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Follow-up strategy and survival for five common cancers: A meta-analysis

Open AccessPublished:August 26, 2022DOI:https://doi.org/10.1016/j.ejca.2022.07.025

      Highlights

      • Intensive follow-up after surgery for colorectal and breast cancer has little impact on survival.
      • Colorectal cancer recurrences are more often treated locally after intensive follow-up.
      • High quality research on follow-up for other cancers is scarce.

      Abstract

      Background

      This meta-analysis aimed to evaluate the effectiveness of intensive follow-up after curative intent treatment for five common solid tumours, in terms of survival and treatment of recurrences.

      Methods

      A systematic literature search was conducted, identifying comparative studies on follow-up for colorectal, lung, breast, upper gastro-intestinal and prostate cancer. Outcomes of interest were overall survival (OS), cancer specific survival (CSS), and treatment of recurrences. Random effects meta-analyses were conducted, with particular focus on studies at low risk of bias.

      Results

      Fourteen out of 63 studies were considered to be at low risk of bias (8 colorectal, 4 breast, 0 lung, 1 upper gastro-intestinal, 1 prostate). These studies showed no significant impact of intensive follow-up on OS (hazard ratio, 95% confidence interval) for colorectal (0.99; 0.92–1.06), breast 1.06 (0.92–1.23), upper gastro-intestinal (0.78; 0.51–1.19) and prostate cancer (1.00; 0.86–1.16). No impact on CSS (hazard ratio, 95% confidence interval) was found for colorectal cancer (0.94; 0.77–1.16). CSS was not reported for other cancer types. Intensive follow-up increased the rate of curative treatment (relative risk; 95% confidence interval) for colorectal cancer recurrences (1.30; 1.05–1.61), but not for upper gastro-intestinal cancer recurrences (0.92; 0.47–1.81). For the other cancer types, no data on treatment of recurrences was available in low risk studies.

      Conclusion

      For colorectal and breast cancer, high quality studies do not suggest an impact of intensive follow-up strategies on survival. Colorectal cancer recurrences are more often treated locally after intensive follow-up. For other cancer types evaluated, limited high quality research on follow-up is available.

      Keywords

      1. Introduction

      Most cancer survivors receive regular follow-up care after being treated with curative intent. Traditionally, follow-up is performed for a period of 5 years or longer for most types of solid tumours. Guidelines differ between tumour types, but generally advocate regular hospital visits, imaging, and serum tumour marker measurements when available [
      • Cardoso R.
      • Coburn N.G.
      • Seevaratnam R.
      • Mahar A.
      • Helyer L.
      • Law C.
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      A systematic review of patient surveillance after curative gastrectomy for gastric cancer: a brief review.
      ,
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      • Keupers M.
      • Soens J.
      • Lavens M.
      • Postema S.
      • Van Ongeval C.
      Breast imaging surveillance after curative treatment for primary non-metastasised breast cancer in non-high-risk women: a systematic review.
      ,
      • van der Stok E.P.
      • Spaander M.C.W.
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      • Verhoef C.
      • Kuipers E.J.
      Surveillance after curative treatment for colorectal cancer.
      ,
      • Schmidt-Hansen M.
      • Baldwin D.R.
      • Hasler E.
      What is the most effective follow-up model for lung cancer patients? A systematic review.
      ].
      The main rationale behind oncologic follow-up is to detect metastases or novel primary tumours early, since prompt treatment of cancer relapses is deemed important for the likelihood of cure and survival. Next to this, follow-up can be used to address patients’ needs with regards to psychosocial counselling, to evaluate treatment effects and complications, and to inform patients on their disease status and risk of recurrence [
      • Brandenbarg D.
      • Berendsen A.J.
      • de Bock G.H.
      Patients' expectations and preferences regarding cancer follow-up care.
      ].
      The debate surrounding oncological follow-up practices has existed for many years. It is associated with a considerable use of hospital resources and costs, may have impact on quality of life, while the effect of follow-up intensity on survival outcomes remains equivocal [
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      • Siegel D.
      The utility of follow-up testing after curative cancer therapy. A critical review and economic analysis.
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      Economic burden of cancer survivorship among adults in the United States.
      ]. Given that the number of cancer survivors will continue to grow [
      Surveillance Research Program DoCCaPSNational Cancer Institute
      Cancer treatment & survivorship.
      ], improvements of follow-up practices should be pursued. Many studies evaluate the effectiveness of follow-up for individual tumours types, but a broad oncological perspective remains lacking.
      We therefore sought to systematically assess and meta-analyse available literature on follow-up after curative intent treatment for five types of solid tumours (colorectal, lung, breast, upper gastro-intestinal, and prostate cancers) in order to determine the impact of different follow-up strategies on survival outcomes and treatment of recurrent disease.

      2. Methods

      2.1 Search strategy

      This study was performed in line with the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analysis, www.prisma-statement.org) guidelines. Pubmed/MEDLINE, Embase, Web of Science, the Cochrane database, and Google Scholar were systematically searched for studies published prior to the 12th of May 2020. The search terms are provided in supplementary table A.1. Reference lists from eligible articles were also reviewed to identify additional publi-cations.

      2.2 Study selection

      Screening for eligible studies was performed by two authors (BG, DH), independently. Studies were included when comparing follow-up approaches after curative intent treatment for colorectal, lung, breast, upper gastro-intestinal or prostate cancer, in light of overall survival (OS) or cancer specific survival (CSS) outcomes. Treatment intent for recurrent disease (i.e. curative or palliative) was also evaluated. Both randomised controlled trials (RCTs) and observational studies (cohort and case–control) were considered. Inclusion was restricted to articles written in English. Non-original studies (e.g. reviews, editorials) were excluded, as were non-comparative studies and studies using simulation techniques (e.g. Markov modelling).

      2.3 Data extraction and presentation

      Data were extracted by two reviewers (BG, DH), independently. Studies were categorised based on the aspect of follow-up evaluated, being the frequency of testing, setting of follow-up (e.g. in-hospital or general practitioner), diagnostic modalities used, or a combination of the aforementioned categories. Data on survival (hazard ratios (HR) including 95% confidence intervals (95% CI) for OS and CSS) and the probability of treatment with curative intent for recurrent disease (relative risk (RR) including 95% CI) were collected. When no ratios were reported, data were extracted from Kaplan–Meier figures, tables, and text. Multi-layered circle plots were created to visualise all aspects in relation to outcomes and the risk of bias.

      2.4 Quality assessment

      Quality assessment was performed by two reviewers (BG, DH), independently. The Cochrane tools ROBINS-I (for observational studies) and RoB2 (for randomised studies) were used [
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      • Reeves B.C.
      • Savović J.
      • Berkman N.D.
      • Viswanathan M.
      • et al.
      ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions.
      ,
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      • Moher D.
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      • et al.
      The Cochrane Collaboration's tool for assessing risk of bias in randomised trials.
      ]. Studies were considered to be at low risk of bias when qualified as either ‘low’ to ‘moderate’ using ROBINS-I, or as ‘low risk’ to ‘some concerns’ using RoB2.

      2.5 Quantitative assessment

      A random effects meta-analysis was conducted per tumour type and stratified for study risk of bias, using the generic inverse variance method (survival) or the Mantel-Haenszel method (treatment of recurrences). Methods described by Tierney et al. were applied to calculate log HRs and corresponding standard errors, in case these were not reported [
      • Tierney J.F.
      • Stewart L.A.
      • Ghersi D.
      • Burdett S.
      • Sydes M.R.
      Practical methods for incorporating summary time-to-event data into meta-analysis.
      ]. Both HRs and RRs were reported using the least intensive approach (e.g. lowest frequency, non-hospital setting) as a reference. In studies with multiple groups (i.e. >2 follow-up approaches), the most intensive approaches were combined to create a single pair-wise comparison with the least intensive approach, as recommended by the Cochrane Handbook [
      • Higgins J.P.
      • Green S.
      • Collaboration C.
      Cochrane Handbook for systematic reviews of interventions.
      ]. The R Project for Statistical Computing version 4.1.0 (https://www.r-project.org/) was used for both the statistical analyses and visualisation of the data (packages: meta (v4.18-1), ggplot2 (v3.3.2); circlize (v0.4.11) [
      • Gu Z.
      • Gu L.
      • Eils R.
      • Schlesner M.
      • Brors B.
      Circlize Implements and enhances circular visualization in R.
      ]).

      3. Results

      The screening and selection process is illustrated in Fig. 1. After screening 4538 studies, 167 were screened full-text. Ultimately, 63 studies were deemed eligible for inclusion [
      • Ohlsson B.
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      Association between intensity of posttreatment surveillance testing and detection of recurrence in patients with colorectal cancer.
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      Nonphysician clinicians in the follow-up of resected patients with colorectal cancer.
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      Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program.
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      Optimal surveillance frequency after CRS/HIPEC for appendiceal and colorectal neoplasms: a multi-institutional analysis of the US HIPEC collaborative.
      ,
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      The association between post-treatment surveillance testing and survival in stage II and III colon cancer patients: an observational comparative effectiveness study.
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      ,
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      ,
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      A prospective randomized study of follow-up after radical surgery for colorectal cancer.
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      Colorectal cancer (CRC) monitoring by 6-monthly 18FDG-PET/CT: an open-label multicentre randomised trial.
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      Nurse or surgeon follow-up after rectal cancer: a randomized trial.
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      General practice vs surgical-based follow-up for patients with colon cancer: randomised controlled trial.
      ,
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      Assessment of risk-independent follow-up to detect asymptomatic recurrence after curative resection of colorectal cancer.
      ,
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      Imaging surveillance and survival for surgically resected non-small-cell lung cancer.
      ,
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      Does intensive follow-up alter outcome in patients with advanced lung cancer?.
      ,
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      Does the method of radiologic surveillance affect survival after resection of stage I non-small cell lung cancer?.
      ,
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      Adherence to surveillance guidelines in resected NSCLC: physician compliance and impact on outcomes.
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      Post-treatment surveillance for stage I and II non-small cell lung cancer: impact on clinical outcome.
      ,
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      Impact of surveillance after lobectomy for lung cancer on disease detection and survival.
      ,
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      More frequent surveillance following lung cancer resection is not associated with improved survival: a nationally representative cohort study.
      ,
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      Postoperative follow-up for patients with non-small cell lung cancer.
      ,
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      Symptom-oriented follow-up of early breast cancer is not inferior to conventional control. Results of a prospective multicentre study.
      ,
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      Intensive diagnostic follow-up after treatment of primary breast cancer. A randomized trial. National Research Council Project on Breast Cancer follow-up.
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      • et al.
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      ,
      Impact of follow-up testing on survival and health-related quality of life in breast cancer patients. A multicenter randomized controlled trial. The GIVIO Investigators.
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      ,
      • Koinberg I.L.
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      ,
      • Lash T.L.
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      ,
      • Lash T.L.
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      Reduced mortality rate associated with annual mammograms after breast cancer therapy.
      ,
      • Lash T.L.
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      • et al.
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      ,
      • Lee J.Y.
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      • Paszat L.
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      ,
      • Bjerring O.S.
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      Phase II randomized clinical trial of endosonography and PET/CT versus clinical assessment only for follow-up after surgery for upper gastrointestinal cancer (EUFURO study).
      ,
      • Peixoto R.D.
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      ,
      • Sisic L.
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      • Tan I.T.
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      ,
      • Verschuur E.M.
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      Nurse-led follow-up of patients after oesophageal or gastric cardia cancer surgery: a randomised trial.
      ,
      • Nabhan M.
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      • et al.
      The relationship of the intensity of posttreatment prostate-specific antigen surveillance and prostate cancer outcomes: results from a population-based cohort.
      ]. For quantitative analyses, 61 studies were eligible.

      3.1 Study characteristics and outcomes

      Fig. 2 visualises the studies obtained. Thirty-three original studies (52%) reported on the effect of follow-up in colorectal [
      • Ohlsson B.
      • Breland U.
      • Ekberg H.
      • Graffner H.
      • Tranberg K.G.
      Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up.
      ,
      • Primrose J.N.
      • Perera R.
      • Gray A.
      • Rose P.
      • Fuller A.
      • Corkhill A.
      • et al.
      Effect of 3 to 5 years of scheduled CEA and CT follow-up to detect recurrence of colorectal cancer: the FACS randomized clinical trial.
      ,
      • Rodríguez-Moranta F.
      • Saló J.
      • Arcusa A.
      • Boadas J.
      • Piñol V.
      • Bessa X.
      • et al.
      Postoperative surveillance in patients with colorectal cancer who have undergone curative resection: a prospective, multicenter, randomized, controlled trial.
      ,
      • Rosati G.
      • Ambrosini G.
      • Barni S.
      • Andreoni B.
      • Corradini G.
      • Luchena G.
      • et al.
      A randomized trial of intensive versus minimal surveillance of patients with resected Dukes B2-C colorectal carcinoma.
      ,
      • Snyder R.A.
      • Hu C.Y.
      • Cuddy A.
      • Francescatti A.B.
      • Schumacher J.R.
      • Van Loon K.
      • et al.
      Association between intensity of posttreatment surveillance testing and detection of recurrence in patients with colorectal cancer.
      ,
      • Treasure T.
      • Monson K.
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      • Luchena G.
      • et al.
      A randomized trial of intensive versus minimal surveillance of patients with resected Dukes B2-C colorectal carcinoma.
      ,
      • Treasure T.
      • Monson K.
      • Fiorentino F.
      • Russell C.
      The CEA Second-Look Trial: a randomised controlled trial of carcinoembryonic antigen prompted reoperation for recurrent colorectal cancer.
      ,
      • Wang T.
      • Cui Y.
      • Huang W.S.
      • Deng Y.H.
      • Gong W.
      • Li C.J.
      • et al.
      The role of postoperative colonoscopic surveillance after radical surgery for colorectal cancer: a prospective, randomized clinical study.
      ,
      • Wille-Jørgensen P.
      • Syk I.
      • Smedh K.
      • Laurberg S.
      • Nielsen D.T.
      • Petersen S.H.
      • 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.
      ,
      • Augestad K.M.
      • Norum J.
      • Dehof S.
      • Aspevik R.
      • Ringberg U.
      • Nestvold T.
      • et al.
      Cost-effectiveness and quality of life in surgeon versus general practitioner-organised colon cancer surveillance: a randomised controlled trial.
      ,
      • Kjeldsen B.J.
      • Kronborg O.
      • Fenger C.
      • Jørgensen O.D.
      A prospective randomized study of follow-up after radical surgery for colorectal cancer.
      ,
      • Mäkelä J.T.
      • Laitinen S.O.
      • Kairaluoma M.I.
      Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial.
      ,
      • Pietra N.
      • Sarli L.
      • Costi R.
      • Ouchemi C.
      • Grattarola M.
      • Peracchia A.
      Role of follow-up in management of local recurrences of colorectal cancer: a prospective, randomized study.
      ,
      • Schoemaker D.
      • Black R.
      • Giles L.
      • Toouli J.
      Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients.
      ,
      • Secco G.B.
      • Fardelli R.
      • Gianquinto D.
      • Bonfante P.
      • Baldi E.
      • Ravera G.
      • et al.
      Efficacy and cost of risk-adapted follow-up in patients after colorectal cancer surgery: a prospective, randomized and controlled trial.
      ,
      • Sobhani I.
      • Itti E.
      • Luciani A.
      • Baumgaertner I.
      • Layese R.
      • André T.
      • et al.
      Colorectal cancer (CRC) monitoring by 6-monthly 18FDG-PET/CT: an open-label multicentre randomised trial.
      ,
      • Strand E.
      • Nygren I.
      • Bergkvist L.
      • Smedh K.
      Nurse or surgeon follow-up after rectal cancer: a randomized trial.
      ,
      • Wattchow D.A.
      • Weller D.P.
      • Esterman A.
      • Pilotto L.S.
      • McGorm K.
      • Hammett Z.
      • et al.
      General practice vs surgical-based follow-up for patients with colon cancer: randomised controlled trial.
      ,-
      • Monteil J.
      • Vergnenègre A.
      • Bertin F.
      • Dalmay F.
      • Gaillard S.
      • Bonnaud F.
      • et al.
      Randomized follow-up study of resected NSCLC patients: conventional versus 18F-DG coincidence imaging.
      ,
      • Sui Y.
      • Wang T.
      • Wang X.
      The impact of WeChat app-based education and rehabilitation program on anxiety, depression, quality of life, loss of follow-up and survival in non-small cell lung cancer patients who underwent surgical resection.
      ,
      • Rosselli Del Turco M.
      • Palli D.
      • Cariddi A.
      • Ciatto S.
      • Pacini P.
      • Distante V.
      Intensive diagnostic follow-up after treatment of primary breast cancer. A randomized trial. National Research Council Project on Breast Cancer follow-up.
      ,
      • Palli D.
      • Russo A.
      • Saieva C.
      • Ciatto S.
      • Rosselli Del Turco M.
      • Distante V.
      • et al.
      Intensive vs clinical follow-up after treatment of primary breast cancer: 10-year update of a randomized trial. National Research Council Project on Breast Cancer Follow-up.
      ,
      Impact of follow-up testing on survival and health-related quality of life in breast cancer patients. A multicenter randomized controlled trial. The GIVIO Investigators.
      ,
      • Grunfeld E.
      • Levine M.N.
      • Julian J.A.
      • Coyle D.
      • Szechtman B.
      • Mirsky D.
      • et al.
      Randomized trial of long-term follow-up for early-stage breast cancer: a comparison of family physician versus specialist care.
      ,
      • Koinberg I.L.
      • Fridlund B.
      • Engholm G.B.
      • Holmberg L.
      Nurse-led follow-up on demand or by a physician after breast cancer surgery: a randomised study.
      ,
      • Bjerring O.S.
      • Fristrup C.W.
      • Pfeiffer P.
      • Lundell L.
      • Mortensen M.B.
      Phase II randomized clinical trial of endosonography and PET/CT versus clinical assessment only for follow-up after surgery for upper gastrointestinal cancer (EUFURO study).
      ,
      • Verschuur E.M.
      • Steyerberg E.W.
      • Tilanus H.W.
      • Polinder S.
      • Essink-Bot M.L.
      • Tran K.T.
      • et al.
      Nurse-led follow-up of patients after oesophageal or gastric cardia cancer surgery: a randomised trial.
      ]. Table 1, Table 2 provide detailed overviews of the low and high risk of bias studies. Risk of bias assessment is provided in supplementary table A.2. Fig. 3 visualises outcomes per study. The results of the meta-analysis per tumour type, including stratified analyses are reported in Table 3.
      Fig. 2
      Fig. 2Multi-layered circle plot displaying all 63 included studies by cancer type (inner circle), aspect of follow-up investigated (middle circle), and study design (outer circle).
      Table 1Studies at low risk of bias.
      Author (year)NCancer type, stageFollow-up durationIntensive follow-up approachComparison (reference)
      Ohlsson (1995) [
      • Ohlsson B.
      • Breland U.
      • Ekberg H.
      • Graffner H.
      • Tranberg K.G.
      Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up.
      ]
      107CRC, Dukes A-CRange 5.5–8.8 yClin exam/CEA/CXR/proctoscopy: every 3 m Y1-2, 6 m Y3-4, 12 m Y5

      CT pelvis: every 6 m Y1-2

      Colonoscopy: 3, 15, 30 and 60 m
      No organised follow-up
      Primrose (2014) [
      • Primrose J.N.
      • Perera R.
      • Gray A.
      • Rose P.
      • Fuller A.
      • Corkhill A.
      • et al.
      Effect of 3 to 5 years of scheduled CEA and CT follow-up to detect recurrence of colorectal cancer: the FACS randomized clinical trial.
      ]
      1202CRC, Dukes A-CMean 3.7 yCEA-only: every 3 m Y1-2, every 6 m Y3-5
      Single chest, abdomen, and pelvis CT scan at 12–18 months if requested at study entry by hospital clinician; ∗∗ Only performed in patients at high risk for metachronous lesions (hereditary cancer, synchronous colorectal neoplasms); ∗∗∗ Classification of follow-up facility based. Expected number of scans/CEA measurements calculated through 2-level random intercept negative binomial model. High frequency facility defined as observed:expected ratio ≥1.


      CT-only: CT chest, abd, pelvis every 6 m Y1-2, every 12 m Y3-5

      CT + CEA: protocols combined
      No scheduled follow-up
      Single chest, abdomen, and pelvis CT scan at 12–18 months if requested at study entry by hospital clinician; ∗∗ Only performed in patients at high risk for metachronous lesions (hereditary cancer, synchronous colorectal neoplasms); ∗∗∗ Classification of follow-up facility based. Expected number of scans/CEA measurements calculated through 2-level random intercept negative binomial model. High frequency facility defined as observed:expected ratio ≥1.
      Rodriguez (2006) [
      • Rodríguez-Moranta F.
      • Saló J.
      • Arcusa A.
      • Boadas J.
      • Piñol V.
      • Bessa X.
      • et al.
      Postoperative surveillance in patients with colorectal cancer who have undergone curative resection: a prospective, multicenter, randomized, controlled trial.
      ]
      259CRC, II–IIIMedian 49 m and 45 mClin exam/CEA: every 3 m Y1-2, every 6 m Y 3-5

      Abd CT or US: every 6 m Y1-2, every 12 m Y3-5

      CXR/colonoscopy: every 12 m Y1-5
      Clin exam/CEA: every 3 m Y1-2, every 6 m Y3-5

      Colonoscopy: @ 12 and 36 m ∗∗
      Rosati (2016) [
      • Rosati G.
      • Ambrosini G.
      • Barni S.
      • Andreoni B.
      • Corradini G.
      • Luchena G.
      • et al.
      A randomized trial of intensive versus minimal surveillance of patients with resected Dukes B2-C colorectal carcinoma.
      ]
      1228CRC, Dukes B2–CMinimum 5 yClin exam/CEA and CA 19-9: every 4 m Y1-2, every 6 m Y3-4, every 12 m Y5

      CXR/colonoscopy: every 12 m Y1-5

      Liver US: @ 4, 8, 12, 16, 24, 16, 48 and 60 m
      Clin exam/CEA: every 4 m Y1-2, every 6 m Y3-4, every 12 m Y5

      Colonoscopy: @ 12 and 48 m

      Liver US: @ 4 and 16 m
      Snyder (2018) [
      • Snyder R.A.
      • Hu C.Y.
      • Cuddy A.
      • Francescatti A.B.
      • Schumacher J.R.
      • Van Loon K.
      • et al.
      Association between intensity of posttreatment surveillance testing and detection of recurrence in patients with colorectal cancer.
      ]
      8529CRC, I–IIIMinimum 5 yHigh-frequency CT and CEA ∗∗∗Low-frequency CT and CEA ∗∗∗
      Treasure (2014) [
      • Treasure T.
      • Monson K.
      • Fiorentino F.
      • Russell C.
      The CEA Second-Look Trial: a randomised controlled trial of carcinoembryonic antigen prompted reoperation for recurrent colorectal cancer.
      ]
      216CRC, Dukes A-CMinimum 18 ySecond look surgery upon CEA rise

      Clin exam: every 3 m Y1-2, every 6 m Y3-5

      CEA: every month Y1-3, every 3 m Y4-5
      No additional diagnostics upon CEA rise

      Clin exam: every 3 m Y1-2, every 6 m Y3-5
      Wang (2009) [
      • Wang T.
      • Cui Y.
      • Huang W.S.
      • Deng Y.H.
      • Gong W.
      • Li C.J.
      • et al.
      The role of postoperative colonoscopic surveillance after radical surgery for colorectal cancer: a prospective, randomized clinical study.
      ]
      326CRC, Dukes A-CMedian 74 mColonoscopy/clin exam/CEA/abd CT or US/CXR: every 3 m Y1, every 6 m Y2-3, every 12 m Y4-5Colonoscopy: @ 6, 30 and 60 months

      Clin exam/CEA/abd CT or US/CXR: every 3 m Y1, every 6 m Y2-3, every 12 m Y4-5
      Wille-Jørgensen (2018) [
      • Wille-Jørgensen P.
      • Syk I.
      • Smedh K.
      • Laurberg S.
      • Nielsen D.T.
      • Petersen S.H.
      • 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.
      ]
      2509CRC, II–IIIMedian 5 yCT/CEA: @ 6, 12, 18, 24 and 36 mCT/CEA: @ 12 and 36 m
      Bornhak (2007) [
      • Bornhak S.
      • Heidemann E.
      • Herschlein H.J.
      • Simon W.
      • Merkle E.
      • Widmaier G.
      • et al.
      Symptom-oriented follow-up of early breast cancer is not inferior to conventional control. Results of a prospective multicentre study.
      ]
      670Breast, T1-4,

      N0-2
      Almost all patients 5 yClin exam/blood tests: every 3 m Y1-3, every 6 m Y4-5

      Liver US/CXR: every 6 m Y1-5

      Mammography: every 6 m Y1-3, every 12 m Y4-5
      Clin exam: every 3 m Y1-3, every 6 m Y4-5

      Mammography: every 6 m Y1-3, every 12 m Y4-5
      Del Turco (1994) [
      • Rosselli Del Turco M.
      • Palli D.
      • Cariddi A.
      • Ciatto S.
      • Pacini P.
      • Distante V.
      Intensive diagnostic follow-up after treatment of primary breast cancer. A randomized trial. National Research Council Project on Breast Cancer follow-up.
      ]

      Palli (1999) [
      • Palli D.
      • Russo A.
      • Saieva C.
      • Ciatto S.
      • Rosselli Del Turco M.
      • Distante V.
      • et al.
      Intensive vs clinical follow-up after treatment of primary breast cancer: 10-year update of a randomized trial. National Research Council Project on Breast Cancer Follow-up.
      ]
      1243Breast, T1-4,

      N−/+
      Almost all patients 10 yClin exam: every 3 m Y1-2, every 6 months Y3-5

      Mammography: every 12 m Y1-5

      CXR/bone scan: every 6 m Y1-5
      Clin exam: every 3 m Y1-2, every 6 months Y3-5

      Mammography: every 12 m Y1-5
      Liberati (1994) [
      Impact of follow-up testing on survival and health-related quality of life in breast cancer patients. A multicenter randomized controlled trial. The GIVIO Investigators.
      ]
      1320Breast, T1-3,

      N0-1
      Median 71 mClin exam/blood tests: every 3 m Y1-2, every 6 m Y3-5

      Mammography/liver US/bone scan: every 12 m Y1-5

      CXR: every 6 m Y1-5
      Clin exam/blood test: every 3 m Y1-2, every 6 m Y3-5

      Mammography: every 12 m Y1-5
      Bjerring (2019) [
      • Bjerring O.S.
      • Fristrup C.W.
      • Pfeiffer P.
      • Lundell L.
      • Mortensen M.B.
      Phase II randomized clinical trial of endosonography and PET/CT versus clinical assessment only for follow-up after surgery for upper gastrointestinal cancer (EUFURO study).
      ]
      183GOJ, gastric, pancreatic, I-IIIAlmost all patients 2 yClin exam/PET-CT/endoscopic US: every 3 m Y1, every 6 m Y2Clin exam: every 3 m Y1, every 6 m Y2
      Nabhan (2012) [
      • Nabhan M.
      • Kim S.P.
      • Shah N.D.
      • Bagniewski S.M.
      • Shi Q.
      • Karnes R.J.
      • et al.
      The relationship of the intensity of posttreatment prostate-specific antigen surveillance and prostate cancer outcomes: results from a population-based cohort.
      ]
      703Prostate, I–IIIMedian 6.7 yPSA test within 2 y after treatmentNo PSA test within 2 y after treatment
      Abd = abdominal, CA 19-9 = carbohydrate antigen 19-9, CEA = carcinoembryonic antigen, clin exam = clinical examination, CRC = colorectal cancer, CT = computed tomography, CXR = chest x-ray, GOJ = gastro-oesophageal junction, m = months, MRI = magnetic resonance imaging, NR = not reported, NSCLC = non-small cell lung cancer, PET-CT = positron emission tomography – computed tomography, PSA = prostate specific antigen, US = ultrasound, w = weeks, y = years.
      a Single chest, abdomen, and pelvis CT scan at 12–18 months if requested at study entry by hospital clinician; ∗∗ Only performed in patients at high risk for metachronous lesions (hereditary cancer, synchronous colorectal neoplasms); ∗∗∗ Classification of follow-up facility based. Expected number of scans/CEA measurements calculated through 2-level random intercept negative binomial model. High frequency facility defined as observed:expected ratio ≥1.
      Table 2Studies at high risk of bias.
      Author (year)NCancer type, stageFollow-up durationIntensive follow-up approachComparison (reference)
      Augestad (2013) [
      • Augestad K.M.
      • Norum J.
      • Dehof S.
      • Aspevik R.
      • Ringberg U.
      • Nestvold T.
      • et al.
      Cost-effectiveness and quality of life in surgeon versus general practitioner-organised colon cancer surveillance: a randomised controlled trial.
      ]
      110Colon, Dukes A-C58% completed 2 y follow-upSurgeon-ledGeneral practitioner-led
      Bergamaschi (1996) [
      • Bergamaschi R.
      • Arnaud J.P.
      Routine compared with nonscheduled follow-up of patients with "curative" surgery for colorectal cancer.
      ]
      800CRC, I-IIIMinimum 60 mClin exam/CEA/liver US: every 3 m Y1, every 6 m Y2-5

      CXR: every 3 m Y1, every 6 m Y2, every 12 m Y3-5

      Endoscopy: every 12 m Y1-5
      Symptom-based
      Borie (2004) [
      • Borie F.
      • Daurès J.P.
      • Millat B.
      • Trétarre B.
      Cost and effectiveness of follow-up examinations in patients with colorectal cancer resected for cure in a French population-based study.
      ]
      231CRC, Dukes A-CNRClin exam: every 3 m Y1-2, every 6 m Y3-5

      CEA/US: every 4–6 m Y1-3, every 12 m Y4-5

      CXR: every 12 m

      Colonoscopy: every 36 m
      Clin. Exam: at most every 6 m Y1-5

      CEA/US: at most every 12 m Y1-3

      CXR: at most every 12 m Y1-2

      Colonoscopy: at most every 36 m
      Castells (1998) [
      • Castells A.
      • Bessa X.
      • Daniels M.
      • Ascaso C.
      • Lacy A.M.
      • García-Valdecasas J.C.
      • et al.
      Value of postoperative surveillance after radical surgery for colorectal cancer: results of a cohort study.
      ]
      199CRC, I-IIIMedian 51 mCompliant (>70% adherence) to follow-upNon-compliant (<70% adherence) to follow-up
      Coebergh (2018) [
      • Coebergh van den Braak R.R.J.
      • Lalmahomed Z.S.
      • Büttner S.
      • Hansen B.E.
      • Ijzermans J.N.M.
      • Group M.S.
      Nonphysician clinicians in the follow-up of resected patients with colorectal cancer.
      ]
      681CRC, I-IIIMedian 68 m for OS

      Median 34 m for DFS
      Intensive (≥3 follow-up moments in first year)Minimal (≤2 follow-up moments in first year)
      Eckardt (1994) [
      • Eckardt V.F.
      • Stamm H.
      • Kanzler G.
      • Bernhard G.
      Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program.
      ]
      212CRC, Dukes A-CMean 91 m and 94 mFull compliance to endoscopic follow-upNon-compliance to endoscopic follow-up
      Gamboa (2020) [
      • Gamboa A.C.
      • Zaidi M.Y.
      • Lee R.M.
      • Speegle S.
      • Switchenko J.M.
      • Lipscomb J.
      • et al.
      Optimal surveillance frequency after CRS/HIPEC for appendiceal and colorectal neoplasms: a multi-institutional analysis of the US HIPEC collaborative.
      ]
      239CRC, IV (peritoneal)Median 17 mHigh frequency follow-up (every 2–4 months)Low-frequency follow-up (every 6–12 months)
      Hines (2019) [
      • Hines R.B.
      • Jiban M.J.H.
      • Specogna A.V.
      • Vishnubhotla P.
      • Lee E.
      • Zhang S.
      The association between post-treatment surveillance testing and survival in stage II and III colon cancer patients: an observational comparative effectiveness study.
      ]
      17,860CRC, II-IIIMedian 9.0 y and 9.6 yMore adherent to guideline recommendationsLess adherent to guideline recommendations
      Hines (2020) [
      • Hines R.B.
      • Jiban M.J.H.
      • Specogna A.V.
      • Vishnubhotla P.
      • Lee E.
      • Troy S.P.
      • et al.
      Surveillance colonoscopy in older stage I colon cancer patients and the association with colon cancer-specific mortality.
      ]
      8783CRC, IMedian >10 y1 colonoscopy during follow-up or ≥2 colonoscopies during follow-upNo colonoscopy during follow-up
      Hyder (2013) [
      • Hyder O.
      • Dodson R.M.
      • Mayo S.C.
      • Schneider E.B.
      • Weiss M.J.
      • Herman J.M.
      • et al.
      Post-treatment surveillance of patients with colorectal cancer with surgically treated liver metastases.
      ]
      507CRC, IV (liver)NRFollow-up with imaging (≥1 scan)No imaging during follow-up
      Kjeldsen (1997) [
      • Kjeldsen B.J.
      • Kronborg O.
      • Fenger C.
      • Jørgensen O.D.
      A prospective randomized study of follow-up after radical surgery for colorectal cancer.
      ]
      597CRC, Dukes A-CNRClin exam/blood analysis without CEA/CXR/colonoscopy: every 6 m Y1-3, every 12 m Y4-5, every 5 y Y6-15Clin exam/blood analysis without CEA/CXR/colonoscopy: every 5 y Y1-15
      Körner (2005) [
      • Körner H.
      • Söreide K.
      • Stokkeland P.J.
      • Söreide J.A.
      Systematic follow-up after curative surgery for colorectal cancer in Norway: a population-based audit of effectiveness, costs, and compliance.
      ]
      314CRC, Dukes A-CMedian 66 mGuideline follow-upNo follow-up
      Laubert (2010) [
      • Laubert T.
      • Bader F.G.
      • Oevermann E.
      • Jungbluth T.
      • Unger L.
      • Roblick U.J.
      • et al.
      Intensified surveillance after surgery for colorectal cancer significantly improves survival.
      ]
      1469CRC, I-IVMedian 70 mIntensive follow-up (>70% adherence) or Minimal follow-up (<70% adherence)No follow-up
      Mahboubi (2007) [
      • Mahboubi A.
      • Lejeune C.
      • Coriat R.
      • Binquet C.
      • Bouvier A.M.
      • Béjean S.
      • et al.
      Which patients with colorectal cancer are followed up by general practitioners? A population-based study.
      ]
      389CRC, I-IVNRRegular (≥1 per 6 months) follow-up at GP or Occasional (<1 per 6 months) follow-up at GPNo follow-up
      Mäkelä (1995) [
      • Mäkelä J.T.
      • Laitinen S.O.
      • Kairaluoma M.I.
      Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial.
      ]
      106CRC, Dukes A-CNRClin exam/CEA/CXR: every 3 m Y1-2, every 6 m Y3-5

      Liver US: every 6 m Y1-5

      CT abd/colonoscopy: every 12 m Y1-5

      Sigmoidoscopy
      For rectal and sigmoid cancer patients only. ∗∗ Only in patients with symptoms possibly related to bone metastases.
      : every 3 m Y1-5
      Clin exam/CEA/CXR/sigmoidoscopy
      For rectal and sigmoid cancer patients only. ∗∗ Only in patients with symptoms possibly related to bone metastases.
      : every 3 m Y1-2, every 6 m Y3-5

      Barium enema: every 12 m Y1-5
      Ovaska (1990) [
      • Ovaska J.
      • Järvinen H.
      • Kujari H.
      • Perttilä I.
      • Mecklin J.P.
      Follow-up of patients operated on for colorectal carcinoma.
      ]
      507CRC, Dukes A-C85% 5 yClin exam/CEA/sigmoidoscopy: @3, 6, 12, 18, 24, 36, 48 and 60 m

      CXR/colography: every 6 m Y1, every 12 m Y2-5
      No follow-up
      Pietra (1998) [
      • Pietra N.
      • Sarli L.
      • Costi R.
      • Ouchemi C.
      • Grattarola M.
      • Peracchia A.
      Role of follow-up in management of local recurrences of colorectal cancer: a prospective, randomized study.
      ]
      207CRC, Astler-Coller B1–C2NRClin exam/CEA/US: every 3 m Y1-2, every 6 m Y3-4, every 12 m thereafter

      CXR/CT/colonoscopy: every 12 m Y1-5
      Clin exam/CEA/US: every 6 m Y1, every 12 m Y2-5

      CXR/colonoscopy: every 12 m Y1-5
      Pugliese (1984) [
      • Pugliese V.
      • Aste H.
      • Saccomanno S.
      • Bruzzi P.
      • Bonelli L.
      • Santi L.
      Outcome of follow-up programs in patients previously resected for colorectal cancer.
      ]
      177CRC, Dukes B–CMedian 33 mClin exam/blood tests - later including CEA: every 3 m Y1-2, every 6 m Y3-5

      CXR/liver US/colonoscopy: every 6 m Y1-2, every 12 m Y3-5
      No follow-up
      Rulyak (2007) [
      • Rulyak S.J.
      • Lieberman D.A.
      • Wagner E.H.
      • Mandelson M.T.
      Outcome of follow-up colon examination among a population-based cohort of colorectal cancer patients.
      ]
      1002CRC, 0-IIIMedian 3.6 y≥1 colonoscopies during follow-upNo colonoscopy during follow-up
      Schoemaker (1998) [
      • Schoemaker D.
      • Black R.
      • Giles L.
      • Toouli J.
      Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients.
      ]
      325CRC, Dukes A-C94% 60 mClin exam/CEA: every 3 m Y1-2, every 6 m Y3-5

      CXR/liver CT/colonoscopy: every 12 m Y1-5
      Clin exam/CEA: every 3 m Y1-2, every 6 m Y3-5
      Secco (2002) [
      • Secco G.B.
      • Fardelli R.
      • Gianquinto D.
      • Bonfante P.
      • Baldi E.
      • Ravera G.
      • et al.
      Efficacy and cost of risk-adapted follow-up in patients after colorectal cancer surgery: a prospective, randomized and controlled trial.
      ]
      358CRC, Dukes A-CMedian 61.5 m (high-risk) and 42 m (low-risk)High risk patients

      Clin exam/CEA: every 3 m Y1-2, every 4 m Y3, every 6 m Y4-5

      Abd and pelvic US: every 6 m 1-3Y, every 12 m Y4-5

      CXR/rectosigmoidoscopy
      For rectal and sigmoid cancer patients only. ∗∗ Only in patients with symptoms possibly related to bone metastases.
      : every 12 m Y1-5

      Low risk patients

      Clin exam/CEA: every 6 m Y1-2, every 12 m Y3-5

      Abd and pelvic US: every 6 m 1-2Y, every 12 m Y3-5

      CXR: every 12 m Y1-5

      Rectosigmoidoscopy
      For rectal and sigmoid cancer patients only. ∗∗ Only in patients with symptoms possibly related to bone metastases.
      : every 12 m Y1-2, every 24 m Y3-5
      Minimal follow-up not clearly defined
      Sobhani (2018) [
      • Sobhani I.
      • Itti E.
      • Luciani A.
      • Baumgaertner I.
      • Layese R.
      • André T.
      • et al.
      Colorectal cancer (CRC) monitoring by 6-monthly 18FDG-PET/CT: an open-label multicentre randomised trial.
      ]
      239CRC, II-IVNRFollow-up with whole body CT and PET-CT: every 6 m Y1-3Follow-up with whole body CT: every 6 m Y1-3
      Strand (2011) [
      • Strand E.
      • Nygren I.
      • Bergkvist L.
      • Smedh K.
      Nurse or surgeon follow-up after rectal cancer: a randomized trial.
      ]
      110CRC, I-IVNRSurgeon-ledNurse-led
      Wattchow (2006) [
      • Wattchow D.A.
      • Weller D.P.
      • Esterman A.
      • Pilotto L.S.
      • McGorm K.
      • Hammett Z.
      • et al.
      General practice vs surgical-based follow-up for patients with colon cancer: randomised controlled trial.
      ]
      203CRC, Dukes A-C87% 2 ySurgeon-ledGeneral practitioner-led
      Zitt (2006) [
      • Zitt M.
      • Mühlmann G.
      • Weiss H.
      • Kafka-Ritsch R.
      • Oberwalder M.
      • Kirchmayr W.
      • et al.
      Assessment of risk-independent follow-up to detect asymptomatic recurrence after curative resection of colorectal cancer.
      ]
      430CRC, I-IVMean 49 mClin exam/CEA: every 3 m Y1-2, every 6 m Y3-5

      CXR + abd US/CT + colonoscopy: every 6 m Y1-5 (alternating per 6 m)

      Rectoscopy @ 3, 6 and 9 months or Non-standardised follow-up in hospital or at GP
      No follow-up
      Backhus (2016) [
      • Backhus L.M.
      • Farjah F.
      • Liang C.K.
      • He H.
      • Varghese Jr., T.K.
      • Au D.H.
      • et al.
      Imaging surveillance and survival for surgically resected non-small-cell lung cancer.
      ]
      18,406NSCLC, I-IINRClinical visitation within 4–8 m after treatmentNo clinical visitation within 4–8 m after treatment
      Benamore (2007) [
      • Benamore R.
      • Shepherd F.A.
      • Leighl N.
      • Pintilie M.
      • Patel M.
      • Feld R.
      • et al.
      Does intensive follow-up alter outcome in patients with advanced lung cancer?.
      ]
      75NSCLC, IIIMedian 77 m and 44 mFollow-up within clinical trial

      Clin exam/blood analysis/CXR: every 2/3 m Y1-2, every 6 m thereafter

      CT chest and upper abd/MRI brain: every 6 m Y1-3, every 12 m thereafter
      Non-trial follow-up

      Clin exam/blood analysis/CXR: every 3 m Y1-2/3, every 6 m Y3/4-5
      Crabtree (2015) [
      • Crabtree T.D.
      • Puri V.
      • Chen S.B.
      • Gierada D.S.
      • Bell J.M.
      • Broderick S.
      • et al.
      Does the method of radiologic surveillance affect survival after resection of stage I non-small cell lung cancer?.
      ]
      554NSCLC, INRRoutine CT-based follow-upRoutine CXR-based follow-up
      Ho (2017) [
      • Ho C.
      • Siegfried J.
      • Remo K.
      • Laskin J.
      Adherence to surveillance guidelines in resected NSCLC: physician compliance and impact on outcomes.
      ]
      263NSCLC, IB-IINRFrequency CT and/or clinical visits per or above guidelinesFrequency CT and/or clinical visits below guidelines
      Karzijn (2016) [
      • Karzijn R.
      • Alberts L.
      • Kelder J.C.
      • Hofman F.N.
      • El Sharouni S.Y.
      • Kastelijn E.A.
      • et al.
      Post-treatment surveillance for stage I and II non-small cell lung cancer: impact on clinical outcome.
      ]
      73NSCLC, I-IINRFollow-up with CT imagingFollow-up with CXR only
      Mayne (2020) [
      • Mayne N.R.
      • Mallipeddi M.K.
      • Darling A.J.
      • Jeffrey Yang C.F.
      • Eltaraboulsi W.R.
      • Shoffner A.R.
      • et al.
      Impact of surveillance after lobectomy for lung cancer on disease detection and survival.
      ]
      187NSCLC, IAMedian 36 m and 56.4 mEarly (6 ± 3 months) start of CT surveillanceLate (12 ± 3 months) start of CT surveillance
      McMurry (2018) [
      • McMurry T.L.
      • Stukenborg G.J.
      • Kessler L.G.
      • Colditz G.A.
      • Wong M.L.
      • Francescatti A.B.
      • et al.
      More frequent surveillance following lung cancer resection is not associated with improved survival: a nationally representative cohort study.
      ]
      4463NSCLC, I-IIIMinimum 60 m3 months CT-imaging interval6 or 12 months CT-imaging interval
      Monteil (2010) [
      • Monteil J.
      • Vergnenègre A.
      • Bertin F.
      • Dalmay F.
      • Gaillard S.
      • Bonnaud F.
      • et al.
      Randomized follow-up study of resected NSCLC patients: conventional versus 18F-DG coincidence imaging.
      ]
      69NSCLC, I-IIIAMedian 25 m and 29 mPET-CT/Brain CTBrain, chest and upper abd CT/abd US/bone scintigraphy ∗∗
      Nakamura (2010) [
      • Nakamura R.
      • Kurishima K.
      • Kobayashi N.
      • Ishikawa S.
      • Goto Y.
      • Sakai M.
      • et al.
      Postoperative follow-up for patients with non-small cell lung cancer.
      ]
      1398NSCLC, I-IIIMedian 79 mFollow-up by chest physician

      Clin exam/CXR: every 3–4 m Y1-3

      CT: every 6 m Y1-3
      Follow-up by thoracic surgeon

      Clin exam/CXR: every 3–4 m Y1-3
      Pan (2015) [
      • Pan Y.
      • Brink C.
      • Schytte T.
      • Petersen H.
      • Wu Y.L.
      • Hansen O.
      Planned FDG PET-CT scan in follow-up detects disease progression in patients with locally advanced NSCLC receiving curative chemoradiotherapy earlier than standard CT.
      ]
      92NSCLC, IIB-IIIBMedian 23 mFollow-up with CT imaging and a single PET-CT @ 9 mFollow-up with CT imaging only
      Reddy (2017) [
      • Reddy J.P.
      • Tang C.
      • Shih T.
      • Kim B.
      • Kim C.
      • Nguyen Q.N.
      • et al.
      Influence of surveillance PET/CT on detection of early recurrence after definitive radiation in stage III non-small-cell lung cancer.
      ]
      200NSCLC, IIIMedian 59.4 mFollow-up with PET-CT and CT alternating in Y1-2Follow-up with CT only
      Sui (2020) [
      • Sui Y.
      • Wang T.
      • Wang X.
      The impact of WeChat app-based education and rehabilitation program on anxiety, depression, quality of life, loss of follow-up and survival in non-small cell lung cancer patients who underwent surgical resection.
      ]
      200NSCLC, I-III85% 5 yWeChat app-based education and rehabilitation program - including disease related education (once a week for 12w), rehabilitation exercise guidance (once a week for 40w), daily activity supervision (once a week for 12 m), and psychosocial support (every 2 weeks for 12 m)Regular rehabilitation program
      Virgo (1995) [
      • Virgo K.S.
      • McKirgan L.W.
      • Caputo M.C.
      • Mahurin D.M.
      • Chao L.C.
      • Caputo N.A.
      • et al.
      Post-treatment management options for patients with lung cancer.
      ]
      182Lung (subtype NR), I-IIIAMean 3.3 yIntensive follow-up, any of the following criteria:

      ≥4 visits and/or blood tests and/or CXR per year,

      ≥1 CT per year, or any bronchoscopy and/or sputum cytology
      Non-intensive follow-up (none of the criteria met)
      Grunfeld (2006) [
      • Grunfeld E.
      • Levine M.N.
      • Julian J.A.
      • Coyle D.
      • Szechtman B.
      • Mirsky D.
      • et al.
      Randomized trial of long-term follow-up for early-stage breast cancer: a comparison of family physician versus specialist care.
      ]
      968Breast, early stageMedian 3.5 yGuideline follow-up carried out by cancer specialistGuideline follow-up carried out by family physician
      Koinberg (2004) [
      • Koinberg I.L.
      • Fridlund B.
      • Engholm G.B.
      • Holmberg L.
      Nurse-led follow-up on demand or by a physician after breast cancer surgery: a randomised study.
      ]
      264Breast, I-IINRPhysician-led

      Clin exam: every 3 m Y1-2, every 6 m Y3-5, and yearly thereafter

      Mammography: every 12 m Y1-5
      Nurse-led

      Clin exam: on-demand

      Mammography: every 12 m Y1-3, screening-programme thereafter
      Lash (2005) [
      • Lash T.L.
      • Clough-Gorr K.
      • Silliman R.A.
      Reduced rates of cancer-related worries and mortality associated with guideline surveillance after breast cancer therapy.
      ]
      303Breast, I-IIMedian 7.4 yNumber of consecutive years of guideline surveillance(continuous analysis, no separate comparison group)
      Lash (2006) [
      • Lash T.L.
      • Fox M.P.
      • Silliman R.A.
      Reduced mortality rate associated with annual mammograms after breast cancer therapy.
      ]
      334Breast, I-IIIANROne or more mammograms during follow-upNo mammograms during follow-up
      Lash (2007) [
      • Lash T.L.
      • Fox M.P.
      • Buist D.S.
      • Wei F.
      • Field T.S.
      • Frost F.J.
      • et al.
      Mammography surveillance and mortality in older breast cancer survivors.
      ]
      812Breast, I-IINRNumber surveillance mammograms received(continuous analysis, no separate comparison group)
      Lee (2015) [
      • Lee J.Y.
      • Lim S.H.
      • Lee M.Y.
      • Kim H.
      • Kim M.
      • Kim S.
      • et al.
      Impact on survival of regular postoperative surveillance for patients with early breast cancer.
      ]
      3770Breast, I-IIIMedian 7.1 yClin exam/blood analysis/mammography/CXR/breast, abd and pelvic US/bone scans: every 3–6 m Y1-5, and yearly thereafterControl group of patients lost to follow-up after adjuvant therapy
      Paszat (2009) [
      • Paszat L.
      • Sutradhar R.
      • Grunfeld E.
      • Gainford C.
      • Benk V.
      • Bondy S.
      • et al.
      Outcomes of surveillance mammography after treatment of primary breast cancer: a population-based case series.
      ]
      901Breast, I-IIMedian 141 m and 29 m≥1 surveillance mammographyNo surveillance mammography
      Peixoto (2014) [
      • Peixoto R.D.
      • Lim H.J.
      • Kim H.
      • Abdullah A.
      • Cheung W.Y.
      Patterns of surveillance following curative intent therapy for gastroesophageal cancer.
      ]
      292Gastroesophageal, I-IIINROncologist follow-up with Clin exam or Blood analysis or Imaging or endoscopyDischarge to general practitioner
      Sisic (2018) [
      • Sisic L.
      • Strowitzki M.J.
      • Blank S.
      • Nienhueser H.
      • Dorr S.
      • Haag G.M.
      • et al.
      Postoperative follow-up programs improve survival in curatively resected gastric and junctional cancer patients: a propensity score matched analysis.
      ]
      587Gastroesophageal, I-IIIMedian 60.5 m and 68.5 mFollow-up in cancer centre

      Clin exam/CT abd or abd US and endoscopy (alternating): every 3 m Y1-2, every 6 m Y3-4, every 12 m Y5
      Individual follow-up by other physicians
      Tan (2007) [
      • Tan I.T.
      • So B.Y.
      Value of intensive follow-up of patients after curative surgery for gastric carcinoma.
      ]
      102Gastric, I-IVMean 3.4 y>1 CT scans per year≤1 CT scans per year
      Verschuur (2009) [
      • Verschuur E.M.
      • Steyerberg E.W.
      • Tilanus H.W.
      • Polinder S.
      • Essink-Bot M.L.
      • Tran K.T.
      • et al.
      Nurse-led follow-up of patients after oesophageal or gastric cardia cancer surgery: a randomised trial.
      ]
      109Gastroesophageal, I-IV98% 1 yPhysician-led follow-upNurse-led follow-up
      Abd = abdominal, CA 19-9 = carbohydrate antigen 19-9, CEA = carcinoembryonic antigen, clin exam = clinical examination, CRC = colorectal cancer, CT = computed tomography, CXR = chest x-ray, GOJ = gastro-oesophageal junction, m = months, MRI = magnetic resonance imaging, NR = not reported, NSCLC = non-small cell lung cancer, PET-CT = positron emission tomography – computed tomography, PSA = prostate specific antigen, US = ultrasound, w = weeks, y = years.
      a For rectal and sigmoid cancer patients only. ∗∗ Only in patients with symptoms possibly related to bone metastases.
      Fig. 3
      Fig. 3Multi-layered circle plot summarising the reported effect in all 63 included studies, stratified by risk of bias. The inner circle represents cancer type, the middle circle study design, and the outer circle the effect of the intervention on overall or cancer specific survival, and treatment intent.
      Table 3Meta-analysis per tumour type.
      OSCSSCurative treatment
      Cancer typeNHR [95% CI]I2NHR [95% CI]I2NRR [95% CI]I2
      All studies
      Colorectal300.82 [0.73–0.91]
      Statistically significant result.
      85%110.80 [0.63–1.01]84%191.60 [1.21–2.11]
      Statistically significant result.
      66%
      Lung120.94 [0.84–1.05]49%11.45 [0.84–2.5]NA41.34 [0.82–2.20]39%
      Breast80.80 [0.54–1.18]92%30.52 [0.27–1.02]94%
      Upper GI50.79 [0.66–0.95]
      Statistically significant result.
      0%21.25 [0.62–2.52]50%
      Prostate11.00 [0.86–1.16]NA
      Low risk of bias
      Colorectal80.99 [0.92–1.06]7%30.94 [0.77–1.16]0%61.30 [1.05–1.61]
      Statistically significant result.
      28%
      Lung
      Breast3
      Long-term updates [62] from the study by Del Turco et al. [61] were used for the meta-analysis in breast cancer patients.
      1.06 [0.92–1.23]0%
      Upper GI10.78 [0.51–1.19]NA10.92 [0.47–1.81]NA
      Prostate11.00 [0.86–1.16]NA
      High risk of bias
      Colorectal220.75 [0.65–0.86]
      Statistically significant result.
      87%80.74 [0.54–1.02]88%131.77 [1.06–2.94]
      Statistically significant result.
      74%
      Lung120.94 [0.84–1.05]49%11.45 [0.84–2.5]NA41.34 [0.82–2.20]39%
      Breast50.68 [0.41–1.14]91%30.52 [0.27–1.02]94%
      Upper GI40.79 [0.65–0.97]
      Statistically significant result.
      0%11.73 [0.84–3.59]NA
      Prostate
      CI = confidence interval, CSS = cancer specific survival, HR = hazard ratio, N = number of studies reporting on outcome, NA = not applicable, OS = overall survival, RR = relative risk, Upper GI = upper gastrointestinal.
      a Statistically significant result.
      b Long-term updates [
      • Palli D.
      • Russo A.
      • Saieva C.
      • Ciatto S.
      • Rosselli Del Turco M.
      • Distante V.
      • et al.
      Intensive vs clinical follow-up after treatment of primary breast cancer: 10-year update of a randomized trial. National Research Council Project on Breast Cancer Follow-up.
      ] from the study by Del Turco et al. [
      • Rosselli Del Turco M.
      • Palli D.
      • Cariddi A.
      • Ciatto S.
      • Pacini P.
      • Distante V.
      Intensive diagnostic follow-up after treatment of primary breast cancer. A randomized trial. National Research Council Project on Breast Cancer follow-up.
      ] were used for the meta-analysis in breast cancer patients.

      3.2 Colorectal cancer

      The 33 colorectal cancer studies comprised 50,431 patients in total (Table 1, Table 2). Across all studies, intensive follow-up led to improved OS (HR 0.82, 95% CI 0.73–0.91) and an increased probability of curative intent treatment for recurrences (RR 1.60, 95% CI 1.21–2.11). An equally large, but non-significant, impact on CSS (HR 0.80, 95% CI 0.63–1.01) was observed. Considerable heterogeneity was present (I2 66–85% for the three outcomes) (Table 3).
      In the eight studies (24%) considered to be at low risk of bias, including seven RCTs [
      • Ohlsson B.
      • Breland U.
      • Ekberg H.
      • Graffner H.
      • Tranberg K.G.
      Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up.
      ,
      • Primrose J.N.
      • Perera R.
      • Gray A.
      • Rose P.
      • Fuller A.
      • Corkhill A.
      • et al.
      Effect of 3 to 5 years of scheduled CEA and CT follow-up to detect recurrence of colorectal cancer: the FACS randomized clinical trial.
      ,
      • Rodríguez-Moranta F.
      • Saló J.
      • Arcusa A.
      • Boadas J.
      • Piñol V.
      • Bessa X.
      • et al.
      Postoperative surveillance in patients with colorectal cancer who have undergone curative resection: a prospective, multicenter, randomized, controlled trial.
      ,
      • Rosati G.
      • Ambrosini G.
      • Barni S.
      • Andreoni B.
      • Corradini G.
      • Luchena G.
      • et al.
      A randomized trial of intensive versus minimal surveillance of patients with resected Dukes B2-C colorectal carcinoma.
      ,
      • Treasure T.
      • Monson K.
      • Fiorentino F.
      • Russell C.
      The CEA Second-Look Trial: a randomised controlled trial of carcinoembryonic antigen prompted reoperation for recurrent colorectal cancer.
      ,
      • Wang T.
      • Cui Y.
      • Huang W.S.
      • Deng Y.H.
      • Gong W.
      • Li C.J.
      • et al.
      The role of postoperative colonoscopic surveillance after radical surgery for colorectal cancer: a prospective, randomized clinical study.
      ,
      • Wille-Jørgensen P.
      • Syk I.
      • Smedh K.
      • Laurberg S.
      • Nielsen D.T.
      • Petersen S.H.
      • 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.
      ], no significant impact on OS (HR 0.99, 95% CI 0.92–1.06) and CSS (0.94, 95% CI 0.77–1.16) was observed with little to no heterogeneity (I2 7% and 0%). All low risk studies evaluated frequency of follow-up, of which three evaluated a symptom-based approach without use of diagnostics [
      • Ohlsson B.
      • Breland U.
      • Ekberg H.
      • Graffner H.
      • Tranberg K.G.
      Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up.
      ,
      • Primrose J.N.
      • Perera R.
      • Gray A.
      • Rose P.
      • Fuller A.
      • Corkhill A.
      • et al.
      Effect of 3 to 5 years of scheduled CEA and CT follow-up to detect recurrence of colorectal cancer: the FACS randomized clinical trial.
      ,
      • Treasure T.
      • Monson K.
      • Fiorentino F.
      • Russell C.
      The CEA Second-Look Trial: a randomised controlled trial of carcinoembryonic antigen prompted reoperation for recurrent colorectal cancer.
      ]. Primrose et al. also compared CT and CEA as diagnostic modalities during surveillance [
      • Primrose J.N.
      • Perera R.
      • Gray A.
      • Rose P.
      • Fuller A.
      • Corkhill A.
      • et al.
      Effect of 3 to 5 years of scheduled CEA and CT follow-up to detect recurrence of colorectal cancer: the FACS randomized clinical trial.
      ]. Although survival was not significantly impacted by follow-up strategy, intensive follow-up remained significantly associated with the probability of curative intent treatment for recurrences (RR 1.30, 95% CI 1.05–1.61) in low risk studies (I2 28%).
      Twenty-five studies (76%) were deemed to be at high risk of bias, the majority being observational (N = 16, 64%) [
      • Augestad K.M.
      • Norum J.
      • Dehof S.
      • Aspevik R.
      • Ringberg U.
      • Nestvold T.
      • et al.
      Cost-effectiveness and quality of life in surgeon versus general practitioner-organised colon cancer surveillance: a randomised controlled trial.
      ,
      • Kjeldsen B.J.
      • Kronborg O.
      • Fenger C.
      • Jørgensen O.D.
      A prospective randomized study of follow-up after radical surgery for colorectal cancer.
      ,
      • Mäkelä J.T.
      • Laitinen S.O.
      • Kairaluoma M.I.
      Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial.
      ,
      • Pietra N.
      • Sarli L.
      • Costi R.
      • Ouchemi C.
      • Grattarola M.
      • Peracchia A.
      Role of follow-up in management of local recurrences of colorectal cancer: a prospective, randomized study.
      ,
      • Schoemaker D.
      • Black R.
      • Giles L.
      • Toouli J.
      Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients.
      ,
      • Secco G.B.
      • Fardelli R.
      • Gianquinto D.
      • Bonfante P.
      • Baldi E.
      • Ravera G.
      • et al.
      Efficacy and cost of risk-adapted follow-up in patients after colorectal cancer surgery: a prospective, randomized and controlled trial.
      ,
      • Sobhani I.
      • Itti E.
      • Luciani A.
      • Baumgaertner I.
      • Layese R.
      • André T.
      • et al.
      Colorectal cancer (CRC) monitoring by 6-monthly 18FDG-PET/CT: an open-label multicentre randomised trial.
      ,
      • Strand E.
      • Nygren I.
      • Bergkvist L.
      • Smedh K.
      Nurse or surgeon follow-up after rectal cancer: a randomized trial.
      ,
      • Wattchow D.A.
      • Weller D.P.
      • Esterman A.
      • Pilotto L.S.
      • McGorm K.
      • Hammett Z.
      • et al.
      General practice vs surgical-based follow-up for patients with colon cancer: randomised controlled trial.
      ]. Most high risk studies evaluated frequency of follow-up (N = 18, 72%) [
      • Bergamaschi R.
      • Arnaud J.P.
      Routine compared with nonscheduled follow-up of patients with "curative" surgery for colorectal cancer.
      ,
      • Borie F.
      • Daurès J.P.
      • Millat B.
      • Trétarre B.
      Cost and effectiveness of follow-up examinations in patients with colorectal cancer resected for cure in a French population-based study.
      ,
      • Castells A.
      • Bessa X.
      • Daniels M.
      • Ascaso C.
      • Lacy A.M.
      • García-Valdecasas J.C.
      • et al.
      Value of postoperative surveillance after radical surgery for colorectal cancer: results of a cohort study.
      ,
      • Coebergh van den Braak R.R.J.
      • Lalmahomed Z.S.
      • Büttner S.
      • Hansen B.E.
      • Ijzermans J.N.M.
      • Group M.S.
      Nonphysician clinicians in the follow-up of resected patients with colorectal cancer.
      ,
      • Eckardt V.F.
      • Stamm H.
      • Kanzler G.
      • Bernhard G.
      Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program.
      ,
      • Gamboa A.C.
      • Zaidi M.Y.
      • Lee R.M.
      • Speegle S.
      • Switchenko J.M.
      • Lipscomb J.
      • et al.
      Optimal surveillance frequency after CRS/HIPEC for appendiceal and colorectal neoplasms: a multi-institutional analysis of the US HIPEC collaborative.
      ,
      • Hines R.B.
      • Jiban M.J.H.
      • Specogna A.V.
      • Vishnubhotla P.
      • Lee E.
      • Zhang S.
      The association between post-treatment surveillance testing and survival in stage II and III colon cancer patients: an observational comparative effectiveness study.
      ,
      • Hines R.B.
      • Jiban M.J.H.
      • Specogna A.V.
      • Vishnubhotla P.
      • Lee E.
      • Troy S.P.
      • et al.
      Surveillance colonoscopy in older stage I colon cancer patients and the association with colon cancer-specific mortality.
      ,
      • Hyder O.
      • Dodson R.M.
      • Mayo S.C.
      • Schneider E.B.
      • Weiss M.J.
      • Herman J.M.
      • et al.
      Post-treatment surveillance of patients with colorectal cancer with surgically treated liver metastases.
      ,
      • Kjeldsen B.J.
      • Kronborg O.
      • Fenger C.
      • Jørgensen O.D.
      A prospective randomized study of follow-up after radical surgery for colorectal cancer.
      ,
      • Körner H.
      • Söreide K.
      • Stokkeland P.J.
      • Söreide J.A.
      Systematic follow-up after curative surgery for colorectal cancer in Norway: a population-based audit of effectiveness, costs, and compliance.
      ,
      • Laubert T.
      • Bader F.G.
      • Oevermann E.
      • Jungbluth T.
      • Unger L.
      • Roblick U.J.
      • et al.
      Intensified surveillance after surgery for colorectal cancer significantly improves survival.
      ,
      • Mahboubi A.
      • Lejeune C.
      • Coriat R.
      • Binquet C.
      • Bouvier A.M.
      • Béjean S.
      • et al.
      Which patients with colorectal cancer are followed up by general practitioners? A population-based study.
      ,
      • Mäkelä J.T.
      • Laitinen S.O.
      • Kairaluoma M.I.
      Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial.
      ,
      • Ovaska J.
      • Järvinen H.
      • Kujari H.
      • Perttilä I.
      • Mecklin J.P.
      Follow-up of patients operated on for colorectal carcinoma.
      ,
      • Pugliese V.
      • Aste H.
      • Saccomanno S.
      • Bruzzi P.
      • Bonelli L.
      • Santi L.
      Outcome of follow-up programs in patients previously resected for colorectal cancer.
      ,
      • Rulyak S.J.
      • Lieberman D.A.
      • Wagner E.H.
      • Mandelson M.T.
      Outcome of follow-up colon examination among a population-based cohort of colorectal cancer patients.
      ,
      • Secco G.B.
      • Fardelli R.
      • Gianquinto D.
      • Bonfante P.
      • Baldi E.
      • Ravera G.
      • et al.
      Efficacy and cost of risk-adapted follow-up in patients after colorectal cancer surgery: a prospective, randomized and controlled trial.
      ]. Pooled effect estimates in high risk colorectal cancer studies were larger for all outcomes evaluated, with considerable heterogeneity (Table 3).

      3.3 Lung cancer

      Within the thirteen lung cancer studies, 26,162 patients were included (Table 2). All of the studies identified were considered to be at high risk of bias, including two RCTs [
      • Monteil J.
      • Vergnenègre A.
      • Bertin F.
      • Dalmay F.
      • Gaillard S.
      • Bonnaud F.
      • et al.
      Randomized follow-up study of resected NSCLC patients: conventional versus 18F-DG coincidence imaging.
      ,
      • Sui Y.
      • Wang T.
      • Wang X.
      The impact of WeChat app-based education and rehabilitation program on anxiety, depression, quality of life, loss of follow-up and survival in non-small cell lung cancer patients who underwent surgical resection.
      ]. Five studies assessed frequency of follow-up [
      • Backhus L.M.
      • Farjah F.
      • Liang C.K.
      • He H.
      • Varghese Jr., T.K.
      • Au D.H.
      • et al.
      Imaging surveillance and survival for surgically resected non-small-cell lung cancer.
      ,
      • Ho C.
      • Siegfried J.
      • Remo K.
      • Laskin J.
      Adherence to surveillance guidelines in resected NSCLC: physician compliance and impact on outcomes.
      ,
      • Mayne N.R.
      • Mallipeddi M.K.
      • Darling A.J.
      • Jeffrey Yang C.F.
      • Eltaraboulsi W.R.
      • Shoffner A.R.
      • et al.
      Impact of surveillance after lobectomy for lung cancer on disease detection and survival.
      ,
      • McMurry T.L.
      • Stukenborg G.J.
      • Kessler L.G.
      • Colditz G.A.
      • Wong M.L.
      • Francescatti A.B.
      • et al.
      More frequent surveillance following lung cancer resection is not associated with improved survival: a nationally representative cohort study.
      ,
      • Virgo K.S.
      • McKirgan L.W.
      • Caputo M.C.
      • Mahurin D.M.
      • Chao L.C.
      • Caputo N.A.
      • et al.
      Post-treatment management options for patients with lung cancer.
      ], five the modalities used [
      • Crabtree T.D.
      • Puri V.
      • Chen S.B.
      • Gierada D.S.
      • Bell J.M.
      • Broderick S.
      • et al.
      Does the method of radiologic surveillance affect survival after resection of stage I non-small cell lung cancer?.
      ,
      • Karzijn R.
      • Alberts L.
      • Kelder J.C.
      • Hofman F.N.
      • El Sharouni S.Y.
      • Kastelijn E.A.
      • et al.
      Post-treatment surveillance for stage I and II non-small cell lung cancer: impact on clinical outcome.
      ,
      • Monteil J.
      • Vergnenègre A.
      • Bertin F.
      • Dalmay F.
      • Gaillard S.
      • Bonnaud F.
      • et al.
      Randomized follow-up study of resected NSCLC patients: conventional versus 18F-DG coincidence imaging.
      ,
      • Pan Y.
      • Brink C.
      • Schytte T.
      • Petersen H.
      • Wu Y.L.
      • Hansen O.
      Planned FDG PET-CT scan in follow-up detects disease progression in patients with locally advanced NSCLC receiving curative chemoradiotherapy earlier than standard CT.
      ,
      • Reddy J.P.
      • Tang C.
      • Shih T.
      • Kim B.
      • Kim C.
      • Nguyen Q.N.
      • et al.
      Influence of surveillance PET/CT on detection of early recurrence after definitive radiation in stage III non-small-cell lung cancer.
      ], one the setting in which follow-up was performed [
      • Sui Y.
      • Wang T.
      • Wang X.
      The impact of WeChat app-based education and rehabilitation program on anxiety, depression, quality of life, loss of follow-up and survival in non-small cell lung cancer patients who underwent surgical resection.
      ], and two evaluated multiple aspects [
      • Benamore R.
      • Shepherd F.A.
      • Leighl N.
      • Pintilie M.
      • Patel M.
      • Feld R.
      • et al.
      Does intensive follow-up alter outcome in patients with advanced lung cancer?.
      ,
      • Nakamura R.
      • Kurishima K.
      • Kobayashi N.
      • Ishikawa S.
      • Goto Y.
      • Sakai M.
      • et al.
      Postoperative follow-up for patients with non-small cell lung cancer.
      ]. Follow-up did not significantly impact OS (HR 0.94, 95% CI 0.84–1.05) (Table 3). Heterogeneity was moderate (I2 49%). Only one study reported on CSS, in which no significant survival difference was obtained [
      • Crabtree T.D.
      • Puri V.
      • Chen S.B.
      • Gierada D.S.
      • Bell J.M.
      • Broderick S.
      • et al.
      Does the method of radiologic surveillance affect survival after resection of stage I non-small cell lung cancer?.
      ]. Intensive follow-up did not increase curative treatment rates (RR 1.34, 95% CI 0.82–2.20, I2 39%), as reported in four studies [
      • Benamore R.
      • Shepherd F.A.
      • Leighl N.
      • Pintilie M.
      • Patel M.
      • Feld R.
      • et al.
      Does intensive follow-up alter outcome in patients with advanced lung cancer?.
      ,
      • Crabtree T.D.
      • Puri V.
      • Chen S.B.
      • Gierada D.S.
      • Bell J.M.
      • Broderick S.
      • et al.
      Does the method of radiologic surveillance affect survival after resection of stage I non-small cell lung cancer?.
      ,
      • Ho C.
      • Siegfried J.
      • Remo K.
      • Laskin J.
      Adherence to surveillance guidelines in resected NSCLC: physician compliance and impact on outcomes.
      ,
      • Mayne N.R.
      • Mallipeddi M.K.
      • Darling A.J.
      • Jeffrey Yang C.F.
      • Eltaraboulsi W.R.
      • Shoffner A.R.
      • et al.
      Impact of surveillance after lobectomy for lung cancer on disease detection and survival.
      ].

      3.4 Breast cancer

      In total 10,585 breast cancer patients were included in eleven studies (Table 1, Table 2). Across all studies no significant impact of intensive follow-up on OS (HR 0.80, 95% CI 0.54–1.18) or CSS (HR 0.52, 95% CI 0.27–1.02) was observed (Table 3). Heterogeneity was considerable for both outcomes (I2 92% and 94%). None of the studies reported on the (curative) treatment for local recurrence or metastatic disease.
      Four studies (36%) were considered to be at low risk of bias, including two RCTs [
      • Rosselli Del Turco M.
      • Palli D.
      • Cariddi A.
      • Ciatto S.
      • Pacini P.
      • Distante V.
      Intensive diagnostic follow-up after treatment of primary breast cancer. A randomized trial. National Research Council Project on Breast Cancer follow-up.
      ,
      Impact of follow-up testing on survival and health-related quality of life in breast cancer patients. A multicenter randomized controlled trial. The GIVIO Investigators.
      ], one long-term update of an RCT [
      • Palli D.
      • Russo A.
      • Saieva C.
      • Ciatto S.
      • Rosselli Del Turco M.
      • Distante V.
      • et al.
      Intensive vs clinical follow-up after treatment of primary breast cancer: 10-year update of a randomized trial. National Research Council Project on Breast Cancer Follow-up.
      ], and one prospective observational study [
      • Bornhak S.
      • Heidemann E.
      • Herschlein H.J.
      • Simon W.
      • Merkle E.
      • Widmaier G.
      • et al.
      Symptom-oriented follow-up of early breast cancer is not inferior to conventional control. Results of a prospective multicentre study.
      ]. All low risk studies compared different modalities used in the same frequency, generally every 3–6 months. When pooling the effects of individual studies, no impact on OS was observed (pooled HR 1.06, 95% CI 0.92–1.23), with no heterogeneity (I2 0%). None observed significant additional value of using multiple diagnostics (e.g. liver ultrasonography, chest radiography, laboratory tests) next to clinical examinations and mammography's. None of the studies reported on CSS.
      Most of the seven high risk studies were observational (71%) [
      • Grunfeld E.
      • Levine M.N.
      • Julian J.A.
      • Coyle D.
      • Szechtman B.
      • Mirsky D.
      • et al.
      Randomized trial of long-term follow-up for early-stage breast cancer: a comparison of family physician versus specialist care.
      ,
      • Koinberg I.L.
      • Fridlund B.
      • Engholm G.B.
      • Holmberg L.
      Nurse-led follow-up on demand or by a physician after breast cancer surgery: a randomised study.
      ]. In contrast to the low risk studies, all of the observational studies evaluated the frequency of follow-up, while the RCTs evaluated setting of follow-up. The randomised studies found no impact on OS when follow-up was performed by the family physician (HR 1.05, 95% CI 0.60–1.84) or the nurse practitioner (HR 1.22, 95% CI 0.58–2.57), compared to the standard hospital-based physician-led approach [
      • Grunfeld E.
      • Levine M.N.
      • Julian J.A.
      • Coyle D.
      • Szechtman B.
      • Mirsky D.
      • et al.
      Randomized trial of long-term follow-up for early-stage breast cancer: a comparison of family physician versus specialist care.
      ,
      • Koinberg I.L.
      • Fridlund B.
      • Engholm G.B.
      • Holmberg L.
      Nurse-led follow-up on demand or by a physician after breast cancer surgery: a randomised study.
      ]. The studies evaluating the frequency of follow-up all assessed the impact of receiving one or more diagnostic evaluations (i.e. mammography or multiple diagnostics) to a nihilistic approach [
      • Lash T.L.
      • Clough-Gorr K.
      • Silliman R.A.
      Reduced rates of cancer-related worries and mortality associated with guideline surveillance after breast cancer therapy.
      ,
      • Lash T.L.
      • Fox M.P.
      • Silliman R.A.
      Reduced mortality rate associated with annual mammograms a