Corrigendum: Childhood cancer survival in Romania—A national pediatric registry perspective

Pediatric cancer survival is increasing over time in European countries, whereas the survival varies by country (1). East-West survival differences documented in the EUROCARE-6 study both in adults as well as in children are a major concern, addressed by current European Union policies (2). Differences in cancer registration and reporting among Eastern European countries further complicate the comparison. This is particularly the case of Romania, an Eastern European country with a total population of 20 million, where national registration of cancer is still in a development process, and with regional registries achieving different coverage rates and levels of activity There is a paucity of internationally available published data on the national incidence and survival of pediatric cancer patients in Romania. This is why, in 2010, the Romanian Society of Pediatric Oncology and Haematology decided to establish a national childhood cancer registry, with all the pediatric oncology facilities in the country reporting-in new cases. Romania population numbers 4.1 million children and adolescents (aged 0-19) (representative of 21% of the total) (3,4). Data collected via the Romanian National Pediatric Oncology and Hematology Registry (RNPOHR) show that pediatric cancer makes up less than 1% of all new cancer cases in Romania, similar to the global data. According to GLOBOCAN, approximately 525 Romanians aged 0-19 are estimated to develop cancers annually, of which, according to the RNPOHR, cca 420 are undergoing treatment in the Romanian pediatric oncology network (5,6).The age-standardized incidence rate of cancers between 2010-2021 in Romanian children and adolescents (0-19) reported by RNPOHR was 9.72 per 100000 and 11.02 per 100000 in the 0-14 population (European Standard Population 2016). In 2022, RNPOHR reported 461 new cases compared to 545 estimated by GLOBOCAN, with an actual crude incidence rate of 11.16 per 100000 vs 13.8 per 100000 estimated (5,6).Age and gender distribution of pediatric cancer cases tend to follow similar patterns to the 0-14 European population for all the three 5-year age groups (0-4 years: 32.4%, 5-9 years: 22.3% 10-14 years: 23.3%), but with a notable difference for the 15-19 age group. The latter represents the largest share of EU cases, whereas in Romania this is the smallest group across all ages (22%). The male-tofemale ratio for new cases is 1.27/1, similar to global trends (6)(7)(8).Leukemia (30%), lymphoma (15%) and central nervous system (CNS) tumors (14%) top the cancer diagnosis in the Romanian pediatric population from 2010-2021, indicating a similar distribution to the European trends (6)(7)(8).The geographic distribution of registry-reported cases does not infer a significant difference in incidence according to the place of residence (urban vs rural) with an age-standardized rate (ASR) of 10.67 per 100000 in urban areas to 9.31 per 100000 in rural areas (0-19 years, European Standard Population 2016) (6)(7)(8). Still, some regional differences were noted in the number of pediatric cancer cases across economic development regions (North-East, Bucharest-Ilfov, Center, North-West, South-East, South-Muntenia, South-West Oltenia, and West). These eight economic development regions were created in Romania after EU accession to address disparities in development between geographic areas, via strategic allocation of national resources and capitalization of the local and regional resources. However, significant differences persist today, with the wealthiest region (Bucharest-Ilfov) having a per-capita GDP almost four times higher than the poorest region (North-East) (9,10). The highest regional incidence (in the 0-19 year) appears to be sourced in the North-West region with an ASR of 11.25 per 100000, while the lowest incidence is observed in the South-Muntenia and West regions, of 8.9 per 100000 (6). This may reflect the differing size of the pediatric population and possible differences in health infrastructure and the accessing care behaviour of the patient population towards the different pediatric oncology centers across regions.To date, little is known about the survival outcomes of Romanian children and adolescents with cancer at the national level, and no studies have yet compared pediatric cancer survival in Romania to other EU countries (including within the East European region). The existing Romanian studies in pediatric cancers were limited to a single institute/ single site (with focus on hematologic, brain, and solid tumors (11)(12)(13). The CONCORD-3 : analysis based on data from 322 population-based registries in 71 countries is the single international registry-based study to mention survival in child cancer in Romania, for brain tumors and acute lymphoblastic leukemia. However, the results, of a 60.1% (95% CI: 31.6, 81.5) overall survival rate in brain cancers and 53.9% (95% CI: 28.2, 79.6) were based on a very small number of cases (19, respectively 21 cases) reported for the 2010 -2014 period by the Cluj Regional Population Cancer Registry (14). The available mortality data based on the Romanian National Statistics Institute reports to Eurostat and published on the European Cancer Inequalities Registry website reflects all deaths by cancer in the 0-19 population occurring on the Romanian territory. The 2021 presented data place Romania among the EU members with the highest cancer mortality in children and adolescents with a rate of 3.8 per 100000, compared to the 2.8 EU average. Significant disparities between member countries can be noted, with the highest rates recorded for Lithuania (4.5 per 100000), Greece (4.3 per 100000) and Bulgaria (4.1 per 100000) in contrast with France and Germany (2.6 per 100000) and Italy, Finland and Hungary (2.7 per 100000). However, these data are not fully informative of the performance of the Romanian pediatric cancer care system as it doesn't distinguish between cases treated in Romanian pediatric oncology facilities and cases treated abroad as well as cases (18+ years) treated in adult cancer facilities (14,15). More so, there have been no studies of the determinants of survival outcomes in Romania and their impact on the potential differences to other EU member countries. The significant regional disparity across economic development regions, most likely results in differing availability of pediatric specialty care and lab/imaging services across economic development regions as well as rural and urban areas (9). Additionally, survival outcomes could also likely differ between rural and urban pediatric cancer patients due to a huge rural-urban disparity in the healthcare infrastructure (the health facilities and the number of hospitals in urban versus rural = 4.5: 1 and 8.9 :1) in Romania (16,17).Given the scarcity of quality pediatric cancer survival data in Romania in the current literature, we took advantage of the only existing national-level data from the RNPOHR with a linkage to economic development regions and rural-urban designation information (6).We aimed to fill the current information gap by conducting a retrospective cohort study in Romanian children and adolescents (0-19 years) diagnosed with cancers spanning over 10 years and examining the potential disparity in survival outcomes of these patients, both from an international European perspective as well as among population groups in Romania.This study was conducted in Romania. Reporting of cancers can be historically traced in Romania to the '80s. With Romania's EU accession in 2007, a Ministerial Order updated the rules and procedures of cancer reporting, to ensure compliance of the cancer reporting process, data collection, classification, and codification with the standards from the European Network of Cancer Registers and the International Agency for Research on Cancer. The same regulatory document established regional cancer registers rooted in each of the eight development regions (18).However, insufficient regulatory reinforcement and funding hampered the development and reporting output of the regional cancer registry network.Given the rarity of pediatric cancers, the national pooling of cases is critical, as well as the adaptation of the reporting process to childhood cancer specificities. Therefore, in 2010 the Romanian Society of Pediatric Oncology and Hematology established the RNPOHR which collects data for analysis purposes for all the cases taken up by Romanian pediatric oncology facilities. RNPOHR receives data from 13 registrars from respective pediatric oncology centres across the nation (6). Trained personnel from these centers report the cancer diagnosis by filling out forms based on the ENCR minimum recommended dataset. Since 2018, reporting has been performed via a dedicated secured digital platform and the dataset has been expanded /customized to fit pediatric cancer registration requirements (such as automatic assignment to ICCC-3 tumor categories, Toronto staging system etc.). Staff at the centers also collect other clinical and demographic information of patients to establish a complete profile for patients. Specifically, tumors are classified according to the International Classification of Disease and Oncology, 3 rd edition (ICD-O-3), and the International Classification of Childhood Cancer, 3 rd edition (ICCC-3). ICCC-3 assignment is based on the morphological and topographic coding of tumor according to ICD-O-3 classification. 12 primary ICCC-3 cancer types included leukemia, lymphoma, CNS tumor, neuroblastoma, soft tissue and other extraosseous sarcomas, retinoblastoma, renal tumor, hepatic tumor, malignant bone tumor, germ cell tumors, other malignant epithelial neoplasms and malignant melanomas, and other and unspecified malignant neoplasms (19,20).For each case, the information retrieved from different sources is aggregated based on the personal identification number. Each cancer case is verified, coded and finalised by one trained cancer registrar in the central setting of the Registry. In addition, each report is subject to an automatic validation procedure via Version 2.2.8 of the JRC-ENCR Quality Check Software.RNPOHR has an estimated coverage of 80% of the total national number of new cases. The cases that escape capture are likely patients aged 17 and more who are taken up by adult cancer facilities as well as the cases that seek care across borders without accessing the national pediatric cancer care network. Also, the RNPHOR does not automatically receive death certificate (DC) notifications from the Office of Vital Statistics, nor from pathology labs. Ascertaining of the vital status is possible only for reported cases included in the registry database. 93.5% of the registry cases are microscopically verified.The study population consisted of individuals who were diagnosed with cancer between January Because the survival differs by cancer type, a sub-analysis was done in 2432 individuals focusing on the common cancer subtypes such as lymphoid leukemias, Hodgkin lymphomas, astrocytomas and intracranial and intraspinal embryonal tumours, neuroblastoma and ganglioneuroblastoma, nephroblastoma and other nonepithelial renal tumors, osteosarcomas and Ewing tumor and related sarcomas of bone, and rhabdomyosarcomas.The study included the following sociodemographic variables: age (year), sex (male/female), geography (rural/urban), and economic development regions (North-East, Bucharest-Ilfov, Center, North-West, South-East, South-Muntenia, South-West Oltenia, and West). Patients' clinical information was retrieved from patients' documented 12 primary ICCC-3 cancer cancer subtypes leukemias, Hodgkin lymphomas, astrocytomas intracranial and intraspinal embryonal tumors, neuroblastoma and ganglioneuroblastoma, nephroblastoma and other nonepithelial renal tumors, osteosarcomas Ewing tumor and related sarcomas of bone, and and in versus and reported treatment no and other versus a of the reported designation was coded according to the of the of the a European the and the of in Romania urban and rural and small areas the analysis small which share more infrastructure and economic with and were included in the rural for the higher share of the rural patients in the study collected was and all results were reported at a of The was to patients' by the treatment type, status of and treatment such as was for the patients' and clinical information by survival was for major and age place of residence (urban vs and ICCC-3 tumor and but survival could not be due to data for and were at years the for cases diagnosed between 2010 and survival are by group age by sex and by and were to the and by development and major cancer In the and clinical such as development regions, treatment and primary cancer types were procedure was in the to the most and significant was to the survival in rural and urban was from the Romanian of the Romanian Society for Pediatric Oncology and Hematology and the current study patients (0-19 diagnosed with cancer and reported to the cancer registry with a of years The age of the patients is the age the are years by 15-19 years with patients in the 10-14 years group only The of patients in the North-West and South-Muntenia regions The lowest of are from the West with only of the total the are from rural areas, and are to the treatment type, and were treated by was the most while only 1 patient reported treatment by and were the most common treatment of has the most in almost at by and to a by rates of other (such as were to reporting, information on cell could not be cancer are of malignant behaviour while the of the cases are CNS the distribution of the according to the ICCC-3 most of the are diagnosed with leukemias, and by and neoplasms and CNS and intracranial and intraspinal neoplasms of the patients are diagnosed with hepatic and with while the lowest is by other and unspecified malignant for ICCC-3 lymphoid Hodgkin and astrocytomas and intracranial and intraspinal embryonal tumors are the most diagnosed cancers in these children and distribution of the in 1 is similar between 0-14 and 15-19 age a higher of patients in rural areas vs patients' and clinical by rural and urban More patients diagnosed with cancer are in rural areas to who urban areas compared to the patients in urban areas, more rural from cancers The gender doesn't to be significant related to the place of residence = but patients in rural areas as to who in urban regions The in the 10-14 and 15-19 age groups in rural and while only aged between and years in urban the economic development regions, a notable difference was observed in the where of the patients in rural whereas only the urban regions and in South-Muntenia where of the in rural areas, while the urban Bucharest-Ilfov, a the the highest per of urban as to who in rural The distribution of the development regions is different in rural areas versus urban areas treatment was in for children from rural areas and in for in urban The most common treatment in both rural and urban patients is treatment was to patients from rural and to patients from urban The most was with in of the in rural regions and in of the in urban no were the geography and = ICCC-3 = and ICCC-3 = overall 5-year survival rate for all the cases diagnosed between 2010 to in the 0-19 years population was (95% CI: the study 5-year overall survival for 0-14 and 15-19 age groups was (95% CI: and (95% CI: respectively further by age groups for 0-14 age the survival rates were (0-4 years) and an international survival analysis by ICCC-3 was performed for the group. 5-year overall survival rates that Hodgkin lymphoma CI: nephroblastoma and other nonepithelial renal tumors CI: and lymphoid CI: the highest survival rates among all the major cancer The survival was observed for CNS tumors CI: CI: bone tumors CI: and neuroblastoma CI: as in The 5-year survival in the 0-19 years group is in also the by tumor in the study population (aged diagnosed in the that Hodgkin lymphoma CI: nephroblastoma and other nonepithelial renal tumors CI: and lymphoid CI: the highest survival rates among all major cancer with Hodgkin and nephroblastoma and other nonepithelial renal tumors CI: and CI: of mortality from cancers compared to patients with lymphoid The mortality for patients with the other four cancers were all higher than for the patients with lymphoid and intracranial and intraspinal embryonal tumors CI: osteosarcomas and Ewing tumor CI: CI: and neuroblastoma CI: the survival of pediatric cancer by rural-urban compared to urban the of from cancer in rural was higher than urban CI: after for other such as age in years, development regions, treatment and primary cancer The survival rate for rural was than urban CI: vs CI: to the patients in the patients in Bucharest-Ilfov, Center, and West and for from cancers for CI: for CI: for CI: as presented in = study is the to report on pediatric cancer survival in Romania based on national cancer registry for a to international in child cancer the overall survival outcomes in different age groups and by cancer subtypes and also potential differences in pediatric cancer mortality by and economic development as a to a more the of determinants of cancer survival of Romanian children and results show a significant difference in survival for Specifically, 5-year survival in the 0-14 group of study population is than the EU and with a major gap to countries such as and but to Bulgaria Lithuania and other Eastern European published by national a such as the Childhood Cancer Registry report a 5-year survival of in the years while the National Registry of Childhood on website a survival of in the 0-14 spanning from to the study not differences in survival among age groups in 80% for the in study the 5-year overall survival rates a to with (0-4 years) and the 15-19 years group of survival was data are available in published analysis on this age childhood population-based cancer registries not collect data on patients diagnosed at the ages of 15-19 years varies by tumor type, with some cancers less in survival over time than a that can be observed in all countries, according to the survival rates in survival for bone tumors, lymphoma and crude 5-year observed survival results in the 0-14 age group for cases diagnosed between 2010 and to results for ICCC-3 we could that the gap in survival rates between Romania and the EU as well as among countries in Eastern vs other European regions differs by In this crude rates were in to countries survival data as published in the Hodgkin and are the tumors with the smallest difference in 5-year survival rates between Romania and the European as from the EUROCARE-6 differences in up to a gap between Romania and the European were in vs and vs and vs these tumours, significant differences are also noted within the Eastern European countries with similar survival rates in the lowest of the in Romania, Lithuania and largest disparities in survival to in were recorded for the CNS and intracranial and intraspinal neoplasms and in Romania vs the European and in malignant bone vs in osteosarcomas and vs in Ewing These are also the cancers with the largest in survival across countries, to the European region to which survival disparities are due to differences in distribution could not be in study of insufficient data on staging and other a similar also reported in the However, data differences in to have been published in in a of to for European children and adolescents by The study that in some countries less than of the were with the of The analysis across the different countries that the lowest availability rates were in European countries with survival Romania, Bulgaria and the countries same of is in the of clinical available to children and which varies between countries, from to over According to data published on the European Cancer Inequalities Registry the lowest in clinical is in the Eastern European countries with survival Romania, and the countries as noted in the the is In Romania's case, the RNPOHR report an analysis of national trends in pediatric cancer 5-year survival outcomes between the diagnosed cohort and the diagnosed In the 0-14 population crude 5-year survival in all cancers has from (95% CI: to (95% CI: a that reported by EUROCARE-6 for the European average. the small number of cases, survival appears to have more for with the lowest survival such as malignant and CNS (95% CI: to (95% CI: : and malignant bone (95% CI: in the cohort to (95% CI: : in the most significant to diagnosis and treatment in Romania were after the Romanian Society of Pediatric Oncology and Hematology the registry to at the trends in cancer outcomes from 2010 to by the crude survival rates between 3 of cases, diagnosed in vs vs The results to an impact of the in diagnosis and on a as well as the of new the availability of on a rates from (95% CI: in to (95% CI: for to (95% CI: in study also potential survival among population in Romania, to and such as place region of study reported survival in the patients in rural areas and survival in and West and development regions as compared to that the survival of pediatric cancer was with of treatment and to pediatric cancer centers as having to care and with more for were reported in and countries to have survival than their urban with some where is study also reported survival of rural pediatric cancer patients in European countries than in countries the the current study reported the rural-urban disparities in economic development region Romanian patients were more likely to be in the region where the per is lowest across all eight The rural population in the region is from the of the it for to pediatric cancer treatment facilities and services that are most available in the of the region (9). areas in Romania have also infrastructure in areas such as and This may the to care and diagnosis to and treatment in rural show a survival rate and a higher of death in rural pediatric cancer patients than their urban all from countries where rural are also more likely to and and to have in to cancer treatment centers and services to the insufficient and on rates in rural areas could also the to care The regional differences in survival in this study could be of the limited resources and health services in regions where rural were more the region where the most rural population was to have the highest mortality national levels in Romania towards European countries, regional disparities in levels have the in Romania This economic further rural within these regions the rural quality of and their survival up to Romanian is with of services healthcare system and the treatment of pediatric cancer is However, to services and the about the health to be addressed of the of personnel and were among the to the survival outcomes of pediatric cancer population in Romania national pediatric cancer registry data that are and and to and coding system for rural-urban designation and development regions the study may be subject to such as potential of cancer cases that were in the registry, in adolescents treatment in adult care facilities and the pediatric population that care without the national pediatric oncology network. Still, not to the of cancer cases in the Romanian pediatric the results reflect the outcomes of the Romanian pediatric oncology care system (6). Also, study could have from a time and complete information which was not available in the potential in the standards of care among centers in the different regions of Romania may also a more in to and quality of care is a central focus of current in Romania, the National Cancer which an to pediatric cancers and is a new the national pediatric oncology network with a of increasing coverage with services of the national study for the time reported the and disparities in survival and mortality of the Romanian pediatric cancer population a national-level cancer at an a significant gap between Romania and other European countries, in in cancers that an in survival over the years such as CNS tumours, neuroblastoma and and regional differences may also to the pediatric cancer survival disparities between Romania and other EU at regional and national levels be to these disparities to the survival of patients with pediatric cancers in Romania and countries where the disparity study have significant health and the for to economic and resources for pediatric cancer rural and and in some at regional and national be to healthcare to establish healthcare services and healthcare in rural areas and economic development is also in the to coverage of the Romanian pediatric population by RNPOHR by and data sources and the clinical information capture by the Registry in to with the current in potential cases by the national-level cancer is for a more of the survival determinants and their in the outcomes of pediatric cancer in Romania.

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