancers when recall rates are reduced. Br J Radiol. 90(1076):20170048, 2017
                                                          10. Warren LM et al: Image processing can cause some malignant soft-tissue lesions to be missed in digital mammography images. Clin Radiol. 72(9):799.e1-799.e8, 2017
                                                          11. Yoon JH et al: Ultrasonographic evaluation of women with pathologic nipple discharge. Ultrasonography. 36(4):310-320, 2017
                                                          12. Yun SJ et al: Benefit of adding digital breast tomosynthesis to digital mammography for breast cancer screening focused on cancer characteristics: a meta-analysis. Breast Cancer Res Treat. 164(3):557-569, 2017
                                                          13. Zuckerman SP et al: Imaging with synthesized 2D mammography: differences, advantages, and pitfalls compared with digital mammography. AJR Am J Roentgenol. 209(1):222-29, 2017
                                                          14. Gubern-Mérida A et al: Automated detection of breast cancer in false-negative screening MRI studies from women at increased risk. Eur J Radiol. 85(2):472-9, 2016
                                                          15. Hayward JH et al: Improving screening mammography outcomes through comparison with multiple prior mammograms. AJR Am J Roentgenol. 207(4):918-24, 2016
                                                          16. Korhonen KE et al: Strategies to increase cancer detection: review of true-positive and false-negative results at digital breast tomosynthesis screening. Radiographics. 36(7):1954-65, 2016
                                                          17. Palazzetti V et al: Analysis of mammographic diagnostic errors in breast clinic. Radiol Med. 121(11):828-33, 2016
                                                          18. Seo M et al: Features of undiagnosed breast cancers at screening breast mr imaging and potential utility of computer-aided evaluation. Korean J Radiol. 17(1):59-68, 2016
                                                          19. Wadhwa A et al: Missed breast cancer: what can we learn? Curr Probl Diagn Radiol. 45(6):402-19, 2016
                                                          20. Geertse TD et al: Value of audits in breast cancer screening quality assurance programmes. Eur Radiol. 25(11):3338-47, 2015
                                                          21. Song SE et al: Undiagnosed breast cancer: features at supplemental screening US. Radiology. 277(2):372-80, 2015
                                                          22. Bae MS et al: Breast cancer detected with screening US: reasons for nondetection at mammography. Radiology. 270(2):369-77, 2014
                                                          23. Uematsu T: Ultrasonographic findings of missed breast cancer: pitfalls and pearls. Breast Cancer. 21(1):10-9, 2014
                                                          24. Yeh ED et al: Positioning in breast MR imaging to optimize image quality. Radiographics. 34(1):E1-17, 2014
                                                          25. Evans KK et al: If you don't find it often, you often don't find it: why some cancers are missed in breast cancer screening. PLoS One. 8(5):e64366, 2013
                                                          26. Hoff SR et al: Breast cancer: missed interval and screening-detected cancer at full-field digital mammography and screen-film mammography-- results from a retrospective review. Radiology. 264(2):378-86, 2012
                                                          27. Nishikawa RM et al: Clinically missed cancer: how effectively can radiologists use computer-aided detection? AJR Am J Roentgenol. 198(3):708-16, 2012
                                                          28. Pages EB et al: Undiagnosed breast cancer at MR imaging: analysis of causes. Radiology. 264(1):40-50, 2012
                                                          29. Obdeijn IM et al: Assessment of false-negative cases of breast MR imaging in women with a familial or genetic predisposition. Breast Cancer Res Treat. 119(2):399-407, 2010
                                                          30. Schnall MD et al: Diagnostic architectural and dynamic features at breast MR imaging: multicenter study. Radiology. 238(1):42-53, 2006
                                                          31. Bassett LW et al: Diagnosis of diseases of the breast. 2nd ed. Philadelphia: Elsevier-Saunders. 193-223, 2005
                                                          32. Wolfe JM et al: Cognitive psychology: rare items often missed in visual searches. Nature. 435(7041):439-40, 2005
                                                          33. Roubidoux MA et al: Invasive cancers detected after breast cancer screening yielded a negative result: relationship of mammographic density to tumor prognostic factors. Radiology. 230(1):42-8, 2004
                                                          34. Ikeda DM et al: Analysis of 172 subtle findings on prior normal mammograms in women with breast cancer detected at follow-up screening. Radiology. 226(2):494-503, 2003
                                                          35. Majid AS et al: Missed breast carcinoma: pitfalls and pearls. Radiographics. 23(4):881-95, 2003
                                                          36. Birdwell RL et al: Mammographic characteristics of 115 missed cancers later detected with screening mammography and the potential utility of computer-aided detection. Radiology. 219(1):192-202, 2001
                                                          37. Ganott MA et al: Analysis of false-negative cancer cases identified with a mammography audit. Breast J. 5(3):166-175, 1999
                                                          38. Siegle RL et al: Rates of disagreement in imaging interpretation in a group of community hospitals. Acad Radiol. 5(3):148-54, 1998
                                                          39. Nodine CF et al: Nature of expertise in searching mammograms for breast masses. Acad Radiol. 3(12):1000-6, 1996
                                                          40. Harvey JA et al: Previous mammograms in patients with impalpable breast carcinoma: retrospective vs blinded interpretation. 1993 ARRS President's Award. AJR Am J Roentgenol. 161(6):1167-72, 1993
                                                          41. Bird RE et al: Analysis of cancers missed at screening mammography. Radiology. 184(3):613-7, 1992