Annals of Oncology Advance Access originally published online on September 5, 2007
Annals of Oncology 2007 18(10):1722-1733; doi:10.1093/annonc/mdm189
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© 2007 European Society for Medical Oncology
pediatric malignancies |
Up-to-date monitoring of childhood cancer long-term survival in Europe: tumours of the sympathetic nervous system, retinoblastoma, renal and bone tumours, and soft tissue sarcomas
1 Division of Clinical Epidemiology and Aging Research, German Cancer Research Center, Heidelberg, Germany
2 French National Registry of Childhood Solid Tumours, Children's Hospital, Vandoeuvre, France
3 Data Analysis and Interpretation Group, International Agency for Research on Cancer, Lyon, France
4 German Childhood Cancer Registry, University of Johannes Gutenberg, Mainz, Germany
5 Croatian National Cancer Registry, Croatian National Institute of Public Health, Zagreb, Croatia
6 Childhood Cancer Registry of Piedmont, Cancer Epidemiology Unit of the Centre for Cancer Epidemiology and Prevention, CeRMS/FIRMS, Torino, Italy
7 Childhood Cancer Research Group, University of Oxford, UK
* Correspondence to: Dr V. Arndt, Division of Clinical Epidemiology and Aging Research, German Cancer Research Center, Bergheimer Strasse 20, D-69115 Heidelberg, Germany. Tel: +49-6221-548144; Fax: +49-6221-548142; E-mail: v.arndt{at}dkfz-heidelberg.de
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Abstract |
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Background: Prognosis for most types of childhood tumours has improved during the last few decades. In this article we estimate up-to-date period survival for less common, but important childhood malignancies in Europe.
Methods: Using the database of the Automated Childhood Cancer Information System we calculated period estimates of 10-year survival for the 1995–1999 period for children aged 0–14 years diagnosed during 1985–1999 with tumours of the sympathetic nervous system (NS), retinoblastoma, renal tumours, bone tumours and soft tissue sarcomas in four European regions.
Results: Ten-year period survival for 1995–1999 was 66% in children with tumours of the sympathetic NS, 96% for retinoblastoma, 87% for renal tumours, 58% for bone tumours and 61% for soft tissue sarcomas. The higher period estimates, as compared with cohort and complete estimates indicate recent improvement in survival for tumours of the sympathetic NS and to a lesser extent for retinoblastoma and renal tumours. Region-specific period survival estimates were lowest for Eastern Europe for renal, bone and soft tissue tumours, but not for the other two tumour groups.
Conclusion: There have been further improvements in the 1990s in long-term survival of children diagnosed with several malignancies, albeit to a different extent in different European regions.
Key words: cancer registries, childhood cancer, Europe, population-based, prognosis, survival, neuroblastoma, retinoblastoma, Wilms' tumour, bone tumours, soft tissue sarcomas
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introduction |
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Prognosis for almost all types of childhood tumours improved impressively during the last few decades [1], but there have been concerns that, with the exception of leukaemia and lymphoma, a plateau with no further improvement has been reached for most types of childhood cancer since the early 1990s [2]. In preceding articles of this series [3–5], we were able to demonstrate further improvements in prognosis during the 1990s for all forms of childhood cancer, as well as leukaemia, lymphoma and CNS tumours by applying the so-called period analysis [6] on data from the Automatic Childhood Cancer Information System (ACCIS) [1]. The period analysis is a new statistical method that is able to depict recent trends in survival in a more timely way than traditional cohort-based approaches [7].
In this paper, we examine the recent development in prognosis for children from four European regions diagnosed with less common, but important malignant tumours, namely tumours of the sympathetic nervous system, retinoblastoma, renal and bone tumours, and soft-tissue sarcoma. Altogether, these five entities account for approximately 25–30% of all childhood tumours, with retinoblastoma somewhat less frequent (2–4%) than the other groups (each around 6–8%).
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methods |
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The methodology for this analysis has been described in detail in a preceding article in this volume of the journal [3]. Briefly, the analysis is based on the database of the Automated Childhood Cancer Information System (ACCIS), September 2003 edition [1]. We included children aged 0–14 years with a first diagnosis of several tumour types during the years 1985–1999 in the participating registries. The tumours were classified and are presented according to the International Classification of Childhood Cancer (ICCC) [8]. The analyses were conducted for tumours of the sympathetic nervous system (Group IV of ICCC including neuroblastoma), retinoblastoma (ICCC Group V), renal tumours (ICCC Group VI including Wilms' tumour), bone tumours (ICCC Group VIII) and soft-tissue sarcomas (ICCC Group IX).
The criteria for selection of the registries in this analysis were:
- (i) availability and high completeness of follow-up with respect to vital status throughout a time window from at least 1987 to 1997 or later;
- (ii) fulfilment of high standards of quality and comparability of the ACCIS data [9].
- (ii) fulfilment of high standards of quality and comparability of the ACCIS data [9].
Data from the contributing cancer registries were grouped into four European regions as follows:
- (i) East: Estonia, Hungary, Slovakia
- (ii) South: Italy, Slovenia, Spain
- (iii) West: France, Germany, Netherlands, Switzerland, United Kingdom
- (iv) North: Denmark, Finland, Iceland, Norway
- (ii) South: Italy, Slovenia, Spain
Period estimates of 10-year survival for the 1995–1999 period (exclusively reflecting the survival experience in 1995–1999 of children diagnosed in 1985–1999) were estimated according to the method developed by Brenner and Gefeller [6]. The most recent estimates that might have been obtained by traditional cohort analysis (pertaining to children diagnosed in 1985–1989 and followed for full 10 years) or complete analysis (pertaining to the survival experience in 1985–1999 of children diagnosed in 1985–1999 and followed for up to 10 years) [10] are given for comparison and to assess recent development in prognosis. We also report 5-year survival estimates for selected groups of patients in order to enhance comparability with other published data.
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Overall, 11 750 children with one of the selected types of cancer were included in the analysis (Table 1). Over 65% of all cases were reported by registries from Western Europe, whereas registries from the other European regions contributed 8–14% of all cases. The German childhood cancer registry provided data for over 50% of all cases. Table 1 also shows the numbers of cases included in the analysis by ICCC tumour groups. There have been 3349 tumours of the sympathetic nervous system; 98% of them were (ganglio)neuroblastoma (ICCC IVa, n = 3284). Retinoblastoma accounted for 1027 cases. The vast majority (97%) of the 2565 renal tumours were Wilms' tumours (ICCC VIa, n = 2493). The most common subgroups among the bone tumours were osteosarcoma (ICCC VIIIa, 50%) and Ewing's sarcoma of bone (ICCC VIIIc, 43%). The predominant subgroup among soft-tissue tumours was rhabdomyo-sarcoma and embryonal sarcoma (ICCC IXa, 56%).
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Table 2 provides 10-year survival estimates derived by cohort, complete, and period analysis for all four European regions combined for the specific tumour types addressed in this study.
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The 10-year period survival for children with sympathetic nervous system was almost 66% (5-year period survival: 68%, data not tabulated). In comparison with the 52% 10-year cohort survival for children diagnosed in 1985–1989, this result indicates a substantial improvement during the 1990s. The comparison of the period estimate with complete estimate (59%) shows further improvement, even if less spectacular, for the patients diagnosed towards the end of the diagnostic period of 1985–1999.
Children with retinoblastoma showed the best survival of all groups of tumours considered in this analysis during the entire study period. Ten-year cohort survival for all children diagnosed in 1985–1989 was 92%. This very good prognosis even further improved throughout the 1990s as indicated by the 10-year complete estimate of 94% and the period estimate of 96%. The corresponding 5-year survival estimates were 93, 95 and 96% (data not tabulated).
Also children with a renal tumour experienced a good prognosis, with 10-year cohort survival of 81% for those diagnosed in the years 1985–1989. The corresponding period estimate of 87% for 1995–1999 period indicates that 10-year survival has further increased for children with this type of tumour during the 1990s (5-year period survival: 88%, data not tabulated).
Prognosis of children with bone tumours was less favourable and did not seem to improve much. The 10-year cohort survival for the patients diagnosed in 1985–1989 was 55%. The complete and period estimates were only slightly higher (58% each), which does not imply much improvement over the 1990s. The corresponding 5-year survival estimates were around 5% units higher (cohort: 60%; complete: 63%; period: 63%). The subgroup of patients with Ewing's bone tumours had lowest survival among other bone-tumour subgroups, although a slight continuous improvement can be inferred from the comparison of the three survival estimates (cohort: 51%; complete: 55%, period: 55%). The corresponding 5-year survival estimates were 6–7% units higher (cohort: 57%; complete: 61%; period: 62%). Survival with osteosarcoma was slightly higher, but there was no indication of a recent improvement, since the 10-year cohort (57%), complete (60%) and period (58%) survival estimates were almost identical (5-year survival: 57, 60 and 58%, respectively).
Prognosis for children with soft-tissue sarcoma was somewhat better than for those with bone tumours, but this does not seem to have changed during the 1990s as cohort, complete and period analysis yielded almost identical 10-year survival estimates of around 60% (5-year survival: 65, 66 and 66%, respectively). The children with most common soft tissue tumour, rhabdomyosarcoma, actually fared worse than those with other soft tissue tumours.
The results of the region specific analysis, which we have restricted to the major ICCC categories, are shown in Table 3 and in Figures 1–5
. Period survival of children with tumours of the sympathetic nervous system was higher in Western Europe than in all other regions. The difference between the period and cohort, or complete estimates was greatest for Eastern Europe, suggesting strongest improvement in survival, whereby the rank for this region changed from 4 to 2 across the three estimates. The period estimate was very similar for Eastern, Northern and Southern Europe. Figure 1 also shows that the risk of death is highest in the first 3–4 years following diagnosis, after this period cumulative survival decreases less steeply.
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An absolute 10-year survival of 100% was estimated by the period method for children with retinoblastoma in Western Europe (Table 3, Figure 2). The corresponding estimates for other regions varied from 85% (South) to 98% (North). Comparison of the three survival estimates shows the most marked improvement of prognosis for children in the East, and mild improvement in the West and North. In South there was no evidence of change and the data suggest that survival perspectives of children with retinoblastoma may have decreased in this region in recent years. However, this pattern has to be interpreted with caution as the standard errors referring to those 76 children from Southern Europe are quite large. The improvement observed in the Eastern Europe resulted in similar survival in this and the other regions, with the period estimate for 10-year survival of 92% for the years 1995–1999. The cohort estimate of 76% for the East was very low compared with the other three regions.
Ten-year period survival of children diagnosed with renal tumours varied between 79% in the East and 90% in the North (Table 3). All region-specific period estimates were higher than those obtained by complete method for the same diagnostic period, which in turn were higher than the respective cohort estimates for the patients diagnosed in 1985–1989 (Figure 3). The prognosis of children with renal tumours thus improved during the 1990s in all European regions. Survival was lowest for children from Eastern Europe, but the gap between Eastern Europe and other European regions became smaller among the most recent estimates by period method. The survival curves flattened after the fifth year indicating that most deaths related to renal tumours occur during the first years after diagnosis.
The 10-year period survival for children diagnosed with malignant bone tumours was poor, particularly for children from Eastern Europe, with less than 50% survival (Table 3, Figure 4). From comparison of the three survival estimates for each region we conclude that the prognosis has improved in three regions (except North), with greatest progress in the South, followed by the East. This development reduced the range of the inter-regional differences from 21 percentage points for the cohort estimate to 17 percentage points in the most recent, period estimates.
The largest regional variation in period survival was observed for children with soft-tissue sarcoma: between 42% for Eastern Europe and 69% for Northern Europe (Table 3). The only region with some improvement as testified by the increasing values of cohort, complete and period estimates, was Western Europe (Figure 5). The corresponding estimates for Eastern Europe showed decreasing trend. The region specific pattern was similar when we restricted the analysis to rhabdomyosarcoma (data not shown).
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discussion |
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This study is the final part of the first analysis of childhood cancer survival using the period methodology to obtain up-to-date long-term survival estimates on European level. The comparison of period estimates with pertinent survival estimates derived by the conventional cohort or complete methods from the same data base has been shown to advance the detection of trends in survival in case of both, adult [7] and childhood cancer [11]. Our analysis indicates that there have been impressive improvements in the prognosis of tumours of the sympathetic nervous system and moderate improvements in case of retinoblastoma, renal tumours, bone tumours (except osteosarcoma) and some soft tissue sarcomas (excluding rhabdomyosarcoma) throughout the 1990s.
Neuroblastoma, which represents the major proportion of tumours of the sympathetic nervous system, is the most common solid tumour among infants (children under 1 year of age) [1,12]. The development of neuroblastoma is not invariably progressive; spontaneous regression without treatment has been reported [13] and the majority of neonates with neuroblastoma do well with no intervention [14]. Although survival has improved to some degree, the prognosis remained unsatisfactory until the early 1990s [15, 16]. Children diagnosed in the late 1980s in Europe still had a 5-year survival rate of less than 50% [17, 18]. Regional differences within Europe in incidence, age and distribution of stage of disease at time of diagnosis [19, 20], as well as regional variation in survival of children with neuroblastoma [20–22] have been described. For example, 5-year survival rates of over 60% have been reported for Germany already prior to the start of the neuroblastoma screening project [23]. These differences may reflect different paediatric health-care systems including the practice of routine health checks for children, but also differences in availability and access to efficient diagnostics and therapy.
Our data indicate an impressive improvement in prognosis for children with neuroblastoma in all European regions during the 1990s. This finding is complementary to the results of other European studies of population-based survival using the cohort method, such as the recent ACCIS report on incidence and survival of children with neuroblastoma in Europe diagnosed in 1978–1997 [24]. The favourable development is correlated with a similar increase in incidence, particularly in infant cases in all regions except in Northern Europe. Some of the increase in incidence must be ascribed to the ‘over-diagnosis’ of cases with a favourable prognosis even without treatment. In particular, the increase in survival for children from Western Europe diagnosed with neuroblastoma might be attributed to the temporary implementation of the large-scale screening trial in Germany, which contributed over 50% of all neuroblastoma cases in this region, whereas the impact of the small-area screening trials in France and England is considered to be negligible [24]. In addition to the effects of over-diagnosis, some of the increase in survival may also be attributed to improvements in the quality of the therapy. The assessment of this would require data by stage, which are currently not available in the ACCIS database.
Retinoblastoma is one of the embryonal neoplasms characterized by young age at onset and very high survival in comparison with other tumours, if diagnosed on time [25]. Survival further improved during the past three decades in many European countries [18, 25–30], Japan [16] and in North America [31]. Survival rates of 100% have been reported from several registries [21, 26, 30, 32]. Retinoblastoma is considered nowadays as a curable tumour, but this strictly depends on early diagnosis, minimal extension of the tumour at diagnosis and the access to optimal treatment. High survival for retinoblastoma is probably related to the implementation of chemotherapy as adjuvant therapy in addition to surgical enucleation [25]. While 5-year survival in the range of 90–100% has already been achieved for children diagnosed in the late 1980s in most parts of Europe, survival was slightly lower, around 85%, for children from Eastern Europe [25]. Our data confirmed further improvement of survival in the East during the 1990s, to the levels equivalent with other regions. With achieving very high survival the potential for further improvement becomes limited, although careful monitoring of survival trends should continue in order to detect any unfavourable development, such as that seen in Southern Europe in this study. Further data collection will help to draw firm conclusion from this observation.
Wilms' tumour is by far the most common malignant renal tumour in children, primarily seen in children 1–5 years of age [33]. Wilms' tumour was the first solid tumour for which the adjuvant use of chemotherapy along with radiation was shown to enhance survival [14, 34, 35]. This led to an increase in 5-year survival from 30 to 40% during the 1970s, up to 80–90% during the 1980s and 1990s [18, 33, 36]. As nowadays most patients with Wilms' tumour in Europe and North America can be cured, studies over the last decade have focused on trying to minimize long-term toxicity of chemotherapy and radiation while maintaining the high cure rate for children with Wilms' tumour [14]. Complementary to the results of a recent ACCIS report on incidence and survival of renal tumours [33], our data indicate that the excellent survival rates have been maintained and were further enhanced in Europe.
Malignancies of the bone occur predominantly during late childhood and adolescence [37]. In the past, survival rates for osteosarcoma were higher than those for Ewing's sarcoma, but during the last two decades the difference in prognosis between these two tumours diminished [21, 37]. There have been substantial improvements during the past 40 years in prognosis for children with bone tumours. For example, 5-year survival in the United Kingdom for children with malignant bone tumours increased from 22% in the 1960s [38] up to 64% for children diagnosed in the 1980s [35]. Similar figures have been reported from Italy [26, 30], the United States [31], New Zealand [32] and from a recent European analysis of childhood cancer data from the ACCIS project [18, 37].
Soft tissue sarcomas which account for 7% of all childhood tumours are a heterogeneous group of malignancies primarily of mesenchymal cell origin that develop at primary sites throughout the body [39]. The introduction of multimodal therapy [40] and the identification of different biological subtypes [41] have improved the prognosis, but the outcome is strongly influenced by how completely the primary tumour can be surgically removed [14]. Our period estimate indicates that currently around 60% of all children with soft tissue sarcoma in Europe can expect to survive 10 years or more. However, this is not higher than the 10-year estimate obtained by cohort method, implying not much improvement in survival during the 1990s. In the latest report of European data, the 5-year survival of children diagnosed in 1988–1997 with soft tissue sarcomas was 65% [39]. The region with strongest indication of improvement was Western Europe, while the tendency to deterioration of previously observed survival, seen in Eastern Europe, should be carefully watched.
Although it is not the primary goal of our study to address regional differences, our study did confirm variability in survival across Europe reported previously [2, 22, 24, 25, 33, 37, 39, 42]. Unlike the previous studies, our period survival method has permitted to report for the first time expected equalisation of childhood survival in Eastern Europe with the other regions, for tumours of sympathetic nervous system and retinoblastoma. The gap was also diminishing for renal tumours and malignant bone tumours, although to a much lesser extent. On the other hand, period estimates of region-specific survival indicate increased lagging of the East behind the rest of Europe for soft tissue sarcomas. Differences in access to quality health care are likely to contribute to the still existing poor outcome in this region. Regional differences in childhood cancer survival within Europe have been described in general terms elsewhere [22, 42].
There are some limitations that should be addressed when interreting the results of our study. In particular, the increase in infant incidence of neuroblastoma as a consequence of the temporary introduction of large-scale neuroblastoma screening programmes or generally improved healthcare for infants due to the wide use of ultrasound-imaging in some, but not all European countries during the study period might have artificially increased the corresponding survival estimates. Hence, the apparent increases in survival for this tumour might reflect a certain degree of over-diagnosis, as well as increased chances of cure. This development would apply to several regions, including East, South and West as defined in the earlier study, where the incidence of neuroblastoma in infants doubled between 1978–82 and 1993–97 [20]. The second shortcoming is the incomplete coverage of Europe, comprising only the populations covered by good quality population-based data and satisfying defined criteria of follow-up. In addition, we have defined the regions according to data availability. As a result, some of the region-specific survival estimates may not be representative of other definition of regions than that used in this study. Also, the results are strongly influenced by the pattern in the largest registries and notably the national childhood cancer registry of Germany, which provided almost half of all cases for this analysis. The interpretation is also limited due to lack of information regarding treatment protocol and tumour stage, which has not been included in the ACCIS database [1]. Beside treatment protocols, the population-based survival estimates may also reflect, for example, ease and rapidity of access to diagnosis or well designed referral system. It would be desirable in the future to include prognostic factors in the data collection protocol, such as access delay between diagnosis and treatment, inclusion in clinical trials, stage at diagnosis and possibly the initial treatment even though this information may be difficult to obtain systematically in a population-based cancer registry.
Despite these limitations, we are confident that our analysis provides valuable information as the most up-to date and presumably most accurate survival estimates for children in Europe diagnosed with selected tumour types and it indicates that there has been ongoing progress in provision of effective treatment, particularly in Eastern Europe.
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This project was funded by the European Commission from the Europe Against Cancer programme (contract SPC.2002303), jointly with the International Agency for Research on Cancer. ESF was partly supported by the Cancéropôle Lyon Auvergne Rhône Alpes and the Federal Ministry of Health of the Federal German Government. The Childhood Cancer Research Group receives funding from the Department of Health and the Scottish Ministers. The views expressed in this publication are those of the authors and not necessarily those of the Department of Health and the Scottish Ministers. The authors are grateful to the following cancer registries participating in ACCIS for their contribution to this study:
- Denmark: Danish Cancer Society
- Estonia: Estonian Cancer Registry
- Finland: Finnish Cancer Registry
- France: Childhood Cancer Registry of Lorraine; Association of Childhood Cancer Registries of the Rhone-Alps Region
- Germany: German Childhood Cancer Registry
- Hungary: Hungarian Paediatric Cancer Registry
- Iceland: Icelandic Cancer Registry
- Italy: Cancer Registry of Latina Province; Lombardy Cancer Register; Childhood Cancer Registry of Piedmont; Ragusa Cancer Registry; Tuscany Cancer Registry
- Netherlands: Eindhoven Cancer Registry of Comprehensive Cancer Centre South
- Norway: Cancer Registry of Norway
- Slovakia: National Cancer Registry of Slovakia
- Slovenia: Cancer Registry of Slovenia
- Spain: Asturias Cancer Registry; Granada Cancer Registry; Tarragona Cancer Registry
- Switzerland: Basel Cancer Registry; Geneva Cancer Registry
- United Kingdom: Scottish Cancer Registry
- Estonia: Estonian Cancer Registry
Received for publication November 17, 2006. Revision received April 4, 2007. Accepted for publication April 11, 2007.
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