Follow-Up after Curative Surgical Treatment of Soft-Tissue Sarcoma for Early Detection of Recurrence: Which Patients Have More or Fewer Visits than Advised in Guidelines?
Abstract
:Simple Summary
Abstract
1. Introduction
2. Methods
2.1. Study Design and Patient Population
2.2. Definitions
2.3. Patient, Tumor and Treatment Characteristics
2.4. Statistical Analysis
3. Results
3.1. Patient Characteristics, Follow-Up Visits, and Incidence of Recurrence
3.2. Type of Patients Receiving More or Fewer Follow-Up Visits
3.3. Type of Patients Receiving More or Fewer Follow-Up Visits in Relation to Recurrence
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer Statistics. Ca-A Cancer J. Clin. 2021, 71, 7–33. [Google Scholar] [CrossRef] [PubMed]
- Stiller, C.A.; Trama, A.; Serraino, D.; Rossi, S.; Navarro, C.; Chirlaque, M.D.; Casali, P.G.; Grp, R.W. Descriptive epidemiology of sarcomas in Europe: Report from the RARECARE project. Eur. J. Cancer 2013, 49, 684–695. [Google Scholar] [CrossRef] [PubMed]
- Picci, P. Epidemiology of Soft Tissue Lesions. In Diagnosis of Musculoskeletal Tumors and Tumor-like Conditions: Clinical, Radiological and Histological Correlations—The Rizzoli Case Archive; Picci, P., Manfrini, M., Donati, D.M., Gambarotti, M., Righi, A., Vanel, D., Tos, A.P.D., Eds.; Springer International Publishing: Cham, Switzerland, 2020; pp. 15–18. [Google Scholar]
- Casali, P.G.; Abecassis, N.; Bauer, S.; Biagini, R.; Bielack, S.; Bonvalot, S.; Boukovinas, I.; Bovee, J.V.M.G.; Brodowicz, T.; Martin-Broto, J.; et al. Soft tissue and visceral sarcomas: ESMO-EURACAN Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 2018, 29, 51–67. [Google Scholar] [CrossRef]
- Whooley, B.P.; Mooney, M.M.; Gibbs, J.F.; Kraybill, W.G. Effective follow-up strategies in soft tissue sarcoma. Semin. Surg. Oncol. 1999, 17, 83–87. [Google Scholar] [CrossRef]
- Fletcher, C.D.M. WHO Classification of Tumours of Soft Tissue and Bone, 4th ed.; IARC Press: Lyon, France, 2013. [Google Scholar]
- Kane, J.M. Surveillance strategies for patients following surgical resection of soft tissue sarcomas. Curr. Opin. Oncol. 2004, 16, 328–332. [Google Scholar] [CrossRef] [PubMed]
- Whooley, B.P.; Gibbs, J.F.; Mooney, M.M.; McGrath, B.E.; Kraybill, W.G. Primary extremity sarcoma: What is the appropriate follow-up? Ann. Surg. Oncol. 2000, 7, 9–14. [Google Scholar] [CrossRef] [PubMed]
- Richardson, K.; Potter, M.; Damron, T.A. Image Intensive Soft Tissue Sarcoma Surveillance Uncovers Pathology Earlier Than Patient Complaints But with Frequent Initially Indeterminate Lesions. J. Surg. Oncol. 2016, 113, 818–822. [Google Scholar] [CrossRef]
- Goel, A.; Christy, M.E.L.; Virgo, K.S.; Kraybill, W.G.; Johnson, F.E. Costs of follow-up after potentially curative treatment for extremity soft-tissue sarcoma. Int. J. Oncol. 2004, 25, 429–435. [Google Scholar] [CrossRef] [PubMed]
- von Mehren, M.; Kane, J.M.; Agulnik, M.; Bui, M.M.; Carr-Ascher, J.; Choy, E.; Connelly, M.; Dry, S.; Ganjoo, K.N.; Gonzalez, R.J.; et al. Soft Tissue Sarcoma, Version 2.2022, NCCN Clinical Practice Guidelines in Oncology. J. Natl. Compr. Cancer Netw. 2022, 20, 815–833. [Google Scholar] [CrossRef]
- Greenberg, D.D.; Crawford, B. Surveillance Strategies for Sarcoma: Results of a Survey of Members of the Musculoskeletal Tumor Society. Sarcoma 2016, 2016, 8289509. [Google Scholar] [CrossRef]
- Gerrand, C.H.; Billingham, L.J.; Woll, P.J.; Grimer, R.J. Follow up after Primary Treatment of Soft Tissue Sarcoma: A Survey of Current Practice in the United Kingdom. Sarcoma 2007, 2007, 34128. [Google Scholar] [CrossRef]
- Team, R.D.C. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2009; Available online: http://www.R-project.org (accessed on 1 April 2023).
- Callegaro, D.; Miceli, R.; Bonvalot, S.; Ferguson, P.; Strauss, D.C.; Levy, A.; Griffin, A.; Hayes, A.J.; Stacchiotti, S.; Pechoux, C.L.; et al. Development and external validation of two nomograms to predict overall survival and occurrence of distant metastases in adults after surgical resection of localised soft-tissue sarcomas of the extremities: A retrospective analysis. Lancet Oncol. 2016, 17, 671–680. [Google Scholar] [CrossRef] [PubMed]
- Kattan, M.W.; Leung, D.H.Y.; Brennan, M.F. Postoperative nomogram for 12-year sarcoma-specific death. J. Clin. Oncol. 2002, 20, 791–796. [Google Scholar] [CrossRef]
- Smolle, M.A.; Sande, M.V.; Callegaro, D.; Wunder, J.; Hayes, A.; Leitner, L.; Bergovec, M.; Tunn, P.U.; van Praag, V.; Fiocco, M.; et al. Individualizing Follow-Up Strategies in High-Grade Soft Tissue Sarcoma with Flexible Parametric Competing Risk Regression Models. Cancers 2019, 12, 47. [Google Scholar] [CrossRef] [PubMed]
- van Praag, V.M.; Rueten-Budde, A.J.; Jeys, L.M.; Laitinen, M.K.; Pollock, R.; Aston, W.; van der Hage, J.A.; Dijkstra, P.D.S.; Ferguson, P.C.; Griffin, A.M.; et al. A prediction model for treatment decisions in high-grade extremity soft-tissue sarcomas: Personalised sarcoma care (PERSARC). Eur. J. Cancer 2017, 83, 313–323. [Google Scholar] [CrossRef]
- Armes, J.; Crowe, M.; Colbourne, L.; Morgan, H.; Murrells, T.; Oakley, C.; Palmer, N.; Ream, E.; Young, A.; Richardson, A. Patients’ Supportive Care Needs Beyond the End of Cancer Treatment: A Prospective, Longitudinal Survey. J. Clin. Oncol. 2009, 27, 6172–6179. [Google Scholar] [CrossRef] [PubMed]
- Draeger, T.; Voelkel, V.; Schreuder, K.; Veltman, J.; Dassen, A.; Strobbe, L.; Heijmans, H.J.; Koelemij, R.; Groothuis-Oudshoorn, C.G.M.; Siesling, S. Adherence to the Dutch Breast Cancer Guidelines for Surveillance in Breast Cancer Survivors: Real-World Data from a Pooled Multicenter Analysis. Oncologist 2022, 27, E766–E773. [Google Scholar] [CrossRef]
- Damery, S.; Biswas, M.; Billingham, L.; Barton, P.; Al-Janabi, H.; Grimer, R. Patient preferences for clinical follow-up after primary treatment for soft tissue sarcoma: A cross-sectional survey and discrete choice experiment. Eur. J. Surg. Oncol. 2014, 40, 1655–1661. [Google Scholar] [CrossRef] [PubMed]
- Tarrant, C.; Krockow, E.M. Antibiotic overuse: Managing uncertainty and mitigating against overtreatment. BMJ Qual. Saf. 2022, 31, 163–167. [Google Scholar] [CrossRef] [PubMed]
- Helfrich, C.D.; Rose, A.J.; Hartmann, C.W.; van Bodegom-Vos, L.; Graham, I.D.; Wood, S.J.; Majerczyk, B.R.; Good, C.B.; Pogach, L.M.; Ball, S.L.; et al. How the dual process model of human cognition can inform efforts to de-implement ineffective and harmful clinical practices: A preliminary model of unlearning and substitution. J. Eval. Clin. Pract. 2018, 24, 198–205. [Google Scholar] [CrossRef]
- van Bodegom-Vos, L.; de Mheen, P.M.-V. Reducing Low-Value Care: Uncertainty as Crucial Cross-Cutting Theme; Comment on “Key Factors That Promote Low-Value Care: Views of Experts from the United States, Canada, and the Netherlands”. Int. J. Health Policy Manag. 2022, 11, 1964. [Google Scholar] [CrossRef]
- Bozzo, A.; Baldawi, H.; Simchovich, G.; Ghert, M. Optimal surveillance strategies following curative surgery for extremity sarcoma: A systematic review of Randomized Control Trials. 2018. Available online: osf.io/7t64v (accessed on 10 September 2023).
- Brennan, M.F. Follow-up is valuable and effective: True, true and unrelated? Ann. Surg. Oncol. 2000, 7, 2–3. [Google Scholar] [CrossRef] [PubMed]
- Acem, I.; Smit, M.M.; Verhoef, C.; van Houdt, W.J.; Haas, R.L.; van der Hage, J.A.; Grunhagen, D.J.; van de Sande, M.A.J. Management of Soft Tissue Sarcomas in Extremities: Variation in Treatment Recommendations and Surveillance according to Specialty and Continent. Ann. Surg. Oncol. 2021, 28, 7923–7936. [Google Scholar] [CrossRef] [PubMed]
- Schneider, P.J.; Evaniew, N.; McKay, P.; Ghert, M. Moving Forward Through Consensus: A Modified Delphi Approach to Determine the Top Research Priorities in Orthopaedic Oncology. Clin. Orthop. Relat. Res. 2017, 475, 3044–3055. [Google Scholar] [CrossRef]
- Grunfeld, E.; Hodgson, D.C.; Del Giudice, M.E.; Moineddin, R. Population-based longitudinal study of follow-up care for breast cancer survivors. J. Oncol. Pract. 2010, 6, 174–181. [Google Scholar] [CrossRef] [PubMed]
- Rueten-Budde, A.J.; van Praag, V.M.; PERSARC studygroup; van de Sande, M.A.J.; Fiocco, M. Dynamic prediction of overall survival for patients with high-grade extremity soft tissue sarcoma. Surg. Oncol. 2018, 27, 695–701. [Google Scholar] [CrossRef] [PubMed]
- Danieli, M.; Gronchi, A. Staging Systems and Nomograms for Soft Tissue Sarcoma. Curr. Oncol. 2023, 30, 3648–3671. [Google Scholar] [CrossRef] [PubMed]
- Acem, I.; van de Sande, M.A.J. Prediction tools for the personalized management of soft-tissue sarcomas of the extremity. Bone Jt. J. 2022, 104, 1011–1016. [Google Scholar] [CrossRef]
Follow-Up | Frequency of Visits in Years 1–3 | Frequency of Visits in Years 4–5 |
---|---|---|
ESMO | Every 3–4 months | Every 6 months |
NCCN | Every 3–6 months | High grade—every 6 months Low grade—annually |
Local guideline | Every 4 months | Every 6 months |
Variables | Soft-Tissue Tumor Patients N (%) |
---|---|
Age at surgery (years) median ± IQR | 60 (46–71) |
Sex Male | 200 (51) |
Histology (most common) Myxofibrosarcoma Liposarcoma Leiomyosarcoma Myxoid liposarcoma Synovial sarcoma Spindle cell sarcoma Other | 78 (20) 61 (16) 50 (13) 39 (10) 26 (6.6) 10 (3) 118 (30) |
Tumor location Lower extremities Upper extremities Pelvis Other | 272 (69) 64 (16) 31 (8) 28 (7) |
Tumor size (cm) Median ± IQR | 7 (5–13) |
Grading High grade (II-III) Low grade (I) Unable to classify | 250 (64) 138 (35) 6 (1.5) |
Surgical margins R0 R1–2 Unknown | 251 (63) 127 (32) 18 (5) |
RTX Pre-operative Post-operative | N = 102 33 (32) 69 (67) |
Year 1 | Year 2 | Year 3 | Year 4 | Year 5 | ||
---|---|---|---|---|---|---|
n at risk * | 394 | 309 | 257 | 226 | 202 | |
Follow-up versus guidelines | ||||||
Fewer than guidelines | 185 (47%) | 161 (52%) | 187 (73%) | 191 (85%) | 130 (64%) | |
Following guidelines | 93 (24%) | 62 (20%) | 38 (15%) | 19 (8%) | 44 (22%) | |
More than guidelines | 116 (29%) | 86 (28%) | 32 (13%) | 16 (7%) | 28 (14%) | |
Median age (IQR) | ||||||
Fewer than guidelines | 62 (50–73) | 60 (47–70) | 58 (44–69) | 59 (46–70) | 57 (44–69) | |
Following guidelines | 61 (43–72) | 61 (48–72) | 54 (40–68) | 52 (41–65) | 49 (39–63) | |
More than guidelines | 54 (42–67) | 56 (43–68) | 57 (47–64) | 55 (43–63) | 57 (51–64) | |
Male gender in % | ||||||
Fewer than guidelines | 49% | 50% | 49% | 48% | 53% | |
Following guidelines | 41% | 44% | 52% | 66% | 54% | |
More than guidelines | 61% | 56% | 63% | 50% | 55% | |
High grade of tumor in % | ||||||
Fewer than guidelines | 79 (43%) | 105 (48%) | 105 (48%) | 64 (42%) | 61 (42%) | |
Following guidelines | 70 (75%) | 36 (72%) | 17 (74%) | 28 (60%) | 25 (68%) | |
More than guidelines | 101 (87%) | 31 (80%) | 12 (75%) | 21 (75%) | 17 (85%) | |
Tumor size (IQR) | ||||||
Fewer than guidelines | 8 (5–13) | 7 (4–13) | 7 (4–13) | 8 (5–13) | 8 (4–13) | |
Following guidelines | 7 (4–12) | 6 (5–11) | 6 (5–10) | 6 (4–10) | 6 (5–12) | |
More than guidelines | 8 (5–14) | 8 (5–12) | 11 (5–17) | 7 (5–15) | 10 (3–17) | |
Free surgical margins in % | ||||||
Fewer than guidelines | 105 (61%) | 134 (61%) | 136 (62%) | 91 (60%) | 83 (64%) | |
Following guidelines | 60 (70%) | 34 (68%) | 20 (87%) | 34 (72%) | 32 (84%) | |
More than guidelines | 86 (71%) | 30 (77%) | 14 (88%) | 22 (79%) | 15 (75%) | |
Radiotherapy in % | ||||||
Fewer than guidelines | 27 (14%) | 37 (17%) | 48 (22%) | 30 (20%) | 33 (23%) | |
Following guidelines | 31 (33%) | 22 (44%) | 10 (44%) | 21 (45%) | 17 (46%) | |
More than guidelines | 44 (38%) | 18 (46%) | 8 (50%) | 11 (40%) | 12 (60%) |
Year 1 | Year 2 | Year 3 | Year 4 | Year 5 | ||
---|---|---|---|---|---|---|
n at risk * | 394 | 309 | 257 | 226 | 202 | |
Total recurrences ** | 62 | 30 | 8 | 4 | 6 | |
Fewer than guidelines | 6 (10%) | 12 (40%) | 5 (63%) | 2 (50%) | 4 (66%) | |
Within guidelines | 28 (45%) | 12 (40%) | 3 (37%) | 2 (50%) | 1 (17%) | |
More than guidelines | 28 (45%) | 6 (20%) | 0 (0%) | 0 (0%) | 1 (17%) | |
Median age (IQR) | ||||||
Fewer than guidelines | 72 (65–79) | 73 (68–79) | 69 (63–76) | 71 (68–75) | 56 (35–73) | |
Within guidelines | 60 (43–68) | 68 (55–77) | 64 (51–68) | 63 (54–71) | 64 | |
More than guidelines | 55 (42–70) | 64 (59–73) | - | - | 23 | |
Male gender in % | ||||||
Fewer than guidelines | 4 (67%) | 4 (33%) | 2 (40%) | - | 3 (75%) | |
Within guidelines | 10 (36%) | 3 (25%) | 2 (67%) | 2 (100%) | 1 (100%) | |
More than guidelines | 21 (75%) | 4 (67%) | - | - | 1 (100%) | |
High grade of tumor in % | ||||||
Fewer than guidelines | 5 (83%) | 10 (83%) | 4 (80%) | - | 2 (50%) | |
Within guidelines | 27 (96%) | 7 (53%) | 3 (100%) | 1 (50%) | - | |
More than guidelines | 26 (93%) | 6 (100%) | - | - | 1 (100%) | |
Tumor size (IQR) | ||||||
Fewer than guidelines | 9 (7–11) | 9 (6–12) | 5 (5–7) | 7 (4–9) | 10 (9–12) | |
Within guidelines | 9 (5–15) | 6 (5–8) | 9 (7–10) | 5 (5–6) | 6 | |
More than guidelines | 10 (6–15) | 11 (7–14) | - | - | 18 | |
Free surgical margins in % | ||||||
Fewer than guidelines | 5 (83%) | 6 (50%) | 3 (60%) | 1 (50%) | 2 (50%) | |
Within guidelines | 15 (54%) | 7 (58%) | 2 (67%) | 2 (100%) | - | |
More than guidelines | 17 (61%) | 4 (67%) | - | - | 1 (100%) | |
Radiotherapy in % | ||||||
Fewer than guidelines | 2 (33%) | 3 (25%) | 2 (40%) | - | - | |
Within guidelines | 13 (46%) | 5 (42%) | 2 (67%) | - | - | |
More than guidelines | 8 (29%) | 3 (50%) | - | - | - |
Year 1 | Year 2 | Year 3 | Year 4 | Year 5 | ||
---|---|---|---|---|---|---|
n at risk * | 394 | 309 | 258 | 226 | 202 | |
No recurrences ** | 336 | 258 | 226 | 202 | 168 | |
Fewer than guidelines | 161 (51%) | 182 (73%) | 191 (85%) | 130 (64%) | 118 (70%) | |
Within guidelines | 62 (20%) | 38 (15%) | 19 (8%) | 44 (22%) | 35 (21%) | |
More than guidelines | 86 (28%) | 32 (13%) | 16 (7%) | 28 (14%) | 15 (9%) | |
Median age (IQR) | ||||||
Fewer than guidelines | 61 (49–72) | 58 (44–69) | 57 (44–68) | 57 (45–70) | 57 (44–67) | |
Within guidelines | 64 (44–72) | 59 (46–69) | 52 (38–68) | 52 (40–65) | 48 (39–62) | |
More than guidelines | 53 (39–64) | 53 (44–68) | 57 (47–64) | 55 (43–63) | 55 (51–62) | |
Male gender in % | ||||||
Fewer than guidelines | 78 (48%) | 93 (50%) | 97 (51%) | 65 (50%) | 60 (51%) | |
Within guidelines | 27 (44%) | 19 (50%) | 10 (53%) | 28 (64%) | 19 (54%) | |
More than guidelines | 49 (57%) | 17 (53%) | 10 (63%) | 14 (50%) | 8 (53%) | |
High grade of tumor in % | ||||||
Fewer than guidelines | 57 (35%) | 81 (43%) | 88 (46%) | 55 (42%) | 44 (37%) | |
Within guidelines | 41 (66%) | 29 (29%) | 13 (68%) | 27 (61%) | 25 (71%) | |
More than guidelines | 74 (86%) | 24 (75%) | 12 (75%) | 21 (75%) | 12 (80%) | |
Tumor size (IQR) | ||||||
Fewer than guidelines | 8 (5–14) | 7 (5–13) | 7 (4–13) | 8 (5–13) | 8 (5–14) | |
Within guidelines | 6 (4–9) | 5 (4–12) | 6 (5–10) | 6 (4–13) | 6 (5–13) | |
More than guidelines | 7 (4–13) | 8 (4–12) | 11 (5–17) | 7 (5–15) | 9 (3–17) | |
Free surgical margins in % | ||||||
Fewer than guidelines | 91 (57%) | 117 (63%) | 116 (61%) | 76 (59%) | 68 (58%) | |
Within guidelines | 42 (68%) | 27 (71%) | 17 (90%) | 32 (73%) | 30 (86%) | |
More than guidelines | 65 (76%) | 26 (81%) | 14 (88%) | 22 (79%) | 11 (73%) | |
Radiotherapy in % | ||||||
Fewer than guidelines | 23 (14%) | 34 (18%) | 46 (24%) | 30 (23%) | 23 (20%) | |
Within guidelines | 18 (29%) | 17 (45%) | 8 (42%) | 21 (48%) | 17 (49%) | |
More than guidelines | 36 (42%) | 15 (47%) | 8 (50%) | 11 (39%) | 10 (67%) |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kruiswijk, A.A.; Kuhrij, L.S.; Dorleijn, D.M.J.; van de Sande, M.A.J.; van Bodegom-Vos, L.; Marang-van de Mheen, P.J. Follow-Up after Curative Surgical Treatment of Soft-Tissue Sarcoma for Early Detection of Recurrence: Which Patients Have More or Fewer Visits than Advised in Guidelines? Cancers 2023, 15, 4617. https://doi.org/10.3390/cancers15184617
Kruiswijk AA, Kuhrij LS, Dorleijn DMJ, van de Sande MAJ, van Bodegom-Vos L, Marang-van de Mheen PJ. Follow-Up after Curative Surgical Treatment of Soft-Tissue Sarcoma for Early Detection of Recurrence: Which Patients Have More or Fewer Visits than Advised in Guidelines? Cancers. 2023; 15(18):4617. https://doi.org/10.3390/cancers15184617
Chicago/Turabian StyleKruiswijk, Anouk A., Laurien S. Kuhrij, Desiree M. J. Dorleijn, Michiel A. J. van de Sande, Leti van Bodegom-Vos, and Perla J. Marang-van de Mheen. 2023. "Follow-Up after Curative Surgical Treatment of Soft-Tissue Sarcoma for Early Detection of Recurrence: Which Patients Have More or Fewer Visits than Advised in Guidelines?" Cancers 15, no. 18: 4617. https://doi.org/10.3390/cancers15184617