Temozolomide Followed by Combination With Low-Dose Ipilimumab and Nivolumab in Patients With Microsatellite-Stable, O6-Methylguanine–DNA Methyltransferase–Silenced Metastatic Colorectal Cancer: The MAYA Trial
Open accessAbstract
PURPOSE: This is a multicenter, single-arm phase II trial evaluating the efficacy and safety of an immune-sensitizing strategy with temozolomide priming followed by a combination of low-dose ipilimumab and nivolumab in patients with microsatellite-stable (MSS) and O 6-methylguanine–DNA methyltransferase (MGMT)–silenced metastatic colorectal cancer (mCRC). PATIENTS AND METHODS: Patients with pretreated mCRC were centrally prescreened for MSS status and MGMT silencing (ie, lack of MGMT expression by immunohistochemistry plus MGMT methylation by pyrosequencing). Eligible patients received two priming cycles of oral temozolomide 150 mg/sqm once daily, days 1-5, once every 4 weeks (first treatment part) followed, in absence of progression, by its combination with ipilimumab 1 mg/kg once every 8 weeks and nivolumab 480 mg once every 4 weeks (second treatment part). The primary end point was the 8-month progression-free survival (PFS) rate calculated from enrollment in patients who started the second treatment part, with ≥ 4 out of 27 subjects progression-free by the 8-month time point as decision rule. RESULTS: Among 716 prescreened patients, 204 (29%) were molecularly eligible and 135 started the first treatment part. Among these, 102 (76%) were discontinued because of death or disease progression on temozolomide priming, whereas 33 patients (24%) who achieved disease control started the second treatment part and represented the final study population. After a median follow-up of 23.1 months (interquartile range, 14.9-24.6 months), 8-month PFS rate was 36%. Median PFS and overall survival were 7.0 and 18.4 months, respectively, and overall response rate was 45%. Grade 3-4 immune-related adverse events were skin rash (6%), colitis (3%), and hypophysitis (3%). No unexpected adverse events or treatment-related deaths were reported. CONCLUSION: The MAYA study provided proof-of-concept that a sequence of temozolomide priming followed by a combination of low-dose ipilimumab and nivolumab may induce durable clinical benefit in MSS and MGMT-silenced mCRC.
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All patients in the ARETHUSA study were RAS mutant, and the majority (72%) of patients in the MAYA study were RAS mutant.
“All patients in the ARETHUSA study were RAS mutant patients, and the majority (72%) of the patients in the MAYA study were RAS mutant patients.”
From RAS Mutations in Advanced Colorectal Cancer: Mechanisms, Clinical Implications, and Novel Therapeutic Approaches (2025) · cites this paper as [90]
In the MAYA study, with temozolomide-nivolumab-ipilimumab combination treatment, an mPFS of 7.1 months (95% CI, 5.6-8.4) was observed.
“With this combination treatment, an mPFS of 7.1 months (95% CI, 5.6–8.4) was observed.”
From RAS Mutations in Advanced Colorectal Cancer: Mechanisms, Clinical Implications, and Novel Therapeutic Approaches (2025) · cites this paper as [90]
In the MAYA study, there was no significant difference in the objective response rates of TMZ and IO between RAS mutant and wild patients (p = 0.660).
“In the MAYA study, there was no significant difference in the objective response rates of TMZ and IO between RAS mutant and wild patients (p = 0.660).”
From RAS Mutations in Advanced Colorectal Cancer: Mechanisms, Clinical Implications, and Novel Therapeutic Approaches (2025) · cites this paper as [90]
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- Authors
- Morano, F., Raimondi, A., Pagani, F., Lonardi, S., Salvatore, L., Cremolini, C., Murgioni, S., Randon, G., Palermo, F., Antonuzzo, L., Pella, N., Racca, P., Prisciandaro, M., Niger, M., Corti, F., Bergamo, F., Zaniboni, A., Ratti, M., Palazzo, M., Cagnazzo, C., Calegari, M. A., Marmorino, F., Capone, I., Conca, E., Busico, A., Brich, S., Tamborini, E., Perrone, F., Di Maio, M., Milione, M., Di Bartolomeo, M., de Braud, F., & Pietrantonio, F.
- Affiliations
- Fondazione IRCCS Istituto Nazionale dei Tumori (IT)
- Istituto Oncologico Veneto (IT)
- Università Cattolica del Sacro Cuore (IT)
- University of Pisa (IT)
- Azienda Ospedaliero-Universitaria Careggi (IT)
- University of Udine (IT)
- Azienda Ospedaliera Citta' della Salute e della Scienza di Torino (IT)
- Fondazione Poliambulanza Istituto Ospedaliero (IT)
- Azienda Socio Sanitaria Territoriale di Cremona (IT)
- University of Turin (IT)
- Agostino Gemelli University Polyclinic (IT)
- Department of Oncology, University of Turin, Division of Medical Oncology, Ordine Mauriziano Hospital, Turin, Italy
- Department of Medical Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
- Corresponding author
- Pietrantonio, Filippo
- ORCID
- Morano, Federica
- Raimondi, Alessandra
- Lonardi, Sara
- Salvatore, Lisa
- Cremolini, Chiara
- Murgioni, Sabina
- Randon, Giovanni
- Palermo, Federica
- Antonuzzo, Lorenzo
- Prisciandaro, Michele
- Niger, Monica
- Corti, Francesca
- Bergamo, Francesca
- Zaniboni, Alberto
- Ratti, Margherita
- Palazzo, Michele
- Cagnazzo, Celeste
- Calegari, Maria Alessandra
- Marmorino, Federica
- Capone, Iolanda
- Conca, Elena
- Busico, Adele
- Brich, Silvia
- Tamborini, Elena
- Perrone, Federica
- Di Maio, Massimo
- Milione, Massimo
- Pietrantonio, Filippo
- Venue
- Journal of Clinical Oncology
- Published
- 2022-05-10
- Volume
- 40
- Issue
- 14
- Pages
- 1562-1573
- ISSN
- 0732-183X (ISSN-L)
- 1527-7755
- PMC
- PMC9084437
- OpenAlex
- W4220750583
- Cited by
- 134
- References
- 37
- Citations by year
- 2026: 18 · 2025: 33 · 2024: 32 · 2023: 36 · 2022: 15
- FWCI
- 12.14
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- Locations
- Journal of Clinical Oncology (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Florence Research (University of Florence) (submittedVersion, cc-by-nc-nd)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion, cc-by-nc-nd)
- ArTS Archivio della ricerca di Trieste (University of Trieste https://www.units.it/) (submittedVersion)
- PubliCatt (Università Cattolica del Sacro Cuore) (submittedVersion, other-oa)
- Topics
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Keywords
- temozolomide, ipilimumab, nivolumab, metastatic colorectal cancer, microsatellite stable, immune checkpoint inhibitors, progression-free survival, immune-related adverse events, MGMT promoter methylation, combination immunotherapy
- MeSH terms
- Ipilimumab, Temozolomide, Nivolumab, Antineoplastic Combined Chemotherapy Protocols, Colonic Neoplasms, Humans, Rectal Neoplasms, Colorectal Neoplasms, Microsatellite Repeats, O(6)-Methylguanine-DNA Methyltransferase
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