Top

The European Journal of Health Economics

Published in:

Open Access 01-09-2020 | Colon Cancer | Original Paper

Modeling Personalized Adjuvant TreaTment in EaRly stage coloN cancer (PATTERN)

Authors: Gabrielle Jongeneel, Marjolein J. E. Greuter, Felice N. van Erning, Miriam Koopman, Jan P. Medema, Raju Kandimalla, Ajay Goel, Luis Bujanda, Gerrit A. Meijer, Remond J. A. Fijneman, Martijn G. H. van Oijen, Jan Ijzermans, Cornelis J. A. Punt, Geraldine R. Vink, Veerle M. H. Coupé

Published in: The European Journal of Health Economics | Issue 7/2020

Abstract

Aim

To develop a decision model for the population-level evaluation of strategies to improve the selection of stage II colon cancer (CC) patients who benefit from adjuvant chemotherapy.

Methods

A Markov cohort model with a one-month cycle length and a lifelong time horizon was developed. Five health states were included; diagnosis, 90-day mortality, death other causes, recurrence and CC death. Data from the Netherlands Cancer Registry were used to parameterize the model. Transition probabilities were estimated using parametric survival models including relevant clinical and pathological covariates. Subsequently, biomarker status was implemented using external data. Treatment effect was incorporated using pooled trial data. Model development, data sources used, parameter estimation, and internal and external validation are described in detail. To illustrate the use of the model, three example strategies were evaluated in which allocation of treatment was based on (A) 100% adherence to the Dutch guidelines, (B) observed adherence to guideline recommendations and (C) a biomarker-driven strategy.

Results

Overall, the model showed good internal and external validity. Age, tumor growth, tumor sidedness, evaluated lymph nodes, and biomarker status were included as covariates. For the example strategies, the model predicted 83, 87 and 77 CC deaths after 5 years in a cohort of 1000 patients for strategies A, B and C, respectively.

Conclusion

This model can be used to evaluate strategies for the allocation of adjuvant chemotherapy in stage II CC patients. In future studies, the model will be used to estimate population-level long-term health gain and cost-effectiveness of biomarker-based selection strategies.

Available only for authorised users

Integraal Kankercentrum Nederland. Cijfers over kanker. http://www.iknl.nl. Accessed 1 June 2019

Kahi, C.J., Anderson, J.C.: 36 - Colorectal cancer screening and surveillance. In: Chandrasekhara, V., Joseph Elmunzer, B., Khashab, M.A., Raman Muthusamy, V . (eds.) Clinical Gastrointestinal Endoscopy (3rd edn), pp. 392–401. Elsevier (2019). https://doi.org/10.1016/B978-0-323-41509-5.00036-0

Eijsden, V.P., Mevius, L., Zaat, J.: Bevolkingsonderzoek naar darmkanker. Ned Tijdschr Geneeskd 159, 8844 (2015)

André, T., Boni, C., Mounedji-Boudiaf, L., Navarro, M., Tabernero, J., Hickish, T., Topham, C., Zaninelli, M., Clingan, P., Bridgewater, J.: Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N. Engl. J. Med. 350(23), 2343–2351 (2004)PubMedCrossRef

Labianca, R., Nordlinger, B., Beretta, G.D., Mosconi, S., Mandala, M., Cervantes, A., Arnold, D.: Early colon cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 24(Suppl 6), 64–72 (2013). https://doi.org/10.1093/annonc/mdt354CrossRef

Kannarkatt, J., Joseph, J., Kurniali, P.C., Al-Janadi, A., Hrinczenko, B.: Adjuvant chemotherapy for stage II colon cancer: a clinical dilemma. J. Oncol. Pract. 13(4), 233–241 (2017)PubMedCrossRef

Sloothaak, D.A.M., van der Linden, R.L.A., van de Velde, C.J.H., Bemelman, W.A., Lips, D.J., van der Linden, J.C., Doornewaard, H., Tanis, P.J., Bosscha, K., van der Zaag, E.S., Buskens, C.J.: Prognostic implications of occult nodal tumour cells in stage I and II colon cancer: the correlation between micrometastasis and disease recurrence. Eur. J. Surg. Oncol. (EJSO) 43(8), 1456–1462 (2017). https://doi.org/10.1016/j.ejso.2017.04.012CrossRef

Hutchins, G., Southward, K., Handley, K., Magill, L., Beaumont, C., Stahlschmidt, J., Richman, S., Chambers, P., Seymour, M., Kerr, D., Gray, R., Quirke, P.: Value of mismatch repair, KRAS, and BRAF mutations in predicting recurrence and benefits from chemotherapy in colorectal cancer. J. Clin. Oncol. 29(10), 1261–1270 (2011). https://doi.org/10.1200/jco.2010.30.1366PubMedCrossRef

Klingbiel, D., Saridaki, Z., Roth, A.D., Bosman, F.T., Delorenzi, M., Tejpar, S.: Prognosis of stage II and III colon cancer treated with adjuvant 5-fluorouracil or FOLFIRI in relation to microsatellite status: results of the PETACC-3 trial. Ann. Oncol. 26(1), 126–132 (2015). https://doi.org/10.1093/annonc/mdu499PubMedCrossRef

10.

Sinicrope, F.A., Foster, N.R., Thibodeau, S.N., Marsoni, S., Monges, G., Labianca, R., Kim, G.P., Yothers, G., Allegra, C., Moore, M.J., Gallinger, S., Sargent, D.J.: DNA mismatch repair status and colon cancer recurrence and survival in clinical trials of 5-fluorouracil-based adjuvant therapy. J. Natl. Cancer Inst. 103(11), 863–875 (2011). https://doi.org/10.1093/jnci/djr153PubMedPubMedCentralCrossRef

11.

Keikes, L., van Oijen, M.G.H., Lemmens, V., Koopman, M., Punt, C.J.A.: Evaluation of guideline adherence in colorectal cancer treatment in The Netherlands: a survey among Medical Oncologists by the Dutch Colorectal Cancer Group. Clin. Colorectal Cancer 17(1), 58–64 (2018). https://doi.org/10.1016/j.clcc.2017.10.007PubMedCrossRef

12.

Dienstmann, R., Salazar, R., Tabernero, J.: Personalizing colon cancer adjuvant therapy: selecting optimal treatments for individual patients. J. Clin. Oncol. 33(16), 1787–1796 (2015). https://doi.org/10.1200/JCO.2014.60.0213PubMedCrossRef

13.

Kawakami, H., Zaanan, A., Sinicrope, F.A.: Microsatellite instability testing and its role in the management of colorectal cancer. Curr. Treat. Options Oncol. 16(7), 30 (2015)PubMedPubMedCentralCrossRef

14.

André, T., De Gramont, A., Vernerey, D., Chibaudel, B., Bonnetain, F., Tijeras-Raballand, A., Scriva, A., Hickish, T., Tabernero, J., Van Laethem, J.L.: Adjuvant fluorouracil, leucovorin, and oxaliplatin in stage II to III colon cancer: updated 10-year survival and outcomes according to BRAF mutation and mismatch repair status of the MOSAIC study. J. Clin. Oncol. 33(35), 4176–4187 (2015)PubMedCrossRef

15.

De Cuba, E., Snaebjornsson, P., Heideman, D., van Grieken, N., Bosch, L., Fijneman, R.J., Belt, E., Bril, H., Stockmann, H., Hooijberg, E.: Prognostic value of BRAF and KRAS mutation status in stage II and III microsatellite instable colon cancers. Int. J. Cancer 138(5), 1139–1145 (2016)PubMedCrossRef

16.

Vilar, E., Gruber, S.B.: Microsatellite instability in colorectal cancer-the stable evidence. Nat. Rev. Clin. Oncol. 7(3), 153–162 (2010). https://doi.org/10.1038/nrclinonc.2009.237PubMedPubMedCentralCrossRef

17.

Sargent, D.J., Marsoni, S., Monges, G., Thibodeau, S.N., Labianca, R., Hamilton, S.R., French, A.J., Kabat, B., Foster, N.R., Torri, V., Ribic, C., Grothey, A., Moore, M., Zaniboni, A., Seitz, J.F., Sinicrope, F., Gallinger, S.: Defective mismatch repair as a predictive marker for lack of efficacy of fluorouracil-based adjuvant therapy in colon cancer. J. Clin. Oncol. 28(20), 3219–3226 (2010). https://doi.org/10.1200/jco.2009.27.1825PubMedPubMedCentralCrossRef

18.

Roth, A.D., Tejpar, S., Delorenzi, M., Yan, P., Fiocca, R., Klingbiel, D., Dietrich, D., Biesmans, B., Bodoky, G., Barone, C., Aranda, E., Nordlinger, B., Cisar, L., Labianca, R., Cunningham, D., Van Cutsem, E., Bosman, F.: Prognostic role of KRAS and BRAF in stage II and III resected colon cancer: results of the translational study on the PETACC-3, EORTC 40993, SAKK 60–00 trial. J. Clin. Oncol. 28(3), 466–474 (2010). https://doi.org/10.1200/jco.2009.23.3452PubMedCrossRef

19.

Gagniuc, P.A.: Markov chains: from theory to implementation and experimentation. Wiley, New York (2017)CrossRef

20.

van den Braak, R.R.C., Sieuwerts, A.M., Kandimalla, R., Lalmahomed, Z.S., Bril, S.I., van Galen, A., Smid, M., Biermann, K., van Krieken, J.H.J., Kloosterman, W.P.: High mRNA expression of splice variant SYK short correlates with hepatic disease progression in chemonaive lymph node negative colon cancer patients. PLoS One 12(9), e0185607 (2017)CrossRef

21.

Ozawa, T., Matsuyama, T., Toiyama, Y., Takahashi, N., Ishikawa, T., Uetake, H., Yamada, Y., Kusunoki, M., Calin, G., Goel, A.: CCAT1 and CCAT2 long noncoding RNAs, located within the 8q. 24.21 ‘gene desert’, serve as important prognostic biomarkers in colorectal cancer. Ann. Oncol. 28(8), 1882–1888 (2017)PubMedPubMedCentralCrossRef

22.

Gooiker, G.A., Dekker, J.W.T., Bastiaannet, E., van der Geest, L.G., Merkus, J.W., van de Velde, C.J., Tollenaar, R.A., Liefers, G.-J.: Risk factors for excess mortality in the first year after curative surgery for colorectal cancer. Ann. Surg. Oncol. 19(8), 2428–2434 (2012)PubMedPubMedCentralCrossRef

23.

van Gestel, Y.R., Lemmens, V.E., de Hingh, I.H., Steevens, J., Rutten, H.J., Nieuwenhuijzen, G.A., van Dam, R.M., Siersema, P.D.: Influence of comorbidity and age on 1-, 2-, and 3-month postoperative mortality rates in gastrointestinal cancer patients. Ann. Surg. Oncol. 20(2), 371–380 (2013)PubMedCrossRef

24.

Jongeneel, G., Klausch, T., van Erning, F.N., Vink, G.R., Koopman, M., Punt, C., Greuter, M., Coupe, V.: Estimating adjuvant treatment effects in stage II colon cancer: comparing the synthesis of randomized clinical trial data to real world data. Int. J. Cancer (2019). https://doi.org/10.1002/ijc.32629PubMedPubMedCentralCrossRef

25.

Ishak, K.J., Kreif, N., Benedict, A., Muszbek, N.: Overview of parametric survival analysis for health-economic applications. Pharmacoeconomics 31(8), 663–675 (2013)PubMedCrossRef

26.

Latimer, N.R.: Survival analysis for economic evaluations alongside clinical trials—extrapolation with patient-level data: inconsistencies, limitations, and a practical guide. Med. Decis. Mak. 33(6), 743–754 (2013)CrossRef

27.

Jackson, C.H.: flexsurv: a platform for parametric survival modeling in R. J. Stat. Softw. 70(8), 1–33 (2016)CrossRef

28.

Hoyle, M.W., Henley, W.: Improved curve fits to summary survival data: application to economic evaluation of health technologies. BMC Med. Res. Methodol. 11, 139 (2011). https://doi.org/10.1186/1471-2288-11-139PubMedPubMedCentralCrossRef

29.

Putter, H., Fiocco, M., Geskus, R.B.: Tutorial in biostatistics: competing risks and multi-state models. Stat. Med. 26(11), 2389–2430 (2007)PubMedCrossRef

30.

Verduijn, M., Grootendorst, D.C., Dekker, F.W., Jager, K.J., le Cessie, S.: The analysis of competing events like cause-specific mortality—beware of the Kaplan–Meier method. Nephrol. Dial. Transplant. 26(1), 56–61 (2011)PubMedCrossRef

31.

Bongers, M.L., De Ruysscher, D., Oberije, C., Lambin, P., Uyl-de Groot, C.A., Coupe, V.: Multistate statistical modeling: a tool to build a lung cancer microsimulation model that includes parameter uncertainty and patient heterogeneity. Med. Decis. Mak. 36(1), 86–100 (2016)CrossRef

32.

Demler, O.V., Paynter, N.P., Cook, N.R.: Tests of calibration and goodness-of-fit in the survival setting. Stat. Med. 34(10), 1659–1680 (2015)PubMedPubMedCentralCrossRef

33.

Uno, H., Cai, T., Pencina, M.J., D'Agostino, R.B., Wei, L.: On the C-statistics for evaluating overall adequacy of risk prediction procedures with censored survival data. Stat. Med. 30(10), 1105–1117 (2011)PubMedPubMedCentral

34.

Harrell Jr., F.E., Lee, K.L., Califf, R.M., Pryor, D.B., Rosati, R.A.: Regression modelling strategies for improved prognostic prediction. Stat. Med. 3(2), 143–152 (1984)PubMedCrossRef

35.

Hosmer, D.W., Lemeshow, S.: Applied logistic regression. Wiley, New York (2000)CrossRef

36.

Ayvaci, M.U., Shi, J., Alagoz, O., Lubner, S.J.: Cost-effectiveness of adjuvant FOLFOX and 5FU/LV chemotherapy for patients with stage II colon cancer. Med. Decis. Mak. 33(4), 521–532 (2013)CrossRef

37.

Koene, R.J., Prizment, A.E., Blaes, A., Konety, S.H.: Shared risk factors in cardiovascular disease and cancer. Circulation 133(11), 1104–1114 (2016)PubMedPubMedCentralCrossRef

38.

Group, Q.C.: Adjuvant chemotherapy versus observation in patients with colorectal cancer: a randomised study. Lancet 370(9604), 2020–2029 (2007)CrossRef

39.

Shi, Q., Andre, T., Grothey, A., Yothers, G., Hamilton, S.R., Bot, B.M., Haller, D.G., Van Cutsem, E., Twelves, C., Benedetti, J.K., O'Connell, M.J., Sargent, D.J.: Comparison of outcomes after fluorouracil-based adjuvant therapy for stages II and III colon cancer between 1978 to 1995 and 1996 to 2007: evidence of stage migration from the ACCENT database. J. Clin. Oncol. 31(29), 3656–3663 (2013). https://doi.org/10.1200/jco.2013.49.4344PubMedPubMedCentralCrossRef

40.

Snaebjornsson, P., Coupe, V., Jonasson, L., Meijer, G., van Grieken, N., Jonasson, J.: pT4 stage II and III colon cancers carry the worst prognosis in a nationwide survival analysis. Shepherd's local peritoneal involvement revisited. Int. J. Cancer 135(2), 467–478 (2014)PubMedCrossRef

41.

Warschkow, R., Sulz, M.C., Marti, L., Tarantino, I., Schmied, B.M., Cerny, T., Guller, U.: Better survival in right-sided versus left-sided stage I–III colon cancer patients. BMC Cancer 16, 554 (2016). https://doi.org/10.1186/s12885-016-2412-0PubMedPubMedCentralCrossRef

42.

Nawa, T., Kato, J., Kawamoto, H., Okada, H., Yamamoto, H., Kohno, H., Endo, H., Shiratori, Y.: Differences between right- and left-sided colon cancer in patient characteristics, cancer morphology and histology. J. Gastroenterol. Hepatol. 23(3), 418–423 (2008). https://doi.org/10.1111/j.1440-1746.2007.04923.xPubMedCrossRef

43.

Sinicrope, F.A., Shi, Q., Smyrk, T.C., Thibodeau, S.N., Dienstmann, R., Guinney, J., Bot, B.M., Tejpar, S., Delorenzi, M., Goldberg, R.M., Mahoney, M., Sargent, D.J., Alberts, S.R.: Molecular markers identify subtypes of stage III colon cancer associated with patient outcomes. Gastroenterology 148(1), 88–99 (2015). https://doi.org/10.1053/j.gastro.2014.09.041PubMedCrossRef

44.

O'Connor, E.S., Greenblatt, D.Y., LoConte, N.K., Gangnon, R.E., Liou, J.-I., Heise, C.P., Smith, M.A.: Adjuvant chemotherapy for stage II colon cancer with poor prognostic features. J. Clin. Oncol. 29(25), 3381 (2011)PubMedPubMedCentralCrossRef

Title: Modeling Personalized Adjuvant TreaTment in EaRly stage coloN cancer (PATTERN)
Authors: Gabrielle Jongeneel
Marjolein J. E. Greuter
Felice N. van Erning
Miriam Koopman
Jan P. Medema
Raju Kandimalla
Ajay Goel
Luis Bujanda
Gerrit A. Meijer
Remond J. A. Fijneman
Martijn G. H. van Oijen
Jan Ijzermans
Cornelis J. A. Punt
Geraldine R. Vink
Veerle M. H. Coupé
Publication date: 01-09-2020
Publisher: Springer Berlin Heidelberg
Keywords: Colon Cancer
Colon Cancer
Cytostatic Therapy
Biomarkers
Published in: The European Journal of Health Economics / Issue 7/2020
Print ISSN: 1618-7598
Electronic ISSN: 1618-7601
DOI: https://doi.org/10.1007/s10198-020-01199-4

At a glance: The STEP trials

Springer Medicine

Modeling Personalized Adjuvant TreaTment in EaRly stage coloN cancer (PATTERN)

Abstract

Aim

Methods

Results

Conclusion

At a glance: The STEP trials

Springer Medicine

Abstract

Aim

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 7/2020

Quantifying the economic impact of caregiving for Duchenne muscular dystrophy (DMD) in Spain

Discrete choice experiments to generate utility values for multi-attribute utility instruments: a systematic review of methods

Patterns of care and cost profiles of women with breast cancer in Italy: EPICOST study based on real world data

The excess economic burden of mental disorders: findings from a cross-sectional prevalence survey in Austria

Cost-utility analysis of inotuzumab ozogamicin for relapsed or refractory B cell acute lymphoblastic leukemia from the perspective of Taiwan’s health care system

Cost-effectiveness of biennial screening for diabetes related retinopathy in people with type 1 and type 2 diabetes compared to annual screening