University of Manchester



Carboplatin in combination with oral or intravenous etoposide for extra-pulmonary, poorly-differentiated neuroendocrine carcinomasMelissa Frizziero1, Francesca Spada2, Angela Lamarca1,?, Zoe Kordatou1, Jorge Barriuso1,3, Christina Nuttall1, Mairéad G McNamara1,3, Richard A Hubner1, Wasat Mansoor1, Prakash Manoharan4, Nicola Fazio2, Juan W Valle1,3.Affiliations:1Department of Medical Oncology, The Christie NHS Foundation Trust, Manchester, United Kingdom. 2Gastrointestinal Medical Oncology and Neuroendocrine Tumors Unit, European Institute of Oncology, Milan, Italy.3Division of Cancer Sciences, University of Manchester, United Kingdom. 4Department of Radiology and Nuclear Medicine, The Christie NHS Foundation Trust, Manchester, United Kingdom.?Part-funded by the ASCO (American Society of Clinical Oncology) Conquer Cancer Foundation Young Investigator Award.Short Title: Carboplatin-etoposide for extra-pulmonary neuroendocrine carcinomasCorresponding author:Prof Juan W. ValleProfessor and Honorary Consultant in Medical OncologyDepartment of Medical OncologyThe Christie NHS Foundation Trust550 Wilmslow Road, M20 4BXManchester, United KingdomJuan.Valle@christie.nhs.ukTel: +44 161 446 8106Fax: +44 446 3468Keywords; carboplatin-etoposide, extra-pulmonary neuroendocrine carcinoma, oral etoposide, intravenous etoposide.1. AbstractBackground:Carboplatin-Etoposide (CarboEtop) is a 1st-line option for patients with advanced extra-pulmonary (EP), poorly-differentiated (PD) neuroendocrine carcinoma (NEC). Different schedules are used in clinical practice and randomised evidence is lacking.Objectives: To provide real-life outcomes of carboplatin combined with oral or intravenous (IV) etoposide (Etop) in advanced EP-PD-NEC, from 2 specialist centres.Methods:Activity/efficacy/toxicity data of CarboEtop were retrospectively collected and analysed.Results:We identified 113 patients; median age: 65.8 years; male: 64%; gastro-entero-pancreatic origin: 54%; stage IV: 90%; median Ki-67: 70%; median follow-up: 11.5 months. A total of 123 courses of CarboEtop (oral: 45%; IV: 55%) were administered; 106 (86%) 1st-line, 16 (13%) 2nd-line and 1 (1%) 3rd-line. Disease-control-rate: 74.5% in 1st-line and 69.2% in 2nd/3rd-line, with no significant difference between oral- and IV-Etop in 1st-line (69.8% versus 80.8%, p=0.237). Median progression-free survival (PFS): 6.0 and 4.5 months in 1st-line and 2nd/3rd-line, respectively. Overall survival (OS): 11.5 and 12.5 months in 1st-line and 2nd/3rd-line, respectively. The schedule (oral- versus IV-Etop) did not impact on 1st-line PFS (5.6 versus 6.2 months, p=0.179), although there was a trend towards shorter OS (8.9 versus 12.1 months, p=0.069). Liver metastases correlated with worse 1st-line-PFS (p=0.015) and 1st-line-OS (p<0.001) on multivariable analysis. The commonest grade 3-4 adverse event was myelosuppression (49%), with comparable toxicity between oral- and IV-Etop, except for venous thromboembolism (12.5% versus 1.7%, p=0.04).Conclusions:CarboEtop for advanced EP-PD-NEC is active, effective and well-tolerated. Oral- and IV-Etop schedules are associated with comparable toxicity; activity should be compared in larger cohorts.2. IntroductionExtra-pulmonary (EP) neuroendocrine carcinoma (NEC) is a poorly-differentiated (PD) neuroendocrine neoplasm with a mitotic count >20/10 high power field (HPF) and/or a Ki-67 index >20%, as defined by the 2010 World Health Organisation (WHO) classification ADDIN EN.CITE <EndNote><Cite><Author>Bosman T</Author><Year>2010</Year><RecNum>1</RecNum><DisplayText>[1]</DisplayText><record><rec-number>1</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1526894485">1</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>Bosman T, Carneiro F, Hruban RH, Theise ND</author></authors></contributors><titles><title>WHO Classification of Tumours of the Digestive System. 4th ed.</title></titles><dates><year>2010</year></dates><pub-location>Lyon</pub-location><publisher>IARC press</publisher><urls></urls></record></Cite></EndNote>[1]. This diagnosis, although rare [incidence in Europe; 0.52/100,000 individuals/annum according to the Surveillance of Rare Cancers in Europe (RARECARE) Registry (, July 20th, 2018)], has been increasingly encountered in routine practice PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5EYXNhcmk8L0F1dGhvcj48WWVhcj4yMDE3PC9ZZWFyPjxS

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ADDIN EN.CITE.DATA [3-9].Extra-pulmonary PD-NEC is an aggressive entity with 57-73% of patients presenting with distant metastatic disease at diagnosis PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Tb3JieWU8L0F1dGhvcj48WWVhcj4yMDE0PC9ZZWFyPjxS

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ADDIN EN.CITE.DATA [4, 5, 10]; these patients have limited treatment options and an extremely poor prognosis, with a median overall-survival (OS) as short as 1 month for those who receive only best supportive care, and between 9.2 and 19 months for those who are treated with palliative chemotherapy PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5IZWV0ZmVsZDwvQXV0aG9yPjxZZWFyPjIwMTU8L1llYXI+

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ADDIN EN.CITE.DATA [14]. This score may be used to assess patient eligibility for active treatment and for patient stratification in clinical trials.Due to the rarity of this disease, data from large randomised trials are lacking. As a result, clinical practice guidelines are usually extrapolated from the more extensive literature on lung-NEC, based on the assumption of a biological similarity between these two entities. In keeping with the treatment paradigm for their pulmonary counterpart, platinum-based chemotherapy is advocated as ‘standard-of-care’ active treatment for advanced EP-PD-NEC ADDIN EN.CITE <EndNote><Cite><Author>Garcia-Carbonero</Author><Year>2016</Year><RecNum>4</RecNum><DisplayText>[15]</DisplayText><record><rec-number>4</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1526901968">4</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Garcia-Carbonero, R.</author><author>Sorbye, H.</author><author>Baudin, E.</author><author>Raymond, E.</author><author>Wiedenmann, B.</author><author>Niederle, B.</author><author>Sedlackova, E.</author><author>Toumpanakis, C.</author><author>Anlauf, M.</author><author>Cwikla, J. B.</author><author>Caplin, M.</author><author>O&apos;Toole, D.</author><author>Perren, A.</author><author>Vienna Consensus Conference, participants</author></authors></contributors><auth-address>Medical Oncology Department, Hospital Universitario Doce de Octubre, Madrid, Spain.</auth-address><titles><title>ENETS Consensus Guidelines for High-Grade Gastroenteropancreatic Neuroendocrine Tumors and Neuroendocrine Carcinomas</title><secondary-title>Neuroendocrinology</secondary-title></titles><periodical><full-title>Neuroendocrinology</full-title></periodical><pages>186-94</pages><volume>103</volume><number>2</number><keywords><keyword>Carcinoma, Neuroendocrine/diagnosis/epidemiology/genetics/*therapy</keyword><keyword>Humans</keyword><keyword>Intestinal Neoplasms/diagnosis/epidemiology/genetics/*therapy</keyword><keyword>Neuroendocrine Tumors/diagnosis/epidemiology/genetics/*therapy</keyword><keyword>Pancreatic Neoplasms/diagnosis/epidemiology/genetics/*therapy</keyword><keyword>Stomach Neoplasms/diagnosis/epidemiology/genetics/*therapy</keyword></keywords><dates><year>2016</year></dates><isbn>1423-0194 (Electronic)&#xD;0028-3835 (Linking)</isbn><accession-num>26731334</accession-num><urls><related-urls><url>;[15]. Although the use of cisplatin/etoposide combination is the most extensively documented in the literature of lung- and EP-PD-NEC, carboplatin-etoposide (CarboEtop) has emerged as a valid and equally-effective alternative ADDIN EN.CITE <EndNote><Cite><Author>Fazio</Author><Year>2013</Year><RecNum>13</RecNum><DisplayText>[16]</DisplayText><record><rec-number>13</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1526922387">13</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Fazio, N.</author><author>Spada, F.</author><author>Giovannini, M.</author></authors></contributors><auth-address>Unit of Upper Gastrointestinal and Neuroendocrine Tumors, Department of Medicine, European Institute of Oncology, Via Ripamonti 435, 20141 Milan, Italy. nicola.fazio@ieo.it</auth-address><titles><title>Chemotherapy in gastroenteropancreatic (GEP) neuroendocrine carcinomas (NEC): a critical view</title><secondary-title>Cancer Treat Rev</secondary-title></titles><periodical><full-title>Cancer Treat Rev</full-title></periodical><pages>270-4</pages><volume>39</volume><number>3</number><keywords><keyword>Antineoplastic Agents/adverse effects/therapeutic use</keyword><keyword>Antineoplastic Combined Chemotherapy Protocols/adverse effects/therapeutic use</keyword><keyword>Carcinoma, Neuroendocrine/*drug therapy/pathology</keyword><keyword>Gastrointestinal Neoplasms/*drug therapy/pathology</keyword><keyword>Humans</keyword><keyword>Pancreatic Neoplasms/*drug therapy/pathology</keyword><keyword>Prognosis</keyword></keywords><dates><year>2013</year><pub-dates><date>May</date></pub-dates></dates><isbn>1532-1967 (Electronic)&#xD;0305-7372 (Linking)</isbn><accession-num>22819619</accession-num><urls><related-urls><url>;[16]. In the large retrospective NORDIC study, which included 305 patients with a diagnosis of advanced EP-NEC (252 treated with chemotherapy), cisplatin-based and carboplatin-based regimens were associated with comparable first-line response rates (RRs), progression-free-survival (PFS) and OS PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Tb3JieWU8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxS

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ADDIN EN.CITE.DATA [17]. However, evidence on CarboEtop in advanced EP-PD-NEC is scarce and mainly derived from small retrospective series PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5EaSBNZWdsaW88L0F1dGhvcj48WWVhcj4yMDEwPC9ZZWFy

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ADDIN EN.CITE.DATA [6, 11, 18, 19]. As a result, there is large variability in the schedules (e.g. oral or intravenous etoposide, 3- or 4-weekly schedules) and doses of CarboEtop across different centres, and which of them should be recommended remains unclear. The use of oral formulations of etoposide carries undoubtable advantages for patients and provides cost saving by reducing the frequency and duration of patient attendance to hospital. A review of the literature, including 48 studies, suggests that patients affected by either solid or haematological cancers prefer oral over intravenous anti-cancer treatments, as oral formulations are perceived as more convenient and less toxic, and can be taken at home and interfere less with work schedules ADDIN EN.CITE <EndNote><Cite><Author>Eek</Author><Year>2016</Year><RecNum>24</RecNum><DisplayText>[20]</DisplayText><record><rec-number>24</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1528100811">24</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Eek, D.</author><author>Krohe, M.</author><author>Mazar, I.</author><author>Horsfield, A.</author><author>Pompilus, F.</author><author>Friebe, R.</author><author>Shields, A. L.</author></authors></contributors><auth-address>AstraZeneca, Gothenburg, Sweden.&#xD;Adelphi Values, Boston, MA, USA.&#xD;AstraZeneca, Macclesfield, UK.</auth-address><titles><title>Patient-reported preferences for oral versus intravenous administration for the treatment of cancer: a review of the literature</title><secondary-title>Patient Prefer Adherence</secondary-title></titles><periodical><full-title>Patient Prefer Adherence</full-title></periodical><pages>1609-21</pages><volume>10</volume><keywords><keyword>literature review</keyword><keyword>mode of administration</keyword><keyword>oncology</keyword><keyword>patient preference</keyword><keyword>treatment</keyword></keywords><dates><year>2016</year></dates><isbn>1177-889X (Print)&#xD;1177-889X (Linking)</isbn><accession-num>27601886</accession-num><urls><related-urls><url>;[20]. Randomised trials comparing oral versus intravenous etoposide in combination with cisplatin for the treatment of patients with SCLC have shown that the two formulations of etoposide have equivalent activity and efficacy outcomes, and a similar toxicity profile ADDIN EN.CITE <EndNote><Cite><Author>Rezonja</Author><Year>2013</Year><RecNum>25</RecNum><DisplayText>[21]</DisplayText><record><rec-number>25</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1528101249">25</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Rezonja, R.</author><author>Knez, L.</author><author>Cufer, T.</author><author>Mrhar, A.</author></authors></contributors><auth-address>Krka, d.d., Novo mesto, Slovenia.</auth-address><titles><title>Oral treatment with etoposide in small cell lung cancer - dilemmas and solutions</title><secondary-title>Radiol Oncol</secondary-title></titles><periodical><full-title>Radiol Oncol</full-title></periodical><pages>1-13</pages><volume>47</volume><number>1</number><keywords><keyword>bioavailability</keyword><keyword>oral etoposide</keyword><keyword>pharmacokinetic variability</keyword><keyword>small cell lung cancer</keyword></keywords><dates><year>2013</year><pub-dates><date>Mar</date></pub-dates></dates><isbn>1318-2099 (Print)&#xD;1318-2099 (Linking)</isbn><accession-num>23450046</accession-num><urls><related-urls><url>;[21]. However, some pharmacokinetic studies have shown that oral etoposide, compared to intravenous etoposide, has a higher inter- and intra-individual variability in bioavailability, which might result in suboptimal tumour activity and increased toxicity PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5IYW5kZTwvQXV0aG9yPjxZZWFyPjE5OTk8L1llYXI+PFJl

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ADDIN EN.CITE.DATA [24].Therefore, acknowledging the difficulties in pursuing randomised comparisons between different schedules of CarboEtop in the context of a rare disease, the current study aimed to conduct a large, retrospective, bi-centre, data collection on treatment outcomes of carboplatin in combination with either oral or intravenous etoposide for advanced EP-PD-NEC, to inform clinical practice. 3. Materials and methodsThis retrospective, bi-centre study was approved by The Christie NHS Foundation Trust Audit committee (SE17/1992) and the local audit committee of The European Institution of Oncology. Informed signed consent from individual patients was not required to be obtained.Patient eligibility criteria for inclusion in this study were: histologically or cytologically proven diagnosis of neuroendocrine neoplasms with a Ki-67 index ≥20%; a primary tumour from outside the lung (extra-pulmonary) [patients with unknown primary tumours were included, provided a lung origin was ruled out], advanced stage disease not amenable to curative treatment, and receipt of at least one line of palliative chemotherapy with CarboEtop (any schedule) [patients who received re-challenge with carboplatin and etoposide were allowed]. Exclusion criteria were: known well-differentiated morphology (morphology was not systematically reviewed for all patients with unreported morphology); failed completion of at least one cycle of CarboEtop, or date of death or last follow-up visit/contact not available. Eligible patients were identified among those referred to and treated at two European Neuroendocrine Tumour Society (ENETS) Centres of Excellence; The Christie National Health Service (NHS) Foundation Trust (Manchester, United Kingdom) and The European Institution of Oncology (Milan, Italy). All consecutive patients meeting eligibility criteria and treated between 1st September 1996 and 28th of February 2018 were considered.Patient demographic data, tumour pathological characteristics, treatment modalities and outcomes (activity, efficacy and toxicity) were collected retrospectively from local medical records. The performance status of patients was reported according to the European Cooperative Oncology Group (ECOG) scale; where the ECOG score was not clearly stated in the medical records, it was extrapolated either by conversion from a different scale (e.g. Karnofsky) or based on the description of clinical signs and symptoms. The choice of CarboEtop schedule was as per clinician preference or local protocol. Dose intensity of CarboEtop was calculated as the percentage of dose actually delivered to a patient, taking as reference the full dose estimated to be delivered based on the number of cycles of CarboEtop administered. Radiological response to CarboEtop was assessed by conventional imaging and classified according the Response Evaluation Criteria in Solid Tumours (RECIST) version 1.1 ADDIN EN.CITE <EndNote><Cite><Author>Eisenhauer</Author><Year>2009</Year><RecNum>18</RecNum><DisplayText>[26]</DisplayText><record><rec-number>18</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1526946145">18</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Eisenhauer, E. A.</author><author>Therasse, P.</author><author>Bogaerts, J.</author><author>Schwartz, L. H.</author><author>Sargent, D.</author><author>Ford, R.</author><author>Dancey, J.</author><author>Arbuck, S.</author><author>Gwyther, S.</author><author>Mooney, M.</author><author>Rubinstein, L.</author><author>Shankar, L.</author><author>Dodd, L.</author><author>Kaplan, R.</author><author>Lacombe, D.</author><author>Verweij, J.</author></authors></contributors><auth-address>National Cancer Institute of Canada-Clinical Trials Group, 10 Stuart Street, Queen&apos;s University, Kingston, Ontario, Canada. eeisenhauer@ctg.queensu.ca</auth-address><titles><title>New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1)</title><secondary-title>Eur J Cancer</secondary-title></titles><periodical><full-title>Eur J Cancer</full-title></periodical><pages>228-47</pages><volume>45</volume><number>2</number><keywords><keyword>Clinical Trials as Topic</keyword><keyword>Disease Progression</keyword><keyword>Europe</keyword><keyword>Humans</keyword><keyword>Lymph Nodes/pathology</keyword><keyword>Magnetic Resonance Imaging</keyword><keyword>Neoplasms/*pathology/*therapy</keyword><keyword>Tomography, X-Ray Computed</keyword><keyword>Treatment Outcome</keyword></keywords><dates><year>2009</year><pub-dates><date>Jan</date></pub-dates></dates><isbn>1879-0852 (Electronic)&#xD;0959-8049 (Linking)</isbn><accession-num>19097774</accession-num><urls><related-urls><url>;[26]. When measurements of target tumour lesions were not provided, original scan images were reviewed by a Radiologist Specialist with expertise in NENs for RECIST 1.1 calculation. Waterfall plots were generated by plotting variations in marker lesions at the time of the best response achieved (compared to baseline). Progression-free-survival (PFS), time-to-progression (TTP) and OS were defined as the time from the beginning of CarboEtop chemotherapy to the time of radiological/clinical progression, or death from any cause (PFS), radiological progression (TTP) or death from any cause (OS), respectively. Adverse events (AEs) of CarboEtop were classified according to the National Institutes of Health Common Terminology Criteria for Adverse Events (CTCAE), version 4.03 [. July 20th, 2018]. Myelosuppression was defined as the presence of at least one haematological AE (anaemia, thrombocytopenia or neutropenia).3.1. Statistical analysisPercentages, median values, ranges and 95%-confidence intervals (95%-CIs) were calculated for description of categorical and continuous variables, as appropriate. Pearson chi-square, Fisher’s exact tests and Student-T test were used as required. Receiver operating characteristic (ROC) and calculation of area under the curve (AUC) were used for identification of Ki-67 cut-offs. Kaplan-Meier analysis was applied to estimate median values, hazard ratio (HR) and 95%-CIs of survival outcomes. Log-rank test for equality of survivors function, Cox-regression univariate and multivariable analyses were used to interrogate potential correlations between survival outcomes and patient clinical-pathological characteristics at baseline or treatment-related data (schedules, causes of treatment discontinuation, dose intensity) in the first-line setting. Probability values (p) were considered statistically significant at a level below 0.05. Variables reaching statistical significance in univariate analysis were included in the multivariable analysis. Descriptive and inferential statistical analyses were performed using the “Statistics and Data” (STATA) software package. 4. Results4.1. Patients characteristicsOne-hundred and thirteen patients met the criteria for inclusion in this study. The median follow-up time was 11.5 months (range; 0.4-99.7). The median age at the beginning of CarboEtop was 65.8 years (range; 24-88). The majority of patients were male (63.7%) and had a primary tumour from the gastro-entero-pancreatic (GEP) tract (54.0%). Small cell carcinoma was the predominant histological subtype (48.7%). Five (4.4%) patients had previous potentially-curative surgery for early stage EP-PD-NEC. Among them, 4 received adjuvant chemotherapy [cisplatin and etoposide (2 patients), streptozotocin and capecitabine (1 patient), cisplatin and gemcitabine (1 patient)] and 1 patient received both neoadjuvant chemo-radiotherapy and adjuvant chemotherapy with 5-fluorouracil/leucovorin and oxaliplatin. Additional baseline patient and tumour characteristics are presented in Table 1.Frequency distribution of Ki-67 values is illustrated in Figure 1.4.2. Treatment modalities of CarboEtopTreatment modalities are illustrated in Figure 2. A total of 123 courses of CarboEtop were administered; 106 (86.2%) in the first-line, 16 (13.0%) in the second-line and 1 (0.8%) in the third-line setting. Ten (8.8%) patients treated with CarboEtop in first-line received re-challenge CarboEtop in second-line. The following schedules of CarboEtop were applied (Supplementary Table S1): CarboEtop-1; etoposide 50 mg twice daily orally from day 1 to day 7 (inclusive) followed by carboplatin area under the curve (AUC) 5, intravenously on day 8, every 28 days; CarboEtop-2; etoposide 120 mg/m2 intravenously on days 1, 2, and 3, and carboplatin AUC 5 or 6 intravenously on day 1, every 21 days; CarboEtop-3; etoposide 100 mg/m2 intravenously on days 1, 2, and 3, and carboplatin AUC 4 or 5 intravenously on day 1, every 21 days; CarboEtop-4; etoposide 120 mg/m2 intravenously on day 1 and 100-150 mg twice daily orally on days 2 and 3, and carboplatin AUC 5 intravenously on day 1, every 21 days. A higher proportion of patients received intravenous etoposide compared to oral etoposide, both in first-line (54.7% versus 45.3%) and second/third-line (58.8% versus 41.2%). The median time on chemotherapy was 3.6 months (range; 0.4-9.9) in first-line and 3.2 months (range; 0.9-6.4) in second/third-line. The median number of cycles of CarboEtop delivered was 4 (range; 1-13) in first-line and 4 (range; 1-8) in second/third-line. Causes of CarboEtop discontinuation included; completion of planned treatment period (41.5%), deterioration in general condition/clinical progression (25.2%), toxicity (14.6%), patient decision (10.6%) and death (8.1%). There were no statistically significant differences in the frequencies of causes of treatment discontinuation between schedules with oral and intravenous etoposide in the first-line setting (Supplementary Table S2).The dose-intensity of CarboEtop could be calculated for 82 courses of treatment, and the median value was 94.3% (95%-CI; 91.3-99.8), when all courses/lines of treatment were included, 95.7% (95%-CI; 91.7-100) in first-line and 91.1% (95%-CI; 84.7-100) in second/third-line. The median dose-intensity of CarboEtop in first-line did not differ significantly between schedules with oral and intravenous etoposide [99.7% (95%-CI; 92.1-100.0) versus 91.8% (95%-CI; 83-96.8), respectively; p = 0.367].4.3. Activity outcomes of CarboEtopRadiological response to CarboEtop could be assessed for 111 courses (90.2%) of treatment. The most common best response (BR) achieved was partial response (PR) in first-line (40.8%) and stable disease (SD) in second/third-line (38.45%). The median time to BR was 2.9 months (95%-CI; 2.5-3.0) in first-line and 2.7 (95%-CI; 2.1-4.5) in second/third-line. Further details on the activity of CarboEtop are provided in Table 2 and Supplementary Figure S1. Comparisons were made between activity outcomes of schedules with oral and intravenous etoposide in first-line. No statistically significant differences were found in disease-control-rate (DCR) [complete response (CR) + PR + SD] between oral [69.8% (95%-CI; 55.5-84.1)] and intravenous [80.8% (95%-CI; 69.7-91.8)] etoposide (p = 0.237). Even though there was a trend towards improved objective response rate (ORR) [CR + PR] for intravenous [57.7% (95%-CI; 43.8-71.6)] versus oral [37.2% (95%-CI; 22.2-52.3)] etoposide, the difference did not achieve statistical significance (p = 0.064).Response to treatment was assessed according to the Ki-67 value (dichotomised at <55% vs ≥55%) for patients receiving CarboEtop as a first-line treatment. No differences in ORR were identified; 50.0% (Ki-67 <55%) versus 50.0% (Ki-67 ≥55%); p = 1.000. Alternative Ki-67 cut-offs were explored with the intention of using Ki-67 as a predictive factor of response [defined as radiological response (CR+PR) or prolonged PFS (defined as PFS above 6 months)]. A Ki-67 value of 70% seemed to be the most informative cut-off, even though performance was poor for both ORR (AUC 0.45 (95%-CI 0.33-0.57); sensitivity 51.2%, specificity 36.2%) and prolonged-PFS (AUC 0.52 (95%-CI 0.39-0.65); sensitivity 55.0%, specificity 42.5%). 4.4 Toxicity profile of CarboEtopToxicity data of CarboEtop was available for 122 (99.2%) courses of treatment. When all courses/lines of treatment were pooled together, the most common grade 1-2 AEs were fatigue (74.0%), nausea/vomiting (56.9%) and myelosuppression (58.2%), whereas the most common grade 3-4 AEs included myelosuppression (49.2%), neutropenia (30.1%) and anaemia (17.1%). There were no statistically significant differences in grade 3-4 AEs between schedules with oral and intravenous etoposide, with the exception of grade 3-4 venous thromboembolism which was significantly more frequent among patients receiving oral etoposide (p = 0.045). Full data is available in Table 3. 4.5 Efficacy outcomes of CarboEtopAt the time of data cut-off (30th April 2018), 83.7%, 94.3% and 91.3% of TTP, PFS and OS events were available, respectively. The median PFS and TTP for patients receiving CarboEtop were 5.8 (95%-CI; 4.8-7.0) and 6.2 months (95%-CI; 5.3-7.6) respectively: 6.0 (95%-CI; 5.0-7.1) and 6.7 months (95%-CI; 5.4-7.8) respectively, in first-line, and 4.5 (95%-CI; 2.3-10.9) and 4.5 months (95%-CI; 2.4-10.9) respectively, in second/third line (Kaplan-Meier curves illustrated in Figure 3A). The median OS for patients receiving CarboEtop was 11.6 months (95%-CI; 9.3-13.6), 11.5 months (95%-CI; 8.9-13.6) in first-line and 12.5 months (95%-CI; 5.5-23.4) in second/third-line (Kaplan-Meier curves illustrated in Figure 3D).Univariate (univ) and multivariable (multiv) Cox-regression analyses for PFS and OS in the first-line setting, according to baseline clinical-pathological characteristics and CarboEtop schedules are presented in Table 4. The presence of liver metastases was the only factor independently associated with worse PFS (multiv-Cox-p = 0.015) and OS (multiv-Cox-p = 0.002) (Kaplan-Meier curves illustrated in Figure 3B and 3E). Noticeably, the presence of lung metastases correlated with shorter OS on multivariable analysis, even though findings did not reach statistical significance (multiv-Cox-p = 0.051). No statistically significant differences were found in PFS (univ-Cox p = 0.179) nor in OS (univ-Cox p = 0.069) between schedules with oral and intravenous etoposide, even though a trend towards prolonged OS was identified in favour of intravenous formulations (Kaplan-Meier curves illustrated in Figure 3C and 3F).4.6. CarboEtop re-challengeTen of the patients who received CarboEtop as first-line treatment had a re-challenge with CarboEtop as second-line. All patients who were offered re-challenge with CarboEtop had a first-line PFS >6 months [median PFS 11.5 months (95%-CI; 7.0-15.4)], which is suggestive of sensitivity to platinum, and 90.0% had achieved radiological objective response (CR+PR) in first-line. Median time from completion of first-line chemotherapy to initiation of re-challenge with CarboEtop was 9.8 months (95% CI 6.5-21.6). Results obtained by re-challenge with CarboEtop seemed less favourable than those achieved with the same regimen in the first-line setting with regard to both median PFS [4.4 months (95%-CI; 1.6-10.9); Log-rank-p = 0.566] and ORR [33.3%; p = 0.200].5. DiscussionThis study presents activity, efficacy and toxicity data from one of the largest pooled series of patients with advanced EP-PD-NEC treated with CarboEtop in the published literature. In the NORDIC study, 67 patients were treated with CarboEtop and a further 56 patients received a triple-drug combination including carboplatin, etoposide and vincristine or other drugs PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Tb3JieWU8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxS

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ADDIN EN.CITE.DATA [11, 12]. By far, only two other small retrospective studies by Di Meglio et al. ADDIN EN.CITE <EndNote><Cite><Author>Di Meglio</Author><Year>2010</Year><RecNum>15</RecNum><DisplayText>[18]</DisplayText><record><rec-number>15</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1526924583">15</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Di Meglio, G.</author><author>Massacesi, C.</author><author>Radice, D.</author></authors></contributors><titles><title>Carboplatin with etoposide in patients with extrapulmonary &quot;aggressive&quot; neuroendocrine carcinoma</title><secondary-title>J Clin Oncol</secondary-title></titles><periodical><full-title>J Clin Oncol</full-title></periodical><pages>e13072, conference abstract</pages><volume>Suppl</volume><dates><year>2010</year></dates><urls></urls></record></Cite></EndNote>[18] and Imai et al. ADDIN EN.CITE <EndNote><Cite><Author>Imai</Author><Year>2016</Year><RecNum>16</RecNum><DisplayText>[19]</DisplayText><record><rec-number>16</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1526924653">16</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Imai, H.</author><author>Shirota, H.</author><author>Okita, A.</author><author>Komine, K.</author><author>Saijo, K.</author><author>Takahashi, M.</author><author>Takahashi, S.</author><author>Takahashi, M.</author><author>Shimodaira, H.</author><author>Ishioka, C.</author></authors></contributors><titles><title>Efficacy and Safety of Carboplatin and Etoposide Combination Chemotherapy for Extrapulmonary Neuroendocrine Carcinoma: A Retrospective Case Series</title><secondary-title>Chemotherapy</secondary-title></titles><periodical><full-title>Chemotherapy</full-title></periodical><pages>111-6</pages><volume>61</volume><number>3</number><keywords><keyword>Adult</keyword><keyword>Aged</keyword><keyword>Antineoplastic Combined Chemotherapy Protocols/administration &amp; dosage/adverse</keyword><keyword>effects/*therapeutic use</keyword><keyword>Carboplatin/administration &amp; dosage</keyword><keyword>Carcinoma, Neuroendocrine/*drug therapy/pathology</keyword><keyword>Disease-Free Survival</keyword><keyword>Etoposide/administration &amp; dosage</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Retrospective Studies</keyword><keyword>Survival Rate</keyword><keyword>Treatment Outcome</keyword></keywords><dates><year>2016</year></dates><isbn>1421-9794 (Electronic)&#xD;0009-3157 (Linking)</isbn><accession-num>26636658</accession-num><urls><related-urls><url>;[19] have specifically looked at treatment outcomes of CarboEtop in patients with advanced EP-NEC and included 20 and 19 patients, respectively. Although results from other studies on the use of platinum-based chemotherapy in advanced EP-PD-NEC are rather heterogeneous, due to differences in patient selection criteria, treatment protocols and population size (ORR; 31-67%, DCR; 62-79%, median PFS/TTP; 4-9 months, median OS; 7.3-20 months) PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5IZWV0ZmVsZDwvQXV0aG9yPjxZZWFyPjIwMTU8L1llYXI+

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ADDIN EN.CITE.DATA [3, 4, 6-8, 11, 12, 18, 19, 27], first-line activity and efficacy outcomes of CarboEtop in the present study were in line with data from the current literature. In particular, first-line RRs were very close to those of CarboEtop reported in the two studies by Di Meglio et al. ADDIN EN.CITE <EndNote><Cite><Author>Di Meglio</Author><Year>2010</Year><RecNum>15</RecNum><DisplayText>[18]</DisplayText><record><rec-number>15</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1526924583">15</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Di Meglio, G.</author><author>Massacesi, C.</author><author>Radice, D.</author></authors></contributors><titles><title>Carboplatin with etoposide in patients with extrapulmonary &quot;aggressive&quot; neuroendocrine carcinoma</title><secondary-title>J Clin Oncol</secondary-title></titles><periodical><full-title>J Clin Oncol</full-title></periodical><pages>e13072, conference abstract</pages><volume>Suppl</volume><dates><year>2010</year></dates><urls></urls></record></Cite></EndNote>[18] and Imai et al. ADDIN EN.CITE <EndNote><Cite><Author>Imai</Author><Year>2016</Year><RecNum>16</RecNum><DisplayText>[19]</DisplayText><record><rec-number>16</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1526924653">16</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Imai, H.</author><author>Shirota, H.</author><author>Okita, A.</author><author>Komine, K.</author><author>Saijo, K.</author><author>Takahashi, M.</author><author>Takahashi, S.</author><author>Takahashi, M.</author><author>Shimodaira, H.</author><author>Ishioka, C.</author></authors></contributors><titles><title>Efficacy and Safety of Carboplatin and Etoposide Combination Chemotherapy for Extrapulmonary Neuroendocrine Carcinoma: A Retrospective Case Series</title><secondary-title>Chemotherapy</secondary-title></titles><periodical><full-title>Chemotherapy</full-title></periodical><pages>111-6</pages><volume>61</volume><number>3</number><keywords><keyword>Adult</keyword><keyword>Aged</keyword><keyword>Antineoplastic Combined Chemotherapy Protocols/administration &amp; dosage/adverse</keyword><keyword>effects/*therapeutic use</keyword><keyword>Carboplatin/administration &amp; dosage</keyword><keyword>Carcinoma, Neuroendocrine/*drug therapy/pathology</keyword><keyword>Disease-Free Survival</keyword><keyword>Etoposide/administration &amp; dosage</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Retrospective Studies</keyword><keyword>Survival Rate</keyword><keyword>Treatment Outcome</keyword></keywords><dates><year>2016</year></dates><isbn>1421-9794 (Electronic)&#xD;0009-3157 (Linking)</isbn><accession-num>26636658</accession-num><urls><related-urls><url>;[19], whereas survival outcomes closely mirrored those of CarboEtop in the NORDIC study PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Tb3JieWU8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxS

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ADDIN EN.CITE.DATA [6]. This suggests that, although retrospective in nature, the results of the present study are reliable and provide further support to the use of CarboEtop as a valid strategy for patients with advanced, previously untreated EP-PD-NEC, with comparable outcomes to cisplatin/etoposide.The formulation of etoposide, oral versus intravenous, did not significantly impact on response rates nor on survival outcomes, even though there was a trend toward prolonged OS and improved ORR in the intravenous etoposide subgroup, which should be explored further in larger series. There are two possible explanations for this observation; 1) the difference in ORR and OS might not have achieved statistical significance because of the insufficient sample size of the two subgroups or 2) there is a still unidentified confounding factor leading to imbalance between the two subgroups which misleadingly drives better outcomes in the subgroup receiving intravenous etoposide. A recently published post-hoc analysis of the NORDIC trial reported no statistically significant differences in PFS [oral-etoposide; 5.4 months vs 24h-intravenous-etoposide; 3.8 months vs 5h-intravenous-etoposide; 5.6 months] or OS [oral-etoposide; 11.3 months vs 24h-intravenous-etoposide; 14.5 months vs 5h-intravenous-etoposide; 11 months] between patients receiving oral and intravenous etoposide in combination with cisplatin or carboplatin PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5BbGk8L0F1dGhvcj48WWVhcj4yMDE4PC9ZZWFyPjxSZWNO

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ADDIN EN.CITE.DATA [27]. However, the large disproportion in sample size between the oral-etoposide subgroup (33 patients) and the intravenous-etoposide subgroup (203 patients) might have undermined the robustness of these results. Furthermore, the proportion of patients receiving CarboEtop and activity data of oral versus intravenous formulations of etoposide are not provided. Controversial results were reported by Dorroh et al. on a large retrospective cohort of patients (n=300) with advanced small cell lung cancer (SCLC) treated with oral versus or intravenous formulations of etoposide in combination with a platinum derivative ADDIN EN.CITE <EndNote><Cite><Author>Dorroh</Author><Year>2013</Year><RecNum>35</RecNum><DisplayText>[28]</DisplayText><record><rec-number>35</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1545174711">35</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Dorroh, S.A.; Siegel, E.R.; Govindarajan, R. </author></authors></contributors><titles><title>Oral (O) versus intravenous (IV) etoposide and platinum in the treatment of extensive-stage small cell lung cancer (SCLC)</title><secondary-title>Journal of Clinical Oncology 2013 31:15_suppl, 7597-7597 </secondary-title></titles><periodical><full-title>Journal of Clinical Oncology 2013 31:15_suppl, 7597-7597</full-title></periodical><dates><year>2013</year></dates><urls></urls></record></Cite></EndNote>[28]. The study showed a statistically significant 2.2 month OS advantage in favour the ‘oral-etoposide only’ subgroup compared to the ‘any intravenous-etoposide’ subgroup. However, schedules and doses of platinum/etoposide used were not specified, and the efficacy and pharmacokinetic of platinum/etoposide chemotherapy may be different in patients with PD-NEC of lung origin.The present study is the second in the published literature, to date, describing activity and efficacy data of platinum-etoposide chemotherapy in the second-line setting of EP-PD-NEC. The other study included 23 patients and reported a median PFS and OS of 1.9 months and 5 months, respectively PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5ZYW1hZ3VjaGk8L0F1dGhvcj48WWVhcj4yMDE0PC9ZZWFy

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ADDIN EN.CITE.DATA [11]. The present study reports second-line CarboEtop outcomes consistent with those of other second-line chemotherapy regimens used in clinical practice for patients with advanced EP-PD-NEC [5-fluourouracil-based, temozolomide-based, docetaxel-based, topotecan] (ORR; 0-31%, median PFS; 2.1-6 months, median OS; 3.2-22 months) PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5IZW50aWM8L0F1dGhvcj48WWVhcj4yMDEyPC9ZZWFyPjxS

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ADDIN EN.CITE.DATA [6, 12, 29-32], and indicates that CarboEtop is an active and effective option also in the second-line setting, where appropriate. Unfortunately, when CarboEtop is used following a first-line chemotherapy with the same regimen (re-challenge), the outcomes are less encouraging than those achieved by the same patients in the first-line setting, despite adequate patient selection based on PFS >6 months and achievement of PR or CR in first-line.Noteworthy, in the present study no comparisons were sought between first- and second-line treatment outcomes of CarboEtop, as the small sample size of the second-line subgroup could have affected the reliability of the results of such comparisons. A further potential bias could be the enrichment of patients with better outcomes in the second-line subgroup, as shown by the longer median OS compared to the first-line subgroup.In the present study, correlations of survival outcomes with other patient-, tumour- and treatment-related factors (univariate and multivariable analyses) were explored only in the first-line setting to avoid potential biases related to the less favourable prognosis of patients receiving second-line treatment, and to allow indirect comparisons with other studies in advanced EP-PD-NEC, nearly all of which included only patients who did not have any previous treatment PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5IZWV0ZmVsZDwvQXV0aG9yPjxZZWFyPjIwMTU8L1llYXI+

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ADDIN EN.CITE.DATA [3, 4, 6-8, 11, 19].The present study reports that patients with liver metastases have significantly poorer first-line survival outcomes compared to patients with no liver involvement, which is in line with the findings of a Japanese study including 41 patients with advanced GEP-NEC treated with platinum-based chemotherapy PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5UZXJhc2hpbWE8L0F1dGhvcj48WWVhcj4yMDEyPC9ZZWFy

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ADDIN EN.CITE.DATA [7]. Likewise, in a large multicentre European study of high-grade GEP-NECs (313 patients) of any disease stage PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5MYW1hcmNhPC9BdXRob3I+PFllYXI+MjAxNzwvWWVhcj48

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ADDIN EN.CITE.DATA [14], the presence of liver metastases was an independent negative prognostic factor for OS. Molecular/genetic studies and comparisons with series of patients receiving first-line non-platinum-based chemotherapy or best supportive care might help clarify whether liver metastatic disease has only a prognostic significance or is suggestive of a tumour biology characterised by a reduced sensitivity to platinum-based chemotherapy. The lack of impact of the ECOG performance status on survival outcomes may be explained by the disproportion in sample size between the comparator subgroups (ECOG≥2; 17.7% versus ECOG=0-1; 80.7%), which may have hampered the emergence of potential statistically significant differences. However, some degree of inconsistency in classifying patient performance status according to the ECOG scale across clinicians or researchers who have collected data in retrospect, especially in cases where the ECOG score had to be estimated based on the clinical description, should be taken into consideration and regarded to as a potential limitation of the study. In contrast with findings from the NORDIC study PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Tb3JieWU8L0F1dGhvcj48WWVhcj4yMDEzPC9ZZWFyPjxS

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ADDIN EN.CITE.DATA [4], might have positively influenced the outcomes of the subgroup with a Ki-67 <55%. In line with the findings of the present study, a large French prospective cohort including 253 patients with EP-PD-NEC of all stages and specifically excluding well-differentiated G3-NENs, showed that a Ki-67 of <55% versus ≥55% has no prognostic significance PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5XYWx0ZXI8L0F1dGhvcj48WWVhcj4yMDE3PC9ZZWFyPjxS

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ADDIN EN.CITE.DATA [12].Furthermore, despite efforts in identifying alternative cut-offs, in the present study the performance of Ki-67 remains limited for predictive purposes. In other words, the role of Ki-67 (either as a binomial or a continuous variable) as an isolated prognostic/predictive factor for advanced EP-PD-NEC could not be confirmed. This corroborates the results of the previously mentioned large retrospective study of patients with GEP-NECs PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5MYW1hcmNhPC9BdXRob3I+PFllYXI+MjAxNzwvWWVhcj48

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ADDIN EN.CITE.DATA [14], showing that a risk-stratification score combining multiple prognostic factors has a stronger ability to discriminate between better and worse outcomes, than Ki-67 alone.A limitation of this study is that the tumour morphology and Ki-67 were not systematically assessed at the time of study entry (although cases where the morphology was reported as “well differentiated” were excluded), and a pathological review of the samples was pursued only in selected cases. Therefore, an accurate estimation of the proportion of patients with well differentiated neuroendocrine tumours as per 2017 World Health Organisation Classification ADDIN EN.CITE <EndNote><Cite><Author>Lloyd RV</Author><Year>2017</Year><RecNum>17</RecNum><DisplayText>[25]</DisplayText><record><rec-number>17</rec-number><foreign-keys><key app="EN" db-id="d9sfdde07az5dee559kx59awwrsdx2vp5ax9" timestamp="1526946068">17</key></foreign-keys><ref-type name="Book">6</ref-type><contributors><authors><author>Lloyd RV, Osamura RY, Kl?ppel G, Rosai J</author></authors></contributors><titles><title>Who Classification of Tumours of Endocrine Organs. 4th ed.</title></titles><dates><year>2017</year></dates><pub-location>Lyon</pub-location><publisher>IARC press</publisher><urls></urls></record></Cite></EndNote>[25] (if any) could not be provided, and a comparison of treatment outcomes between the poorly and well differentiated subgroups could not be pursued.In keeping with other studies of CarboEtop in lung-NEC and EP-NEC PEVuZE5vdGU+PENpdGU+PEF1dGhvcj5Sb3NzaTwvQXV0aG9yPjxZZWFyPjIwMTI8L1llYXI+PFJl

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ADDIN EN.CITE.DATA [17-19], grade 3-4 AEs observed in the present study were most commonly haematological, with neutropenia being the most frequent, whereas non-haematological grade 3-4 AEs occurred at a low frequency, consistent with an overall manageable toxicity profile. However, consideration should be given to the possible inconsistency and incompleteness in reporting AEs, which is inherent in the retrospective nature of the study. Noticeably, dose-intensity data of CarboEtop were missing for 33% of courses of treatment; this represents an attrition bias due to the fact that information on doses of chemotherapy could be retrieved only for patients with a more recent diagnosis (in contrast with toxicity data which could be extracted from medical records for nearly all patients).It has also to be acknowledged that, as the majority of patients who received CarboEtop as second-line treatment had already been treated with the same regimen in first-line (10 out of 16 patients), in order to increase the sample size of and gather as much information as possible on the second-line subgroup, survival and toxicity outcomes of CarboEtop were calculated for courses of chemotherapy instead of for individual patients, and this might have introduced potential biases.Finally, despite the effort to retrieve information from all consecutive patients over a 22 year period, potential selection biases (e.g. missed inclusion of eligible patients) related to the retrospective design of the study cannot be completely excluded. In conclusion, the present study provides further corroboration for the use of CarboEtop as an active, effective and well-tolerated alternative to other platinum-based chemotherapy regimens for the treatment of advanced EP-PD-NEC, both in first- and second-line. It also suggests that oral etoposide can be substituted for intravenous etoposide, in order to minimise the frequency and length of patient attendance to hospital, advocating patient preferences and potentially cutting down on health economic-related expenses for nursing staff, materials and facilities, with no or minimal impact on survival or additional toxicities. To investigate whether the differences observed in treatment outcomes in patients receiving schedules using oral and intravenous etoposide are only due to bias related to the retrospective nature of the data collection, or reflect actual discrepancies in the activity and efficacy of the two schedules, participation by other centres, or alternatively a pooled/meta-analysis including other studies investigating both formulations of etoposide, will be sought to further increase the study population size, and allow more reliable conclusions. 6. Statements6.1 Statement of EthicsThis study was conducted ethically in accordance with the World Medical Association Declaration of Helsinki, and was approved by The Christie NHS Foundation Trust Audit committee (SE17/1992) and the local audit committee of The European Institution of Oncology. Informed signed consent from individual patients was not required to be obtained.6.2 Disclosure StatementThe authors have declared no conflict of interest.6.3. Funding SourcesThis study was partially funded by the American Society of Clinical Oncology (ASCO) Conquer Cancer Foundation Young Investigator Award.6.4 Author contributionMelissa Frizziero, Francesca Spada; identification of eligible patients, data collection, and manuscript writing. Angela Lamarca; idea conception and study design, identification of eligible patients, statistical analysis, review and proof-reading, and approval of the final version.Nicola Fazio, Juan W Valle; idea conception and study design, review and proof-reading, and approval of the final version.Zoe Kordatou, Jorge Barriuso, Christina Nuttall, Mairéad G McNamara, Richard A Hubner, Wasat Mansoor, Prakash Manoharan; review, proof-reading, and approval of the final version.7. 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Frequency distribution of Ki-67 values assessed on diagnostic pathological samples37973015240000CharacteristicVariable N %CharacteristicVariableN%Gender Distant metFemale41 36.3%Yes10290.3%Male 72 63.7%No119.7%ECOG PSNumber of met sites098.0%Median 218272.6%Range1-6≥22017.7%N.A.21.8%ACE-27 scoreCommonest met sites (>1%)07162.8%Distant lymph nodes5856.7%11311.5%Liver5452.9%≥265.3%Bones2120.6%N.A.32.6%Lung2019.6%Peritoneum/omentum1211.8%PT siteAdrenal gland76.9%Foregut2723.9%Subcutaneous tissue43.9%Pancreas119.7%Brain 22.0%Hindgut1916.8%UKP2623.0%Ki-67Bladder108.8%Median70Biliary tract43.5%Range30-100Cervix/Ovary76.2%95%-CI60-80Prostate76.2%Mean (+/-SD)67.8 (+/- 20.0)Others21.8%<552623.0%≥556759.3%G.E.P.6154.0%N.A.2017.7%G.U.2421.2%Morphological subtypeNSE (ug/L)*Small cell5548.7%Median19.6Large cell2017.7%Range6.4-122.6Others21.8%95%-CI13.1-41.4N.A.3631.9%-1714507058025NEC = neuroendocrine carcinoma; N = number of patients; PS = performance status; ECOG = Eastern Cooperative Oncology Group; N.A. = information not available/missing; ACE-27 = adult comorbidity evaluation score-27; PT = primary tumour; met = metastasis/metastatic; foregut = oesophagus, stomach and duodenum; hindgut = colon and rectum; UKP = unknown primary (not lung); G.E.P. = gastro-entero-pancreatic tract; G.U. = genito-urinary tract; 95%-CI = 95% Confidence Interval; SD = standard deviation; NSE = neuron specific enolase; * = at the beginning of any line of carboplatin and etoposide chemotherapy00NEC = neuroendocrine carcinoma; N = number of patients; PS = performance status; ECOG = Eastern Cooperative Oncology Group; N.A. = information not available/missing; ACE-27 = adult comorbidity evaluation score-27; PT = primary tumour; met = metastasis/metastatic; foregut = oesophagus, stomach and duodenum; hindgut = colon and rectum; UKP = unknown primary (not lung); G.E.P. = gastro-entero-pancreatic tract; G.U. = genito-urinary tract; 95%-CI = 95% Confidence Interval; SD = standard deviation; NSE = neuron specific enolase; * = at the beginning of any line of carboplatin and etoposide chemotherapy-740410-480060Table 1. Baseline characteristics of patients with advanced extra-pulmonary, poorly differentiated NEC and their tumours00Table 1. Baseline characteristics of patients with advanced extra-pulmonary, poorly differentiated NEC and their tumours-583565-509270Table 2. Activity data of CarboEtop in the first-line treatment of patients with advanced extra-pulmonary, poorly differentiated NEC020000Table 2. Activity data of CarboEtop in the first-line treatment of patients with advanced extra-pulmonary, poorly differentiated NECOutcomeVariableAny line N=111 (90.2%)First-line N=98 (89.9%)Second/third line N=13 (92.9%)Response*[number of courses (%)]CR9 (8.1%)7 (7.1%)2 (15.4%)PR42 (37.8%)40 (40.8%)2 (15.4%)SD31 (27.9%)26 (26.5%)5 (38.5%)PD29 (26.1%)25 (25.5%)4 (30.8%)DCR82 (73.43%)73 (74.5%)9 (69.2%)ORR51 (45.9%)47 (47.9%)4 (30.8%)Median time to BR[months]All BR2.86 (95%CI; 2.5-3.0)2.87 (95%CI; 2.5-3.0)2.71 (95%CI; 2.1-4.5)if CR3.02 (95%CI; 1.9-4.4)3.02 (95%CI; 1.8-4.6)3.47 (95%CI; 2.5-4.4)if PR3.04 (95%CI; 2.5-4.2)3.04 (95%CI; 2.6-4.1)2.95 (95%CI; 1.2-4.7)if SD2.87 (95%CI; 2.5-3.3)2.86 (95%CI; 2.4-3.3)3.01 (95%CI; 1.6-4.6)if PD2.45 (95%CI; 2.3-2.7)2.45 (95%CI; 2.3-2.9)2.38 (95%CI; 1.9-14.1)if CR/PR3.04 (95%CI; 2.6-3.8)3.04 (95%CI; 2.6-3.7)3.47 (95%CI; 1.2-4.7)Median variation** [%]Any line N=64 (77.1%)First-line N=52 (75.4%)Second/third line N=12 (85.7%)All BR-19.1 (95%CI; -41.1- -0.8)-27.9 (95%CI; -43.3- -0.512)-15.2 (95%CI; -76.7- 14.8)if PR-48.4 (95%CI; -58.4- -44.0)-46.5 (95%CI; -58.0- -43.6)-64.6 (95%CI; -80.0- -49.2)if SD-7.3 (95%CI; -16.8-4.3)-7.3 (95%CI; -18.8-4.1)-4.7 (95%CI; -21.2-17.7)if PD+26.9 (95%CI; 15.0-37.9)+28.8 (95%CI; 15.2-42.1)+8.8 (95%CI;-13.9-68.8)PD due to new lesions8 5 3 -93345-6350NEC = neuroendocrine carcinoma; CarboEtop = carboplatin/etoposide chemotherapy; N = number of courses of CarboEtop; * = response evaluated as per RECIST 1.1. criteria; ** = percentage of variation in the sum of the sizes of “marker lesions” as defined by RECIST 1.1 criteria. CR = complete response; PR = partial response; SD = stable disease; PD = progressive disease; DCR = disease control rate (CR + PR + SD); ORR = objective response rate (CR + PR); BR = best response; 95%CI = 95% Confidence Interval.00NEC = neuroendocrine carcinoma; CarboEtop = carboplatin/etoposide chemotherapy; N = number of courses of CarboEtop; * = response evaluated as per RECIST 1.1. criteria; ** = percentage of variation in the sum of the sizes of “marker lesions” as defined by RECIST 1.1 criteria. CR = complete response; PR = partial response; SD = stable disease; PD = progressive disease; DCR = disease control rate (CR + PR + SD); ORR = objective response rate (CR + PR); BR = best response; 95%CI = 95% Confidence Interval.Univariate Cox Regression for PFSMultivariable Cox Regression for PFSUnivariate Cox Regression for OSMultivariable Cox Regression for OSVariableCategoryHR (95%-CI)p-valueHR (95%-CI)p-valueHR (95%-CI)p-valueHR (95%-CI)p-valueAge (start of CarboEtop)Continuous variable1.01 (0.98-1.02)0.8041.01 (0.99-1.02)0.541GenderMale (vs Female)1.04 (0.69-1.57)0.8371.04 (0.69-1.57)0.848MorphologySmall cell1 (Ref)-1 (Ref)-Large cell1.18 (0.69-2.02)0.5421.31 (0.76-2.28)0.336Others1.09 (0.15-8.07)0.9282.73 (0.64-11.70)0.175Ki-67Continuous variable1.01 (0.99-1.02)0.5111.01 (0.99-1.02)0.517Ki-67≥55% (vs <55%)1.29 (0.78-2.11)0.3170.99 (0.60-1.62)0.958ECOG PS>2 (vs 0/1)1.35 (0.79-2.28)0.2651.47 (0.86-2.50)0.156ACE-27 score (binary)None/Mild1 (Ref)-1 (Ref)-Moderate/Severe0.96 (0.57-1.63)0.8861.39 (0.81-2.36)0.229PT siteGEP/UKP1 (Ref)-1 (Ref)-Others1.05 (0.65-1.69)0.8521.04 (0.65-1.67)0.870Previous curative resectionYes (vs. No)1.16 (0.47-2.87)0.7500.97 (0.35-2.66)0.955Baseline NSE (ug/L)Continuous variable1.01 (0.99-1.03)0.0831.01 (0.99-1.03)0.263Stage IV*Yes (vs. No)1.8 (0.93-3.480.0801.59 (0.62-3.08)0.164Presence of distant met*Yes (vs. No)2.28 (1.05-4.99)0.0381.47 (0.62-3.48)0.3871.51 (0.72-3.13)0.273N distant met sitesContinuous variable1.24 (1.07-1.44)0.0051.14 (0.94-1.38)0.1801.16 (0.98-1.37)0.094LiverYes (vs. No)2.01 (1.33-3.03)0.0011.71 (1.11-2.63)0.0152.01 (1.32-3.06)0.0011.88 (1.28-2.76)0.002LungYes (vs. No)1.65 (0.98-2.77)0.0591.80 (1.05-3.09)0.0321.72 (1.00-2.95)0.050Distant lymph nodesYes (vs. No)1.14 (0.77-1.71)0.5110.72 (0.48-1.09)0.122Peritoneum/omentumYes (vs. No)1.02 (0.67-1.83)0.9500.94 (0.49-1.76)0.837CarboEtop scheduleIV Etop (vs. Oral Etop)0.76 (0.51-1.14)0.1790.68 (0.45-1.03)0.069CarboEtop dose intensityContinuous variable0.99 (0.98-1.02)0.9780.99 (0.97-1.01)0.232-1524006486525CarboEtop = carboplatin/etoposide chemotherapy; PFS = progression-free-survival; OS = overall-survival; PS = performance status; ECOG = Eastern Cooperative Oncology Group; ACE-27 = adult comorbidity evaluation score-27; PT = primary tumour; met = metastasis/metastatic; foregut = oesophagus, stomach and duodenum; hindgut = colon and rectum; UKP = unknown primary (not lung); G.E.P. = gastro-entero-pancreatic tract; G.U. = genito-urinary tract; HR = hazard Ratio; 95%-CI = 95% Confidence Interval; NSE = neuron specific enolase. *Stage IV disease (as per TNM staging, 7th edition) does not necessarily correspond to the presence of distant for prostate and bladder poorly differentiated neuroendocrine carcinomas.00CarboEtop = carboplatin/etoposide chemotherapy; PFS = progression-free-survival; OS = overall-survival; PS = performance status; ECOG = Eastern Cooperative Oncology Group; ACE-27 = adult comorbidity evaluation score-27; PT = primary tumour; met = metastasis/metastatic; foregut = oesophagus, stomach and duodenum; hindgut = colon and rectum; UKP = unknown primary (not lung); G.E.P. = gastro-entero-pancreatic tract; G.U. = genito-urinary tract; HR = hazard Ratio; 95%-CI = 95% Confidence Interval; NSE = neuron specific enolase. *Stage IV disease (as per TNM staging, 7th edition) does not necessarily correspond to the presence of distant for prostate and bladder poorly differentiated neuroendocrine carcinomas.-668020-692785Table 4. Univariate and multivariable analyses of factors effecting PFS and OS in patients with extra-pulmonary, poorly differentiated NEC treated with CarboEtop in the first-line setting00Table 4. Univariate and multivariable analyses of factors effecting PFS and OS in patients with extra-pulmonary, poorly differentiated NEC treated with CarboEtop in the first-line setting ................
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