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  • Review Article
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Active surveillance for prostate and thyroid cancers: evolution in clinical paradigms and lessons learned

Nature Reviews Clinical Oncology volume 16, pages 168–184 (2019)Cite this article

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Abstract

The adverse effects of overdiagnosis and overtreatment observed in men with clinically insignificant prostate cancers after the introduction of prostate-specific antigen-based screening are now being observed in those with thyroid cancer, owing to the introduction of new imaging technologies. Thus, the evolving paradigm of active surveillance in prostate and thyroid cancers might be valuable in informing the development of future active surveillance protocols. The lessons learned from active surveillance and their implications include the need to minimize the use of broad, population-based screening programmes that do not incorporate patient education and the need for individualized or shared decision-making, which can decrease the extent of overtreatment. Furthermore, from the experience in patients with prostate cancer, we have learned that consensus is required regarding the optimal selection of patients for active surveillance, using more-specific evidence-based methods for stratifying patients by risk. In this Review, we describe the epidemiology, pathology and screening guidelines for the management of patients with prostate and thyroid cancers; the evidence of overdiagnosis and overtreatment; and provide overviews of existing international active surveillance protocols.

Key points

  • The harms of overdiagnosis and overtreatment that were observed in patients with prostate cancer following the introduction of prostate-specific antigen based screening are now being observed in those with thyroid cancer.

  • Broad population-based screening can lead to the overdiagnosis and overtreatment of indolent cancers, as originally seen in prostate cancer and now also seen in thyroid cancer.

  • Data from clinical trials demonstrate that active surveillance is an appropriate management strategy for patients with low-risk prostate cancer, and the results from similar trials in those with thyroid cancer are promising.

  • Consensus is needed regarding both the optimal approach to patient selection for active surveillance and the most appropriate active surveillance scheduling and monitoring strategies.

  • More specific methods of stratifying patients by risk, before consideration for active surveillance, are needed.

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Fig. 1: Incidence rates and mortality associated with prostate and thyroid cancers in the USA, per 100,000 persons, 1980–2015.
Fig. 2: Follow-up monitoring schedules from ongoing prostate cancer active surveillance programmes.

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References

  1. Carter, S. M. et al. The challenge of overdiagnosis begins with its definition. BMJ 350, h869 (2015).

    Article  CAS  PubMed  Google Scholar 

  2. US Preventive Services Task Force. Screening for prostate cancer: US Preventive Services Task Force recommendation statement. JAMA 319, 1901–1913 (2018).

    Article  Google Scholar 

  3. Resnick, M. J. et al. Long-term functional outcomes after treatment for localized prostate cancer. N. Engl. J. Med. 368, 436–445 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Donovan, J. L. et al. Patient-reported outcomes after monitoring, surgery, or radiotherapy for prostate cancer. N. Engl. J. Med. 375, 1425–1437 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Wilt, T. J., Andriole, G. L. & Brawer, M. K. Prostatectomy versus observation for early prostate cancer. N. Engl. J. Med. 377, 1302–1303 (2017).

    Article  PubMed  Google Scholar 

  6. Cooperberg, M. R. & Carroll, P. R. Trends in management for patients with localized prostate cancer, 1990–2013. JAMA 314, 80–82 (2015).

    Article  CAS  PubMed  Google Scholar 

  7. Barocas, D. A. et al. What percentage of patients with newly diagnosed carcinoma of the prostate are candidates for surveillance? An analysis of the CaPSURE database. J. Urol. 180, 1330–1334; discussion 1334–1335 (2008).

    Article  PubMed  Google Scholar 

  8. Davies, L. & Welch, H. G. Current thyroid cancer trends in the United States. JAMA Otolaryngol. Head Neck Surg. 140, 317–322 (2014).

    Article  PubMed  Google Scholar 

  9. Sun, F. et al. Therapies for Clinically Localized Prostate Cancer: Update of a 2008 Systematic Review (Agency for Healthcare Research and Quality, Rockville, MD, 2014).

    Google Scholar 

  10. Hamdy, F. C. et al. 10-year outcomes after monitoring, surgery, or radiotherapy for localized prostate cancer. N. Engl. J. Med. 375, 1415–1424 (2016).

    Article  PubMed  Google Scholar 

  11. Wilt, T. J. et al. Radical prostatectomy versus observation for localized prostate cancer. N. Engl. J. Med. 367, 203–213 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Wilt, T. J. Management of low risk and low PSA prostate cancer: long term results from the Prostate Cancer Intervention Versus Observation Trial. Recent Results Cancer Res. 202, 149–169 (2014).

    Article  PubMed  Google Scholar 

  13. Wilt, T. J. The Prostate Cancer Intervention Versus Observation Trial:VA/NCI/AHRQ Cooperative Studies Program #407 (PIVOT): design and baseline results of a randomized controlled trial comparing radical prostatectomy with watchful waiting for men with clinically localized prostate cancer. J. Natl. Cancer Inst. Monographs 2012, 184–190 (2012).

    Article  Google Scholar 

  14. Ito, Y. et al. Patient age is significantly related to the progression of papillary microcarcinoma of the thyroid under observation. Thyroid 24, 27–34 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Miyauchi, A. Clinical trials of active surveillance of papillary microcarcinoma of the thyroid. World J. Surg. 40, 516–522 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Sugitani, I. & Fujimoto, Y. Management of low-risk papillary thyroid carcinoma: unique conventional policy in Japan and our efforts to improve the level of evidence. Surg. Today 40, 199–215 (2010).

    Article  PubMed  Google Scholar 

  17. Sugitani, I. et al. Three distinctly different kinds of papillary thyroid microcarcinoma should be recognized: our treatment strategies and outcomes. World J. Surg. 34, 1222–1231 (2010).

    Article  PubMed  Google Scholar 

  18. Bruinsma, S. M. et al. Active surveillance for prostate cancer: a narrative review of clinical guidelines. Nat. Rev. Urol. 13, 151–167 (2016).

    Article  CAS  PubMed  Google Scholar 

  19. Loeb, S. et al. Active surveillance for prostate cancer: a systematic review of clinicopathologic variables and biomarkers for risk stratification. Eur. Urol. 67, 619–626 (2015).

    Article  PubMed  Google Scholar 

  20. National Cancer Institute. Cancer Stat Facts: prostate cancer. SEER https://seer.cancer.gov/statfacts/html/prost.html (2018).

  21. Fenton, J. J. et al. Prostate-Specific Antigen–Based Screening for Prostate Cancer: a Systematic Evidence Review for the U. S. Preventive Services Task Force (Agency for Healthcare Research and Quality, Rockville, MD, 2018).

    Book  Google Scholar 

  22. Global Burden of Disease Cancer Collaboration. The global burden of cancer 2013. JAMA Oncol. 1, 505–527 (2015).

    Article  PubMed Central  Google Scholar 

  23. Haas, G. P., Delongchamps, N., Brawley, O. W., Wang, C. Y. & de la Roza, G. The worldwide epidemiology of prostate cancer: perspectives from autopsy studies. Can. J. Urol. 15, 3866–3871 (2008).

    PubMed  PubMed Central  Google Scholar 

  24. Meyer, M. S. et al. Homogeneous prostate cancer mortality in the Nordic countries over four decades. Eur. Urol. 58, 427–432 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Jemal, A., Siegel, R., Xu, J. & Ward, E. Cancer statistics, 2010. CA Cancer J. Clin. 60, 277–300 (2010).

    Article  PubMed  Google Scholar 

  26. Moyer, V. A. & US Preventive Services Task Force. Screening for prostate cancer: U. S. Preventive Services Task Force recommendation statement. Ann. Intern. Med. 157, 120–134 (2012).

    Article  PubMed  Google Scholar 

  27. Fleshner, K., Carlsson, S. V. & Roobol, M. J. The effect of the USPSTF PSA screening recommendation on prostate cancer incidence patterns in the USA. Nat. Rev. Urol. 14, 26 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. American Cancer Society. Prostate cancer prevention and early detection. cancer.org https://www.cancer.org/cancer/prostate-cancer/early-detection/acs-recommendations.html (2016).

  29. Basch, E. et al. Screening for prostate cancer with prostate-specific antigen testing: American Society of Clinical Oncology provisional clinical opinion. J. Clin. Oncol. 30, 3020–3025 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Carter, H. B. et al. Early detection of prostate cancer: AUA Guideline. J. Urol. 190, 419–426 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Qaseem, A. et al. Screening for prostate cancer: a guidance statement from the Clinical Guidelines Committee of the American College of Physicians. Ann. Intern. Med. 158, 761–769 (2013).

    Article  PubMed  Google Scholar 

  32. Carroll, P. R. et al. NCCN guidelines insights: prostate cancer early detection, version 2.2016. J. Natl Compr. Canc. Netw. 14, 509–519 (2016).

    Article  PubMed  Google Scholar 

  33. Horwich, A. et al. Prostate cancer: ESMO consensus conference guidelines 2012. Ann. Oncol. 24, 1141–1162 (2013).

    Article  CAS  PubMed  Google Scholar 

  34. Heidenreich, A. et al. EAU guidelines on prostate cancer. Part 1: screening, diagnosis, and local treatment with curative intent — update 2013. Eur. Urol. 65, 124–137 (2014).

    Article  PubMed  Google Scholar 

  35. Pashayan, N. et al. Mean sojourn time, overdiagnosis, and reduction in advanced stage prostate cancer due to screening with PSA: implications of sojourn time on screening. Br. J. Cancer 100, 1198–1204 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Fouad, M. N. et al. Comorbidity independently predicted death in older prostate cancer patients, more of whom died with than from their disease. J. Clin. Epidemiol. 57, 721–729 (2004).

    Article  PubMed  Google Scholar 

  37. Loeb, S. et al. Overdiagnosis and overtreatment of prostate cancer. Eur. Urol. 65, 1046–1055 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Etzioni, R., Gulati, R., Mallinger, L. & Mandelblatt, J. Influence of study features and methods on overdiagnosis estimates in breast and prostate cancer screening. Ann. Intern. Med. 158, 831–838 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  39. de Gelder, R. et al. Interpreting overdiagnosis estimates in population-based mammography screening. Epidemiol. Rev. 33, 111–121 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Aizer, A. A. et al. Cost implications and complications of overtreatment of low-risk prostate cancer in the United States. J. Natl Compr. Canc. Netw. 13, 61–68 (2015).

    Article  PubMed  Google Scholar 

  41. Heijnsdijk, E. A. et al. Quality-of-life effects of prostate-specific antigen screening. N. Engl. J. Med. 367, 595–605 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Chen, R. C. et al. Active surveillance for the management of localized prostate cancer (Cancer Care Ontario Guideline): American Society of Clinical Oncology clinical practice guideline endorsement. J. Clin. Oncol. 34, 2182–2190 (2016).

    Article  PubMed  Google Scholar 

  43. Sanda, M. G. et al. Clinically localized prostate cancer: AUA/ASTRO/SUO guideline. ProstateCancerReports http://www.prostatecancerreports.org/fulltext/2017/Sanda_MG170000.pdf (2017).

  44. Bokhorst, L. P. et al. A decade of active surveillance in the PRIAS study: an update and evaluation of the criteria used to recommend a switch to active treatment. Eur. Urol. 70, 954–960 (2016).

    Article  PubMed  Google Scholar 

  45. Bul, M. et al. Active surveillance for low-risk prostate cancer worldwide: the PRIAS study. Eur. Urol. 63, 597–603 (2013).

    Article  PubMed  Google Scholar 

  46. Tosoian, J. J. et al. Intermediate and longer-term outcomes from a prospective active-surveillance program for favorable-risk prostate cancer. J. Clin. Oncol. 33, 3379–3385 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Tosoian, J. J. et al. Active surveillance program for prostate cancer: an update of the Johns Hopkins experience. J. Clin. Oncol. 29, 2185–2190 (2011).

    Article  PubMed  Google Scholar 

  48. Klotz, L. Active surveillance for prostate cancer: for whom? J. Clin. Oncol. 23, 8165–8169 (2005).

    Article  PubMed  Google Scholar 

  49. Klotz, L. et al. Long-term follow-up of a large active surveillance cohort of patients with prostate cancer. J. Clin. Oncol. 33, 272–277 (2015).

    Article  PubMed  Google Scholar 

  50. Klotz, L. et al. Clinical results of long-term follow-up of a large, active surveillance cohort with localized prostate cancer. J. Clin. Oncol. 28, 126–131 (2010).

    Article  PubMed  Google Scholar 

  51. Whitson, J. M. et al. The relationship between prostate specific antigen change and biopsy progression in patients on active surveillance for prostate cancer. J. Urol. 185, 1656–1660 (2011).

    Article  PubMed  Google Scholar 

  52. Welty, C. J. et al. Extended followup and risk factors for disease reclassification in a large active surveillance cohort for localized prostate cancer. J. Urol. 193, 807–811 (2015).

    Article  PubMed  Google Scholar 

  53. Cooperberg, M. R., Broering, J. M. & Carroll, P. R. Risk assessment for prostate cancer metastasis and mortality at the time of diagnosis. J. Natl Cancer Inst. 101, 878–887 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Soloway, M. S. et al. Careful selection and close monitoring of low-risk prostate cancer patients on active surveillance minimizes the need for treatment. Eur. Urol. 58, 831–835 (2010).

    Article  PubMed  Google Scholar 

  55. Adamy, A. et al. Role of prostate specific antigen and immediate confirmatory biopsy in predicting progression during active surveillance for low risk prostate cancer. J. Urol. 185, 477–482 (2011).

    Article  PubMed  Google Scholar 

  56. Davis, J. W. et al. Disease reclassification risk with stringent criteria and frequent monitoring in men with favourable-risk prostate cancer undergoing active surveillance. BJU Int. 118, 68–76 (2016).

    Article  PubMed  Google Scholar 

  57. Kakehi, Y. et al. Prospective evaluation of selection criteria for active surveillance in Japanese patients with stage T1cN0M0 prostate cancer. Jpn J. Clin. Oncol. 38, 122–128 (2008).

    Article  PubMed  Google Scholar 

  58. Lin, D. W. et al. Urinary TMPRSS2:ERG and PCA3 in an active surveillance cohort: results from a baseline analysis in the Canary Prostate Active Surveillance Study. Clin. Cancer Res. 19, 2442–2450 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Newcomb, L. F. et al. Outcomes of active surveillance for clinically localized prostate cancer in the prospective, multi-institutional Canary PASS cohort. J. Urol. 195, 313–320 (2016).

    Article  PubMed  Google Scholar 

  60. van den Bergh, R. C. et al. Outcomes of men with screen-detected prostate cancer eligible for active surveillance who were managed expectantly. Eur. Urol. 55, 1–8 (2009).

    Article  PubMed  Google Scholar 

  61. Schroder, F. H. et al. Screening and prostate cancer mortality: results of the European Randomised Study of Screening for Prostate Cancer (ERSPC) at 13 years of follow-up. Lancet 384, 2027–2035 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Godtman, R. A. et al. Long-term results of active surveillance in the Goteborg randomized, population-based prostate cancer screening trial. Eur. Urol. 70, 760–766 (2016).

    Article  PubMed  Google Scholar 

  63. Loeb, S. et al. Five-year nationwide follow-up study of active surveillance for prostate cancer. Eur. Urol. 67, 233–238 (2015).

  64. Selvadurai, E. D. et al. Medium-term outcomes of active surveillance for localised prostate cancer. Eur. Urol. 64, 981–987 (2013).

  65. Tosoian, J. J., Carter, H. B., Lepor, A. & Loeb, S. Active surveillance for prostate cancer: current evidence and contemporary state of practice. Nat. Rev. Urol. 13, 205–215 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Kinsella, N. et al. Active surveillance for prostate cancer: a systematic review of contemporary worldwide practices. Transl Androl. Urol. 7, 83–97 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Bruinsma, S. M. et al. The Movember Foundation’s GAP3 cohort: a profile of the largest global prostate cancer active surveillance database to date. BJU Int. 121, 737–744 (2018).

    Article  PubMed  Google Scholar 

  68. Inoue, L. Y. T. et al. Comparative analysis of biopsy upgrading in four prostate cancer active surveillance cohorts. Ann. Intern. Med. 168, 1–9 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  69. Gleason, D. F. Classification of prostatic carcinomas. Cancer Chemother. Rep. 50, 125–128 (1966).

    CAS  PubMed  Google Scholar 

  70. Gleason, D. F. & Mellinger, G. T. Prediction of prognosis for prostatic adenocarcinoma by combined histological grading and clinical staging. J. Urol. 111, 58–64 (1974).

    Article  CAS  PubMed  Google Scholar 

  71. Mellinger, G. T. Prognosis of prostatic carcinoma. Recent Results Cancer Res. 60, 61–72 (1977).

    Article  Google Scholar 

  72. Gleason, D. F. & Mellinger, G. T., Veterans Administration Cooperative Urological Research Group. Prediction of prognosis for prostatic adenocarcinoma by combined histological grading and clinical staging. J. Urol. 167, 953–958; discussion 959 (2002).

    Article  PubMed  Google Scholar 

  73. Montironi, R. et al. Original Gleason system versus 2005 ISUP modified Gleason system: the importance of indicating which system is used in the patient’s pathology and clinical reports. Eur. Urol. 58, 369–373 (2010).

    Article  PubMed  Google Scholar 

  74. Epstein, J. I., Allsbrook, W. C. Jr., Amin, M. B. & Egevad, L. L., ISUP Grading Committee. The 2005 International Society of Urological Pathology (ISUP) Consensus Conference on Gleason grading of prostatic carcinoma. Am. J. Surg. Pathol. 29, 1228–1242 (2005).

    Article  PubMed  Google Scholar 

  75. Epstein, J. I. et al. The 2014 International Society of Urological Pathology (ISUP) Consensus Conference on Gleason grading of prostatic carcinoma: definition of grading patterns and proposal for a new grading system. Am. J. Surg. Pathol. 40, 244–252 (2016).

    Article  PubMed  Google Scholar 

  76. Epstein, J. I. et al. A contemporary prostate cancer grading system: a validated alternative to the Gleason score. Eur. Urol. 69, 428–435 (2016).

    Article  PubMed  Google Scholar 

  77. Humphrey, P. A., Moch, H., Cubilla, A. L., Ulbright, T. M. & Reuter, V. E. The 2016 WHO classification of tumours of the urinary system and male genital organs — Part B: prostate and bladder tumours. Eur. Urol. 70, 106–119 (2016).

    Article  PubMed  Google Scholar 

  78. Nelson, W. G., De Marzo, A. M. & Isaacs, W. B. Prostate cancer. N. Engl. J. Med. 349, 366–381 (2003).

    Article  CAS  PubMed  Google Scholar 

  79. Pichon, A. et al. Preoperative low serum testosterone is associated with high-grade prostate cancer and an increased Gleason score upgrading. Prostate Cancer Prostatic Dis. 18, 382–387 (2015).

    Article  CAS  Google Scholar 

  80. Schatzl, G. et al. Association of polymorphisms within androgen receptor, 5α-reductase, and PSA genes with prostate volume, clinical parameters, and endocrine status in elderly men. Prostate 52, 130–138 (2002).

    Article  CAS  PubMed  Google Scholar 

  81. Chodak, G. W. et al. Nuclear localization of androgen receptor in heterogeneous samples of normal, hyperplastic and neoplastic human prostate. J. Urol. 147, 798–803 (1992).

    Article  CAS  PubMed  Google Scholar 

  82. Lee, D. K. & Chang, C. Endocrine mechanisms of disease: expression and degradation of androgen receptor: mechanism and clinical implication. J. Clin. Endocrinol. Metab. 88, 4043–4054 (2003).

    Article  CAS  PubMed  Google Scholar 

  83. Takeda, H. et al. Androgen receptor content of prostate carcinoma cells estimated by immunohistochemistry is related to prognosis of patients with stage D2 prostate carcinoma. Cancer 77, 934–940 (1996).

    Article  CAS  PubMed  Google Scholar 

  84. Khera, M., Crawford, D., Morales, A., Salonia, A. & Morgentaler, A. A new era of testosterone and prostate cancer: from physiology to clinical implications. Eur. Urol. 65, 115–123 (2014).

    Article  CAS  PubMed  Google Scholar 

  85. Weischenfeldt, J. et al. Integrative genomic analyses reveal an androgen-driven somatic alteration landscape in early-onset prostate cancer. Cancer Cell 23, 159–170 (2013).

    Article  CAS  PubMed  Google Scholar 

  86. Demichelis, F., Garraway, L. A. & Rubin, M. A. Molecular archeology: unearthing androgen-induced structural rearrangements in prostate cancer genomes. Cancer Cell 23, 133–135 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Sowalsky, A. G., Ye, H., Bubley, G. J. & Balk, S. P. Clonal progression of prostate cancers from Gleason grade 3 to grade 4. Cancer Res. 73, 1050–1055 (2013).

    Article  CAS  PubMed  Google Scholar 

  88. Pritchard, C. C. et al. Inherited DNA-repair gene mutations in men with metastatic prostate cancer. N. Engl. J. Med. 375, 443–453 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Sanchez, D. et al. Androgen receptor mutations are associated with Gleason score in localized prostate cancer. BJU Int. 98, 1320–1325 (2006).

    Article  CAS  PubMed  Google Scholar 

  90. Gallagher, D. J. et al. Germline BRCA mutations denote a clinicopathologic subset of prostate cancer. Clin. Cancer Res. 16, 2115–2121 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Boutros, P. C. et al. Spatial genomic heterogeneity within localized, multifocal prostate cancer. Nat. Genet. 47, 736–745 (2015).

    Article  CAS  PubMed  Google Scholar 

  92. Agoulnik, I. U. et al. Role of SRC-1 in the promotion of prostate cancer cell growth and tumor progression. Cancer Res. 65, 7959–7967 (2005).

    Article  CAS  PubMed  Google Scholar 

  93. Gundem, G. et al. The evolutionary history of lethal metastatic prostate cancer. Nature 520, 353–357 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Kumar, A. et al. Substantial interindividual and limited intraindividual genomic diversity among tumors from men with metastatic prostate cancer. Nat. Med. 22, 369–378 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Parton, R. G. & del Pozo, M. A. Caveolae as plasma membrane sensors, protectors and organizers. Nat. Rev. Mol. Cell. Biol. 14, 98–112 (2013).

    Article  CAS  PubMed  Google Scholar 

  96. Yang, G., Truong, L. D., Wheeler, T. M. & Thompson, T. C. Caveolin-1 expression in clinically confined human prostate cancer: a novel prognostic marker. Cancer Res. 59, 5719–5723 (1999).

    CAS  PubMed  Google Scholar 

  97. Tahir, S. A. et al. Development of an immunoassay for serum caveolin-1: a novel biomarker for prostate cancer. Clin. Cancer Res. 9, 3653–3659 (2003).

    CAS  PubMed  Google Scholar 

  98. Gumulec, J. et al. Caveolin-1 as a potential high-risk prostate cancer biomarker. Oncol. Rep. 27, 831–841 (2012).

    CAS  PubMed  Google Scholar 

  99. Tahir, S. A. et al. Preoperative serum caveolin-1 as a prognostic marker for recurrence in a radical prostatectomy cohort. Clin. Cancer Res. 12, 4872–4875 (2006).

    Article  CAS  PubMed  Google Scholar 

  100. Basourakos, S. P. et al. Baseline and longitudinal plasma caveolin-1 level as a biomarker in active surveillance for early-stage prostate cancer. BJU Int. 121, 69–76 (2018).

    Article  CAS  PubMed  Google Scholar 

  101. Yang, G. et al. Caveolin-1 upregulation contributes to c-Myc-induced high-grade prostatic intraepithelial neoplasia and prostate cancer. Mol. Cancer Res. 10, 218–229 (2012).

    Article  CAS  PubMed  Google Scholar 

  102. Kretschmer, A. & Tilki, D. Biomarkers in prostate cancer — current clinical utility and future perspectives. Crit. Rev. Oncol. Hematol. 120, 180–193 (2017).

    Article  PubMed  Google Scholar 

  103. Lin, J. S., Bowles, E. J. A., Williams, S. B. & Morrison, C. C. Screening for thyroid cancer updated evidence report and systematic review for the US Preventive Services Task Force. JAMA 317, 1888–1903 (2017).

    Article  PubMed  Google Scholar 

  104. Jemal, A. et al. Global cancer statistics. CA Cancer J. Clin. 61, 69–90 (2011).

    Article  PubMed  Google Scholar 

  105. US Preventive Services Task Force. Screening for thyroid cancer: U. S. Preventive Services Task Force recommendation statement. JAMA 317, 1882–1887 (2017).

    Article  Google Scholar 

  106. Siegel, R. L., Miller, K. D. & Jemal, A. Cancer statistics, 2015. CA Cancer J. Clin. 65, 5–29 (2015).

    Article  PubMed  Google Scholar 

  107. La Vecchia, C. et al. Author’s reply to thyroid cancer: an epidemic of disease or an epidemic of diagnosis? Int. J. Cancer 136, 2740 (2015).

    Article  CAS  PubMed  Google Scholar 

  108. Hughes, D. T., Haymart, M. R., Miller, B. S., Gauger, P. G. & Doherty, G. M. The most commonly occurring papillary thyroid cancer in the United States is now a microcarcinoma in a patient older than 45 years. Thyroid 21, 231–236 (2011).

    Article  PubMed  Google Scholar 

  109. Davies, L. & Welch, H. G. Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA 295, 2164–2167 (2006).

    Article  CAS  PubMed  Google Scholar 

  110. Horn-Ross, P. L. et al. Continued rapid increase in thyroid cancer incidence in California: trends by patient, tumor, and neighborhood characteristics. Cancer Epidemiol. Biomarkers Prev. 23, 1067–1079 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  111. Malandrino, P. et al. Papillary thyroid microcarcinomas: a comparative study of the characteristics and risk factors at presentation in two cancer registries. J. Clin. Endocrinol. Metab. 98, 1427–1434 (2013).

    Article  CAS  PubMed  Google Scholar 

  112. American Cancer Society. Can thyroid cancer be found early? cancer.org https://www.cancer.org/cancer/thyroid-cancer/detection-diagnosis-staging/detection.html (2016).

  113. Haugen, B. R. et al. 2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer: the American Thyroid Association Guidelines Task Force on Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid 26, 1–133 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  114. Gharib, H. et al. American Association of Clinical Endocrinologists, American College of Endocrinology, and Associazione Medici Endocrinologi medical guidelines for clinical practice for the diagnosis and management of thyroid nodules — 2016 update. Endocr. Pract. 22, 622–639 (2016).

    Article  PubMed  Google Scholar 

  115. Ridley, J., Ischayek, A., Dubey, V. & Iglar, K. Adult health checkup: update on the Preventive Care Checklist Form©. Can. Fam. Physician 62, 307–313 (2016).

    PubMed  PubMed Central  Google Scholar 

  116. American Academy of Family Physicians. Clinical preventive service recommendation: thyroid cancer. AAFP https://www.aafp.org/patient-care/clinical-recommendations/all/thyroid-cancer.html (2017).

  117. Rad, M. P., Zakavi, S. R., Layegh, P., Khooei, A. & Bahadori, A. Incidental thyroid abnormalities on carotid color Doppler ultrasound: frequency and clinical significance. J. Med. Ultrasound 23, 25–28 (2015).

    Article  Google Scholar 

  118. Nguyen, X. V. et al. Incidental thyroid nodules on CT: evaluation of 2 risk-categorization methods for work-up of nodules. AJNR Am. J. Neuroradiol. 34, 1812–1817 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Soelberg, K. K., Bonnema, S. J., Brix, T. H. & Hegedus, L. Risk of malignancy in thyroid incidentalomas detected by 18F-fluorodeoxyglucose positron emission tomography: a systematic review. Thyroid 22, 918–925 (2012).

    Article  CAS  PubMed  Google Scholar 

  120. Hoang, J. K. et al. Managing incidental thyroid nodules detected on imaging: white paper of the ACR Incidental Thyroid Findings Committee. J. Am. Coll. Radiol 12, 143–150 (2015).

    Article  PubMed  Google Scholar 

  121. Haugen, B. R. et al. American Thyroid Association guidelines on the management of thyroid nodules and differentiated thyroid cancer task force review and recommendation on the proposed renaming of encapsulated follicular variant papillary thyroid carcinoma without invasion to noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Thyroid 27, 481–483 (2017).

    Article  CAS  PubMed  Google Scholar 

  122. Durante, C. et al. The natural history of benign thyroid nodules. JAMA 313, 926–935 (2015).

    Article  CAS  PubMed  Google Scholar 

  123. Takebe, K., Date, M. & Yamamoto, Y. Mass screening for thyroid cancer with ultrasonography. Karkinos 7, 309–317 (1994).

    Google Scholar 

  124. Ahn, H. S. et al. Thyroid cancer screening in South Korea increases detection of papillary cancers with no impact on other subtypes or thyroid cancer mortality. Thyroid 26, 1535–1540 (2016).

    Article  PubMed  Google Scholar 

  125. Lee, Y. S., Lim, H., Chang, H. S. & Park, C. S. Papillary thyroid microcarcinomas are different from latent papillary thyroid carcinomas at autopsy. J. Kor. Med. Sci. 29, 676–679 (2014).

    Article  Google Scholar 

  126. Flynn, M. B., Lyons, K. J., Tarter, J. W. & Ragsdale, T. L. Local complications after surgical resection for thyroid carcinoma. Am. J. Surg. 168, 404–407 (1994).

    Article  CAS  PubMed  Google Scholar 

  127. Hundahl, S. A. et al. Initial results from a prospective cohort study of 5583 cases of thyroid carcinoma treated in the United States during 1996. U. S. and German Thyroid Cancer Study Group. An American College of Surgeons Commission on Cancer Patient Care Evaluation study. Cancer 89, 202–217 (2000).

    Article  CAS  PubMed  Google Scholar 

  128. McMullen, C., Rocke, D. & Freeman, J. Complications of bilateral neck dissection in thyroid cancer from a single high-volume center. JAMA Otolaryngol. Head Neck Surg. 143, 376–381 (2017).

    Article  PubMed  Google Scholar 

  129. Bergenfelz, A. et al. Complications to thyroid surgery: results as reported in a database from a multicenter audit comprising 3,660 patients. Langenbecks Arch. Surg. 393, 667–673 (2008).

    Article  CAS  PubMed  Google Scholar 

  130. Ito, Y. & Miyauchi, A. A therapeutic strategy for incidentally detected papillary microcarcinoma of the thyroid. Nat. Clin. Pract. Endocrinol. Metab. 3, 240–248 (2007).

    Article  PubMed  Google Scholar 

  131. Miyauchi, A. et al. Estimation of the lifetime probability of disease progression of papillary microcarcinoma of the thyroid during active surveillance. Surgery 163, 48–52 (2018).

    Article  PubMed  Google Scholar 

  132. Agrawal, N. et al. Integrated genomic characterization of papillary thyroid carcinoma. Cell 159, 676–690 (2014).

    Article  CAS  PubMed Central  Google Scholar 

  133. Haugen, B. R. 2015 American Thyroid Association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: what is new and what has changed? Cancer 123, 372–381 (2017).

    Article  PubMed  Google Scholar 

  134. Yabuta, T. et al. TERT promoter mutations were not found in papillary thyroid microcarcinomas that showed disease progression on active surveillance. Thyroid 27, 1206–1207 (2017).

    Article  PubMed  Google Scholar 

  135. National Cancer Institute. Cancer Stat Facts: thyroid cancer. SEER https://seer.cancer.gov/statfacts/html/thyro.html (2018).

  136. Lao, C. et al. The cost-effectiveness of active surveillance compared to watchful waiting and radical prostatectomy for low risk localised prostate cancer. BMC Cancer 17, 529 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  137. Becerra, V. et al. Economic evaluation of treatments for patients with localized prostate cancer in Europe: a systematic review. BMC Health Serv. Res. 16, 541 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  138. Brandes, A. et al. Cost-effectiveness of radical prostatectomy, radiation therapy and active surveillance for the treatment of localized prostate cancer - a claims data analysis. Value Health 17, A636–A637 (2014).

    Article  CAS  PubMed  Google Scholar 

  139. Lang, B. H. & Wong, C. K. A cost-effectiveness comparison between early surgery and non-surgical approach for incidental papillary thyroid microcarcinoma. Eur. J. Endocrinol. 173, 367–375 (2015).

    Article  CAS  PubMed  Google Scholar 

  140. Venkatesh, S. et al. Cost-effectiveness of active surveillance versus hemithyroidectomy for micropapillary thyroid cancer. Surgery 161, 116–126 (2017).

    Article  PubMed  Google Scholar 

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Acknowledgements

The work from the authors is supported in part by a Cancer Center Support Grant (CA16672) from the National Cancer Institute and National Institutes of Health.

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Author notes

  1. These authors contributed equally: Lisa M. Lowenstein, Spyridon P. Basourakos.

Authors and Affiliations

  1. Department of Health Services Research, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    Lisa M. Lowenstein

  2. Department of Urology, New York Presbyterian Hospital/Weill Cornell Medical Center, New York, NY, USA

    Spyridon P. Basourakos

  3. Department of Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    Michelle D. Williams & Patricia Troncoso

  4. Department of Urology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    Justin R. Gregg

  5. Department of Genitourinary Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    Timothy C. Thompson & Jeri Kim

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Contributions

L.M.L., S.P.B., M.D.W. and J.K. researched data for this manuscript, all authors made a substantial contribution to discussions of content, L.M.L., S.P.B. and J.K. wrote the manuscript and all authors reviewed and/or edited the manuscript before submission.

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Correspondence to Jeri Kim.

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Competing interests

At the time of this work, J.K. was a Professor at the University of Texas MD Anderson Cancer Center. She is now a full-time employee of Merck. L.M.L, S.P.B, M.D.W, P.T., J.R.G. and T.C.T declare no competing interests.

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Lowenstein, L.M., Basourakos, S.P., Williams, M.D. et al. Active surveillance for prostate and thyroid cancers: evolution in clinical paradigms and lessons learned. Nat Rev Clin Oncol 16, 168–184 (2019). https://doi.org/10.1038/s41571-018-0116-x

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