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Preoperative Chemoradiotherapy With CApecitabine and Temozolomide in MGMT Silenced, MSS, Locally Advanced RecTal Cancer

Phase 2
Recruiting
Conditions
Rectal Cancer
Interventions
Radiation: External-beam radiation
Registration Number
NCT05136326
Lead Sponsor
Fondazione IRCCS Istituto Nazionale dei Tumori, Milano
Brief Summary

In patients with locally advanced rectal cancer (LARC), preoperative chemo-radiotherapy (CTRT) is considered the standard of care. Preoperative CTRT approach often results in a significant tumor downstaging and local control, with evidence of complete pathological response (pCR) rate of about 15% in high volume institutions. In high-risk LARC a new strategy called total neoadjuvant therapy (TNT) has emerged, in which systemic chemotherapy with fluorouracil and oxaliplatin (RAPIDO trial) or with the triplet FOLFIRINOX (as was used in the PRODIGE 23 study) is incorporated before or after the administration of short-course RT or neoadjuvant CTRT and prior to surgery. However, given the fact that TNT may represent an overtreatment for a subset of patients, additional therapeutic strategies are warranted to improve the outcomes also in patients with lower risk that are not good candidate for a TNT.

In the era of personalized medicine, tumor molecular profiling may lead to the identification of therapeutic targets for pharmacological intervention potentially useful to enhance treatment outcomes.

O(6)-methylguanine-DNA-methyltransferase (MGMT) repairs DNA damage induced by alkylating agents and MGMT inactivation due to promoter methylation confers enhanced sensitivity to alkylating agents such as temozolomide (TMZ).

TMZ has modest activity in patients with MGMT-methylated pretreated metastatic colorectal cancer and responses are restricted to tumors with complete MGMT loss by immunohistochemistry (IHC) and microsatellite stable (MSS) status.

Both capecitabine and temozolomide induces deoxythymidine triphosphate thymidine pool depletion might induce deoxyribonucleic acid (DNA)-double strand breaks and eventually apoptosis in rapidly dividing cells. On the basis of such evidences, there is a strong biological and clinical rationale for testing the addition of TMZ to capecitabine-based CTRT in patients with MGMT silenced and MSS technically resectable LARC.

The aim of this trial is investigating whether the addition of TMZ to standard concurrent capecitabine-based long-course chemoradiation may increase pCR rate as compared to historical control in patients with locally advanced rectal cancer not candidate to TNT and molecularly selected for the presence of MGMT silencing and microsatellite stable status.

Detailed Description

Preoperative CTRT (long-course radiotherapy with a recommended dose of 45-50 Gy in 25-28 fractions plus a boost with a further 5.4 Gy in 3 fractions, and concomitant administration of oral capecitabine or continuous intravenous infusions of 5-fluorouracil) is considered the standard of care in the management of LARC, based on the significantly better down-staging and local control obtained by preoperative CTRT compared with radiotherapy (RT) alone, with a consequent reduction of local recurrence rate, and given its superior tolerability profile compared with postoperative treatment. Preoperative CTRT approach often results in a significant tumor downstaging and local control, with evidence of complete pathological response (pCR) rate of about 15% in high volume institutions. In high-risk LARC a new strategy called total neoadjuvant therapy (TNT) has emerged, in which systemic chemotherapy with fluorouracil and oxaliplatin (RAPIDO trial) or with the triplet FOLFIRINOX (as was used in the PRODIGE 23 study) is incorporated before or after the administration of short-course RT or neoadjuvant CTRT and prior to surgery. However, given the fact that TNT may represent an overtreatment for a subset of patients, additional therapeutic strategies are warranted to improve the outcomes also in patients with lower risk that are not good candidate for a TNT.

In the era of personalized medicine, tumor molecular profiling may lead to the identification of therapeutic targets for pharmacological intervention potentially useful to enhance treatment outcomes. About 30-40% of colorectal carcinomas (CRCs) are characterized by the promoter methylation of the O(6)-methylguanine-DNA-methyltransferase (MGMT) gene, encoding a repair enzyme involved in the elimination of alkyl groups from the O6-position of guanine, usually caused by alkylating agents. MGMT defect, due to epigenetic silencing of the MGMT gene, may be involved in early steps of colorectal tumor genesis leading to an increase of G-to-A transitions and may be associated with enhanced chemosensitivity to alkylating agents including dacarbazine and its oral analogue temozolomide (TMZ) - as shown for melanoma and glioblastoma. Previous phase II studies showed that TMZ can induce an objective response by RECIST criteria in about 10% of heavily pre-treated patients with advanced CRC carrying MGMT promoter methylated, as determined by the qualitative assay methylation-specific polymerase chain reaction (MSP). To refine patient selection for TMZ therapy, we recently showed how digital PCR quantification of MGMT methylation may further refine patient selection, with benefit restricted to those with highly hyper-methylated tumors. Moreover, we showed that MGMT negative/low expression by immunohistochemistry (IHC) is found in about one third of MSP-methylated samples and is associated with increased response rate, since patients with retained MGMT expression in their tumors do not benefit from TMZ therapy. Therefore, ongoing trials (MAYA \[NCT03832621\], ARETHUSA \[NCT03519412\], FLIRT-bev \[NCT04689347\], ERASE-TMZ \[EUDRACT:2020-005437-32\]) select patients based on lack of MGMT expression assessed by means of IHC and presence of MGMT methylation by pyrosequencing or methylBEAMing. Finally, patients with microsatellite instability-high (MSI-high) metastatic colorectal cancer (mCRC) are intrinsically resistant to TMZ and therefore should be excluded by clinical trials on TMZ-based therapies. Based on these data, an assessment of MGMT promoter methylation coupled with absent protein expression and of the microsatellite instability status could optimize the prediction of response.

Finally, previous reports indicate that acquired resistance to TMZ may emerge through the induction of a MSI-like phenotype with emergence of MMR gene mutations and elevated tumor mutational burden characterized by G\>A transitions (signature 8 according to Alexandrov et al, Nature 2013). The recently completed MAYA trial (NCT03832621) investigated the combination of TMZ with nivolumab and ipilimumab in patients with metastatic and chemorefractory disease; however, no data are available on potential synergy between RT and TMZ in inducing potential sensitization to immunotherapy of "cold" tumors and translational data are required.

Both capecitabine and temozolomide induces deoxythymidine triphosphate. Thymidine pool depletion might induce deoxyribonucleic acid (DNA)-double strand breaks and eventually apoptosis in rapidly dividing cells. On the basis of such evidences, there is a strong biological and clinical rationale for testing the addition of TMZ to capecitabine-based CTRT in patients with MGMT silenced and MSS technically resectable LARC. Concurrent treatment with TMZ during RT followed by adjuvant TMZ is the standard of care for the treatment of malignant glioblastomas, showing a survival benefit compared to radiation alone, at the cost of a limited additional toxicity. When used together to radiotherapy, TMZ stabilize RT-induced double-strand breaks by producing 12-base adducts in DNA, including the cytotoxic lesions O6-methylguanine and 3-methyladenine. Therefore, the synergy between RT and TMZ could be of particular value in patients with MGMT silenced, MSS rectal cancers candidates for preoperative CTRT. Therefore, there is a strong rationale to investigate capecitabine plus temozolomide (CAPTEM)-based CTRT in this molecular subgroup.

In a phase 1 study, Jeong and colleagues evaluated the dose limiting toxicity (DLT) and the recommended dose (RD) of temozolomide when combined with capecitabine as preoperative CTRT in patients with molecularly unselected LARC, showing that this treatment strategy is feasible and safe. No dose limiting toxicities were observed in patients treated with the highest temozolomide dose level tested in the study of 75 mg/m2/day, nor National Cancer Institute Common Terminology Criteria for Adverse Event (NCI-CTCAE) grade IV adverse events (AEs) were observed. Overall, the most frequent AE reported was nausea, occurring in 77.2% of the 22 patients treated. The MGMT promoter hypermethylation was detected in the 72.7% of patient enrolled. Tumor downstaging of the primary tumor and lymph nodes was observed in 81.8% and 72.7% of patients, respectively, the R0 resection rate was 90.9% and a pCR of the primary tumor (ypT0) was achieved in 31.8% of patients. As expected, the pCR rates were higher in the hypermethylated than in the unmethylated MGMT group (37.5% vs 16.7%), although this difference did not reach the statistical significance (odds ratio= 0.33; 95% Confidence Interval \[CI\], 0.03-3.58; p=0.616).

The aim of this trial is investigating whether the addition of TMZ to standard concurrent capecitabine-based long-course chemoradiation may increase pCR rate as compared to historical control in patients with locally advanced rectal cancer not candidate to TNT and molecularly selected for the presence of MGMT silencing and microsatellite stable status.

Recruitment & Eligibility

Status
RECRUITING
Sex
All
Target Recruitment
21
Inclusion Criteria
  • Written informed consent to study procedures;

  • Willing and able to comply with the protocol;

  • Age ≥ 18 years;

  • Eastern Cooperative Oncology Group (ECOG) Performance Status (PS) 0-1;

  • Life expectancy of at least 5 years (excluding diagnosis of cancer);

  • Histologically confirmed diagnosis of rectal adenocarcinoma, with centrally confirmed mismatch repair proficiency (MSS) by PCR, lack of MGMT expression by IHC and MGMT promoter methylation by pyrosequencing;

  • Locally advanced, resectable disease defined by the presence of at least one of the following features:

    1. Distal tumor margin at <15 cm from the anal verge;
    2. cT3N0 or cT1-3N1 (with the definition of a clinically positive lymph node being any node ≥ 1 cm);
    3. Less than four lymph nodes in the mesorectum showing morphological signs on MRI indicating metastatic disease;
    4. No evidence of enlarged lateral pelvic clinically positive lymph node (> 1 cm);
    5. No evidence of extramural vascular invasion (EMVI);
    6. No evidence of metastatic disease by CT scan of the chest and abdomen and total body fluorodeoxyglucose positron emission tomography (FDG-PET)/CT scan;
    7. No clear indication of involvement of the pelvic side walls by imaging;
  • Tumor must be amenable to curative resection (curative resection can include pelvic exenteration);

  • Hematopoietic: absolute neutrophil count ≥1500/mm3; platelet count ≥ 100,000/mm3; haemoglobin level ≥ 10 g/dL;

  • Hepatic total bilirubin ≤1.5 time upper limit of normal (ULN); alkaline phosphatase ≤ 2 times ULN; AST and ALT ≤ 2.5 times ULN Serum creatinine ≤ 1.5 × ULN or renal creatinine clearance ≥ 50 mL/min according to the Cockcroft-Gault formula (or local institutional standard methods);

  • Availability of an adequate archival tumor sample (Formalin Fixed Paraffin-embedded [FFPE]) for central tissue screening. If the tumor block is not available, a minimum of twenty-five (25) 3-micron unstained sections of tumor will be required (5 of those on standard non charged slides for immunochemistry, the others on charged slides);

  • Male subjects with female partners of childbearing potential must be willing to use adequate contraception as approved by the investigator (barrier contraceptive measure or oral contraception) contraception starting with the first dose of study therapy, through 180 days after the last dose of treatment; Note: Abstinence is acceptable if this is the usual lifestyle and preferred contraception for these subject.

  • Women of childbearing potential must have a negative blood pregnancy test at the baseline visit and must be willing to use an effective means of contraception and to continue its use for the duration of the study and for 180 days after the last infusion of study treatment. For this trial, women of childbearing potential are defined as all women after puberty, unless they are postmenopausal for at least 12 months, are surgically sterile, or are sexually inactive. Note: Abstinence is acceptable if this is the usual lifestyle and preferred contraception for the subject.

Exclusion Criteria
  • Dihydropyrimidine dehydrogenase (DPD) deficiency;
  • Previous pelvic RT;
  • Any of the following in the 6 months prior to treatment start: myocardial infarction, severe/unstable angina, coronary/peripheral artery bypass graft, congestive heart failure (≥ New York Heart Association Classification Class II), cerebrovascular accident/stroke, transient ischemic attack, serious cardiac arrhythmia requiring medication or symptomatic pulmonary embolism;
  • Uncontrolled coagulopathy;
  • Active infection requiring systemic therapy;
  • Infection with human immunodeficiency virus (HIV) plus CD4 cells <200/mm3 or AIDS-defining conditions despite HAART;
  • Known prior severe hypersensitivity to investigational product or any component in its. formulations;
  • Lack of upper gastrointestinal tract integrity or malabsorption syndrome; immune colitis; active inflammatory bowel disease (i.e., patients requiring current medical interventions or who are symptomatic);
  • Presence of metastatic disease, recurrent rectal cancer or history of invasive rectal malignancy, regardless of disease-free interval;
  • Other rectal cancers (i.e., sarcoma, lymphoma, carcinoid, squamous cell or cloacogenic carcinoma) or synchronous colon cancer;
  • Patients with prior malignancies, including invasive colon cancer, are eligible provided they have been disease-free for ≥ 3 years and are deemed by their physician to be at low risk for recurrence (patients with effectively treated squamous cell or basal cell skin cancer, melanoma in situ, carcinoma in situ of the cervix, or carcinoma in situ of the colon or rectum are eligible even if diagnosed less than 3 years before study enrollment);
  • Other severe acute or chronic medical conditions including immune pneumonitis, pulmonary fibrosis or psychiatric conditions including recent (within the past year) or active suicidal ideation or behavior; or laboratory abnormalities that may increase the risk associated with study participation or study treatment administration or may interfere with the interpretation of study results and, in the judgment of the investigator, would make the patient inappropriate for entry into this study;
  • Any concomitant drugs contraindicated for use with the trial drugs according to the product information of the pharmaceutical companies;
  • Pregnant or lactating women.

Study & Design

Study Type
INTERVENTIONAL
Study Design
SINGLE_GROUP
Arm && Interventions
GroupInterventionDescription
Catartic: chemoradiotherapy plus temozolomideExternal-beam radiationExternal-beam radiation: 50.4 GY (45 Gy in 25 fractions + Boost 5.4 Gy in 3 fractions over 5 weeks) in association with: Capecitabine 825 mg/sqm/bid per os (p.o.) 5 days/week for 5 weeks plus Temozolomide 75 mg/sqm p.o. 5 days/week for 5 weeks.
Catartic: chemoradiotherapy plus temozolomideTemozolomideExternal-beam radiation: 50.4 GY (45 Gy in 25 fractions + Boost 5.4 Gy in 3 fractions over 5 weeks) in association with: Capecitabine 825 mg/sqm/bid per os (p.o.) 5 days/week for 5 weeks plus Temozolomide 75 mg/sqm p.o. 5 days/week for 5 weeks.
Catartic: chemoradiotherapy plus temozolomideCapecitabineExternal-beam radiation: 50.4 GY (45 Gy in 25 fractions + Boost 5.4 Gy in 3 fractions over 5 weeks) in association with: Capecitabine 825 mg/sqm/bid per os (p.o.) 5 days/week for 5 weeks plus Temozolomide 75 mg/sqm p.o. 5 days/week for 5 weeks.
Primary Outcome Measures
NameTimeMethod
To evaluate the rate of complete pathologic response (pCR)24 months

pCR, defined as complete histological regression with no available tumor cells yT0N0

Secondary Outcome Measures
NameTimeMethod
To assess the R0 resection rate24 months

R0 defined as the rate of microscopically margin-negative resections

To assess the tumor downstaging rate24 months

Tumor downstaging rate defined as the rate of reduction in the stage of the tumor as a result of pre-operative therapy, from a more to a less threatening stage at the radiologic assessment after the the end of CTRT

To assess the disease-free survivalThe disease-free survival will be evaluated during a follow up of 5 years

Disease-free survival defined as the time from the enrollment in the study to the occurrence of disease relapse (local and/or distant) or death from any cause

To assess the rate of sphincter preservation24 months

Sphincter preservation rate defined as the percentage of patients with preserved ano-rectal sphincter after surgery

To assess the overall survivalThe overall survival will be evaluated during a follow up of 5 years

Overall survival defined as the time from the enrollment in the study to the occurrence of death.

To assess the incidence, nature, and severity of adverse events24 months

Adverse events defined and graded according to the NCI CTCAE v5.0

To assess the rate of local recurrence rate24 months

Local recurrence rate defined as the rate of detectable local disease at follow-up after study treatment completion

Trial Locations

Locations (1)

Fondazione IRCCS Istituto Nazionale dei Tumori

🇮🇹

Milan, Italy

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