Revisiting surveillance schemes for cancer survivors
Authors: Ø. Holme, M. Bretthauer, M. Løberg, M. Kalager, H.O. Adami
Journal: Annals of Oncology (2019)

Due to population growth, increasing longevity and improved cancer prognosis, the prevalence of cancer survivors will increase substantially over the coming decades. The estimated number of cancer survivors is currently 12.2 million in Europe [1.Lagergren P. Schandl A. Aaronson N.K. et al.Cancer survivorship: an integral part of Europe's research agenda.Mol Oncol. 2019; 13: 624-635Crossref PubMed Scopus (71) Google Scholar] and 15.5 million in the United States with a predicted increase to 26.1 million in 2040 [2.National Cancer Institute. Division of Cancer Control & Population Sciences; https://cancercontrol.cancer.gov/ocs/statistics/statistics.html (10 January 2019, date last accessed).Google Scholar, 3.Shapiro C.L. Cancer survivorship.N Engl J Med. 2018; 379: 2438-2450Crossref PubMed Scopus (256) Google Scholar]. Consequently, in many clinical disciplines, out-patient departments are crowded by a growing number of cancer survivors attending for their routine surveillance visits. Over many years, these surveillance schemes—based on expert opinion rather than scientific evidence [3.Shapiro C.L. Cancer survivorship.N Engl J Med. 2018; 379: 2438-2450Crossref PubMed Scopus (256) Google Scholar]—have remained mostly unchanged. They will consume a rapidly increasing share of already constrained health care resources. Hence, if surveillance could be less resource-consuming with equal or better patient outcome, the potential gains might be substantial. We are confident that the noble principle of doing good but no harm guided the establishment of regular, often life-long surveillance of patients diagnosed and treated for cancer. Laboratory tests and use of imaging techniques are often part of these schemes. But we are also convinced that accumulated scientific evidence now allows a more critical review of the potential harms and benefits of routine surveillance in cancer survivors. Numerous guidelines do indeed recommend surveillance after primary cancer treatment with a curative intent despite lack of evidence for a survival benefit. Surveillance schemes for colorectal cancer have been most extensively studied. A recent Cochrane review [4.Jeffery M. Hickey B. Hider P. See A.M. Follow-up strategies for patients treated for non-metastatic colorectal cancer.Cochrane Database Syst Rev. 2016; 11: CD002200PubMed Google Scholar] and a large randomized trial [5.Wille-Jorgensen P. Syk I. Smedh K. et al.Effect of more vs less frequent follow-up testing on overall and colorectal cancer-specific mortality in patients with stage II or III colorectal cancer: the COLOFOL randomized clinical trial.JAMA. 2018; 319: 2095-2103Crossref PubMed Scopus (119) Google Scholar] found no difference between standard and less-intensive surveillance programs, neither in disease-specific nor in all-cause mortality. Surveillance for breast cancer has also been tested in randomized trials, with no documented survival benefit following intensive vs. less frequent follow-up [6.Moschetti I. Cinquini M. Lambertini M. et al.Follow-up strategies for women treated for early breast cancer.The Cochrane Database Syst Rev. 2016; 5: CD001768Google Scholar]. Follow-up of lung-cancer patients every 3–6 months in the first year after treatment, including regular computed tomography scanning, has been advocated [7.Vansteenkiste J. Crino L. Dooms C. et al.2nd ESMO Consensus Conference on Lung Cancer: early-stage non-small-cell lung cancer consensus on diagnosis, treatment and follow-up.Ann Oncol. 2014; 25: 1462-1474Abstract Full Text Full Text PDF PubMed Scopus (322) Google Scholar]. Risk of false-positive findings is, however, substantial. In one study, 25% of lung-cancer survivors had a false-positive computed tomography scan [8.Lou F. Huang J. Sima C.S. et al.Patterns of recurrence and second primary lung cancer in early-stage lung cancer survivors followed with routine computed tomography surveillance.J Thorac Cardiovasc Surg. 2013; 145: 75-81Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar], but well-designed randomized trials of surveillance after lung-cancer treatment have never been conducted [7.Vansteenkiste J. Crino L. Dooms C. et al.2nd ESMO Consensus Conference on Lung Cancer: early-stage non-small-cell lung cancer consensus on diagnosis, treatment and follow-up.Ann Oncol. 2014; 25: 1462-1474Abstract Full Text Full Text PDF PubMed Scopus (322) Google Scholar]. To the best of our knowledge, no solid evidence supports that the goals of surveillance for presumably cured cancer patients are better achieved by fixed schemes than by more flexible, patient-driven alternatives. In addition, with the current frequent and fixed surveillance schemes, many patients experience anxiety that the next check-up will reveal something concerning [9.Thompson C.A. Charlson M.E. Schenkein E. et al.Surveillance CT scans are a source of anxiety and fear of recurrence in long-term lymphoma survivors.Ann Oncol. 2010; 21: 2262-2266Abstract Full Text Full Text PDF PubMed Scopus (132) Google Scholar, 10.Cupit-Link M. Syrjala K.L. Hashmi S.K. Damocles' syndrome revisited: update on the fear of cancer recurrence in the complex world of today's treatments and survivorship.Hematol Oncol Stem Cell Ther. 2018; 11: 129-134Crossref PubMed Scopus (26) Google Scholar]. When nothing worrisome is discovered, the relief may be only transient. Novel diagnostic technologies to detect cancer recurrence are constantly introduced to the health care system. It is now well-documented for several malignancies that these tools increase overdiagnosis of non-lethal disease that would not otherwise surface during the individual's remaining lifetime [11.Kalager M. Adami H.O. Bretthauer M. Tamimi R.M. Overdiagnosis of invasive breast cancer due to mammography screening: results from the Norwegian screening program.Ann Intern Med. 2012; 156: 491-499Crossref PubMed Scopus (188) Google Scholar, 12.Loeb S. Bjurlin M.A. Nicholson J. et al.Overdiagnosis and overtreatment of prostate cancer.Eur Urol. 2014; 65: 1046-1055Abstract Full Text Full Text PDF PubMed Scopus (583) Google Scholar, 13.Park S. Oh C.M. Cho H. et al.Association between screening and the thyroid cancer "epidemic" in South Korea: evidence from a nationwide study.BMJ. 2016; 355: i5745.Crossref PubMed Scopus (144) Google Scholar]. But these technologies–including tumor markers, circulating cancer cells and particularly the increasingly sensitive imaging techniques—will also change the landscape of cancer surveillance. They extend the lead time because recurrences are detected earlier which conveys an unproven and biologically questionable benefit. Hence, intense surveillance may in fact be harmful, due to overdiagnosis and unnecessary treatment [4.Jeffery M. Hickey B. Hider P. See A.M. Follow-up strategies for patients treated for non-metastatic colorectal cancer.Cochrane Database Syst Rev. 2016; 11: CD002200PubMed Google Scholar]. Today, effective, bilateral communication 24 hours per day is possible between patients and health care providers, and the use of mobile devices and wearable technology constantly add new opportunities and layers of sophistication to these interactions. The health care system has been slow in the uptake of these new opportunities to support and monitor cancer survivors—not as a substitute, but as a complement to face-to-face meetings. Many cancer survivors are more likely to die from chronic, often preventable non-communicable disease, rather than from their malignancy. Therefore, lifestyle interventions targeted to each patient's risk profile and personal preferences should be prioritized, aided by novel communication tools as specified in the accompanying table. The practice of oncology would thereby adopt a more holistic approach which might not only improve quality of life but also extend survival. With no documented benefit on cancer survival—and substantial evidence of harm and waste of health care resources—we suggest that rigid surveillance schemes for cancer survivors should be reconsidered and maybe abandoned altogether. As an alternative, we propose on-demand access to a network of specialized health care providers, e.g. specialized nurses. Several studies have shown that patient-initiated surveillance is feasible in breast cancer [14.Brown L. Payne S. Royle G. Patient initiated follow up of breast cancer.Psychooncology. 2002; 11: 346-355Crossref PubMed Scopus (80) Google Scholar] and endometrial cancer [15.Jeppesen M.M. Jensen P.T. Hansen D.G. et al.Patient-initiated follow up affects fear of recurrence and healthcare use: a randomised trial in early-stage endometrial cancer.BJOG. 2018; 125: 1705-1714Crossref PubMed Scopus (27) Google Scholar]. Studies are underway for rectal cancer [16.Hovdenak Jakobsen I. Juul T. Bernstein I. et al.Follow-up after rectal cancer: developing and testing a novel patient-led follow-up program. Study protocol.Acta Oncol. 2017; 56: 307-313Crossref PubMed Scopus (12) Google Scholar]. Each provider is in charge of, and closely interacting with, a defined cohort of cancer survivors. The patient takes the driver's seat as long as their health and well-being permits. We suggest introduction of new distinct components of the patient–provider partnership, as outlined in in Table 1.Table 1Features of patient-driven surveillance for cancer survivors, to replace current fixed surveillance schemesFeatureContentEasy, fast and streamlined access to specialized health careWhenever a cancer survivor has questions, concerns or wants an appointment with his/her doctor, contact with the provider through should be the first step. We believe that in the next phase—an experienced provider will resolve the majority of issues that arise during follow-up. Whenever consultation with the doctor is needed or requested by the patient, optimizing continuity is the highest priority. To meet the same doctor is indeed a central goal of a flexible patient-driven surveillance system.Monitoring health using smart toolsUse of smartphones and wearable technology for close interaction between the patient and the health care system should help providers to monitor quality of life, disease symptoms and lifestyle interventions with a much deeper level of resolution than has traditionally been within reach. We believe in a highly optimized management of cancer survivors in terms of pain relief, psychosocial support, doctors' appointment and use of diagnostic tools.Lifestyle interventions to improve quality of life and reduce overall mortalityLifestyle intervention is the second key component of our proposed surveillance scheme. The goal is to improve quality of life and extend the overall survival. This intervention must accommodate the patients age, health status, risk factor profile, psychosocial situation and preferences. Patients may select priorities from a laundry list of relevant interventions. But we foresee that electronic applications that have survived proper scientific scrutiny will rapidly offer the most efficient, sustainable and cost-effective tool to promote a healthy life.Integrated terminal careThe health status of virtually all humans deteriorate before they die and this unavoidably applies to those with an incurable cancer. We propose as a final key mission for the provider to be in charge of a timely and competent planning of terminal care in close cooperation with the patient and relatives. Open table in a new tab Although considered also by others [3.Shapiro C.L. Cancer survivorship.N Engl J Med. 2018; 379: 2438-2450Crossref PubMed Scopus (256) Google Scholar, 17.Shah M. Denlinger C.S. Optimal post-treatment surveillance in cancer survivors: is more really better?.Oncology. 2015; 29: 230-240PubMed Google Scholar, 18.Whear R. Abdul-Rahman A.K. Boddy K. et al.The clinical effectiveness of patient initiated clinics for patients with chronic or recurrent conditions managed in secondary care: a systematic review.PLoS One. 2013; 8: e74774Crossref PubMed Scopus (17) Google Scholar], our proposed change in surveillance of cancer survivors may appear provocative. Professional—and in some settings even financial—interests might be challenged due to reduced volumes of out-patient visits, less use of imaging techniques and fewer opportunities for surgical resection of, for example, liver metastases. Any change in clinical practice that have prevailed dogmatically for many decades will indeed likely create resistance. Hence, barriers to implementation are likely substantial, but so are the potential gains for patients, doctors and health care systems. The potential benefits of our proposed changes need to be tested and quantified in properly designed randomized trials, ideally with a pragmatic, population-based design that facilitates generalizability of results. We suggest that initiatives of the type proposed herein should take advantage of registry-based clinical trial technologies [19.Mayer-Schönberger V. Cukier K. Big Data: A Revolution That Will Transform How we Live, Work and Think. John Murray, London2013Google Scholar]. Within reach is indeed collection of an overwhelming amount of data that characterize the consequences of a cancer diagnosis and its treatment both for patients and their caregivers. These data will likely allow more evidence-based management of cancer patients. They might be used to develop prediction models to guide a more individualized surveillance, and new research hypotheses will unavoidably arise. In conclusion, we believe the time is ripe to reconsider the management of cancer survivors. It is time to move from a rigid, non-evidence based to a patient-driven surveillance with adequate scientific testing. If modern communication tools are used properly and our hypotheses are realistic, management of cancer survivors would change dramatically entailing improved quality of life, more cost-effective use of health care resources—and perhaps—prolonged survival. None declared.