Annals of Oncology Advance Access originally published online on July 28, 2007
Annals of Oncology 2007 18(9):1569-1577; doi:10.1093/annonc/mdm187
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© 2007 European Society for Medical Oncology
Up-to-date monitoring of childhood cancer long-term survival in Europe: leukaemias and lymphomas
1 Division of Clinical Epidemiology and Aging Research, German Cancer Research Center, Heidelberg, Germany
2 Department of Public Health, Erasmus University Medical Centre, Rotterdam, The Netherlands
3 Clinical Trial Service Unit and Epidemiological Studies Unit, University of Oxford, Oxford, United Kingdom
4 Basque Country Cancer Registry, Vitoria-Gasteiz, Spain
5 INSERM, Villejuif, France
6 Data Analysis and Interpretation Group, International Agency for Research on Cancer, Lyon, France
* Correspondence to: Dr Hermann Brenner, Division of Clinical Epidemiology and Aging Research, German Cancer Research Center, Bergheimer Strasse 20, D-69115 Heidelberg, Germany. Tel: +49-6221-548140; Fax: +49-6221-548142; E-mail: h.brenner{at}dkfz-heidelberg.de
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Abstract |
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Background: In recent decades, following the introduction of effective chemotherapy, the prognosis of children with leukaemia and lymphoma has dramatically improved, but data reflecting further possible improvement achieved in the 1990s are scarce.
Methods: Using the Automated Childhood Cancer Information (ACCIS) database, we carried out a period analysis of 10-year survival for the 1995–99 period. Analyses were carried out by diagnostic groups, age-group at diagnosis, sex and four European regions.
Results: Ten-year survival estimates for the 1995–99 period were 73% for any type of leukaemia, 78% for acute lymphoid leukaemia and 52% for acute non-lymphocytic leukaemia. The corresponding 10-year survival rates for all types of lymphomas, Hodgkin lymphoma, and non-Hodgkin lymphoma were 84, 91 and 79%, respectively. These figures are much higher than those obtained by traditional (cohort-based) methods of survival analysis. A large difference in prognosis is still observed between the East and other parts of Europe.
Conclusion: Major improvement in prognosis for children with leukaemia or lymphoma has been ongoing in Europe during the 1990s, but further monitoring and investments are required to remove the large regional differences between European regions.
Key words: cancer registries, childhood cancer, Europe, leukaemia, lymphoma, survival
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introduction |
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Leukaemias and lymphomas comprise about 43% of all forms of cancer among children less than 15 years of age in Europe [1]. Leukaemias alone account for more than 30% of all childhood cancer, including about 80% acute lymphoid leukaemia (ALL), and about 15% acute non-lymphocytic leukaemia (ANLL) cases [2].
Until the 1970s, a diagnosis of childhood leukaemia was tantamount to a sentence of death, as 5-year survival rates were well below 10% [3]. However, following the introduction of chemotherapy in the 1950s, and its refinement in later decades, prognosis greatly improved, particularly for children with ALL [4]. Up until the early 1990s, 5-year survival of children with ALL increased to more than 80% in some European regions, although much lower levels were attained in others [2, 5]. For ANLL, 5-year survival of children in Europe reached about 50% [2, 5].
Hodgkin lymphoma (HL) and non-Hodgkin lymphoma (NHL) each account for about 5% of all childhood cancers in Europe [1]. Survival of children with HL was already quite favourable in the 1970s, and has increased rather little since then. For example, in Britain, the 5-year survival rate increased from 52% for children diagnosed with HL in 1962–70 to 86% in 1971–85 [6], later exceeded 90%, and then the upward trend has slowed down [7]. In Europe, the 5-year survival in children with HL increased from 87 to 94% over the 1980s and early 1990s [5, 8, 9].
Survival of children with NHL has been poorer compared to HL, but steadily increased over the past decades in European countries following the introduction of intensive therapy protocols [10]. In Britain, 5-year survival was as low as 19% for children diagnosed with NHL in 1962–70, then it increased to 43% for children diagnosed in 1971–85, and within the 1980s, a further increase to more than 70% was observed [7]. In Europe overall, 5-year survival increased from around 50% to almost 80% in the 1980s and 1990s [5, 8, 10].
The results cited above pertain to children diagnosed 10 or more years ago and therefore do not reflect possible further improvements in prognosis in the meantime. Furthermore, few data have been published for follow-up periods longer than 5 years.
In this paper, we present up-to-date estimates of survival, using the period survival method. Ten-year survival of children diagnosed with leukaemias and lymphomas is reported for various European regions for the 1995–99 period. Using the same database, we also compare the period survival estimates with cohort-based survival estimates, as calculated in the majority of previously published studies of population-based survival. Our study is based on the large European database of childhood and adolescent cancer cases built within the Automated Childhood Cancer Information system (ACCIS) project [11].
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methods |
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Information on all cases of leukaemias and lymphomas in children less than 15 years was extracted from the ACCIS database, September 2003 edition. The methodology for this analysis has been described in detail in a preceding article [12]. Briefly, only cancer registries that had submitted data with close to or entirely complete follow-up for vital status throughout a time window from 1987 (or earlier) to 1997 (or later) were included. Leukaemia and lymphoma diagnostic groups were defined as in the International Classification of Childhood Cancer [13].
The selected registries are listed in Table 1, showing also the grouping of countries into regions: East, South, North and West. About half of the total 20 506 children with leukaemia or lymphoma were contributed by the German national childhood cancer registry, while the other half were contributed from 23 registries in 14 countries. Each of the four European regions was represented by at least three countries, more than 1000 leukaemia cases and about 500 or more lymphoma cases. In the Netherlands, national data were available for children with leukaemia, whereas there was only regional coverage for children with lymphoma. Children with lymphoma from Finland were included in analyses for all forms of lymphoma only, but not in analyses by lymphoma subtype, due to missing information on lymphoma subtype in 57% of cases.
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Period estimates of 10-year survival [14] were calculated for the 1995–99 period, exclusively reflecting the survival experience in 1995–99 of children diagnosed in 1985–99. To compare the 10-year period estimates with those obtained using the cohort-based methods [15], we also calculated the most recent estimates that might have been obtained by cohort analysis (pertaining to the survival experience in 1985–99 of children diagnosed in 1985–89 and followed-up for at least 10 years) or complete analysis (pertaining to the survival experience in 1985–99 of children diagnosed in 1985–99 and followed-up for up to 10 years).
The results are shown for overall leukaemia and lymphoma groups, selected diagnostic subgroups (ALL, ANLL, other leukaemias,; HL, NHL, other lymphomas), for patients of all ages combined, as well as for age groups (0, 1–4, 5–9, 10–14 years), according to sex and four European regions.
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Table 2 provides the numbers of children with leukaemia by diagnostic group, age group, sex and European region included in the analysis. Overall, 15 370 children with leukaemia were included. ALL accounted for more than 80% of all leukaemia cases, followed by ANLL with about 15% of cases. The diagnosis was made in the first year of life among 5% of patients, and before the 5th birthday in slightly more than half of the patients. The dataset included somewhat more boys than girls.
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Estimates of 10-year survival for all leukaemia patients, and by leukaemia subgroup, age group at diagnosis, sex and European region are also shown in Table 2. The overall 10-year period survival estimate for the 1995–99 period was 73%, markedly higher than the estimates obtained by traditional cohort analysis (63%) or complete analysis (68%).
Survival estimates were considerably higher for children with ALL than for children with ANLL. The differences between period, complete and cohort estimates were much larger for ANLL than for ALL. This observation suggests that particularly large improvements have been achieved in the 1990s for the group of ANLL patients. Prognosis was poorest for children with other forms of leukaemia, for which the highest 10-year survival estimate, obtained by the period method, was as low as 35% (5-year survival: 53%).
Prognosis was clearly worst for children who developed leukaemia in their first year of life. The best prognosis was observed for the age group 1–4 years, and prognosis gradually decreased in the higher age groups. Due to similar differences between the period and the cohort estimates for the individual age groups, it can be concluded that the improvement in the prognosis towards the end of the study period was similar across age groups.
Sex-specific differences in survival were smaller when period analysis was used, compared to the other methods. This suggests that the recent improvement was somewhat larger in boys, so that their survival disadvantage (evident from the sex-specific results obtained by cohort or complete method) has reduced partly, compared to girls.
A major improvement in the prognosis of children with leukaemias appears to have been ongoing in the 1990s in all European regions, as indicated by the higher estimates obtained with the 1995–99 period analysis compared with the cohort and complete survival estimates. This pattern was particularly pronounced in Eastern and Southern Europe, but a major gap in prognosis has persisted between children from Eastern Europe and other parts of Europe, even with the period method. In the 1995–99 period, 10 year survival was only about 60% in Eastern Europe, compared to about 75% in Western and Northern Europe, and about 70% in Southern Europe (5-year survival: 64, 80 and 75%, respectively).
Figure 1 shows survival curves for the ALL subgroup in the four European regions. Ten-year survival of around 80% has been achieved for children with ALL in all European regions except Eastern Europe, where it remained below 70% (5-year survival: 80–86 and 70%, respectively). If the favourable development, suggested by the marked difference between period, complete and cohort estimates, continues, further improvement may be expected in near future.
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The relative position of survival curves shown in Figure 2 suggests that the prognosis for children with ANLL has dramatically improved in Northern and Western Europe between the 1980s and the 1990s: the 10-year period survival estimates for the 1995–99 period were close to 60%; that is, respectively, 26 and 14% units higher than the corresponding cohort estimates for the children diagnosed in 1985–89. A dramatic increase is suggested also for Southern Europe, because the 10-year 1995–99 period survival estimate was 42%; much higher than the 10-year survival estimate of 26% for the 1985–89 cohort. Unfortunately, virtually no improvement can be inferred from the survival curves in Figure 2 in Eastern Europe, where 10-year survival rates remained very low and the inter-regional gap has reached more than 30% units compared to Northern and Western European countries according to the 1995–99 period estimates.
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Table 3 provides the numbers of children with lymphoma by diagnostic group, age group, sex and region. HL and NHL accounted for about 40 and 45% of lymphomas, respectively. Occurrence of lymphoma in the first year of life was rare (1.3%), and about half of the children were 10 years or older at the time of diagnosis. There were about twice as many male than female patients.
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Ten-year survival estimates for the 1995–99 period were 84% for children with any type of lymphoma, and 91, 79 and 83% for children with HL, NHL, and other lymphoma, respectively (Table 3). The corresponding 5-year survival estimates were 93, 80 and 84%, respectively. Except for HL, these figures are much higher than the corresponding figures obtained by cohort methods of survival analysis, which suggests ongoing major improvement in prognosis towards the end of the study period.
Among children diagnosed with lymphomas in 1985–89, 10-year survival differed enormously by age group, ranging from 20% among children under 1 year of age to about 82% among those aged 10–14 years (5-year survival: 20–84%). The difference between the period and cohort or complete estimates was largest for the youngest children. In consequence, the age difference in prognosis has strongly decreased, even though children below 1 year of age do still have the worst period survival estimates. However, the small number of children and the large standard error for the survival estimates for this group have to be kept in mind. Ten-year survival estimates were very similar for boys and girls, as were the differences between various survival estimates within each sex, suggesting similar improvement for girls and boys in the 1990s.
Among children diagnosed with lymphomas in 1985–89, a strong gradient in prognosis had been observed between various European regions, with the lowest survival observed in Eastern Europe and the highest in Western Europe. From the smaller difference between period survival region-specific estimates (compared to cohort or complete estimates) we conclude that the regional gradient has become smaller, but has not disappeared completely in the 1990s. Ten-year survival estimates for the 1995–99 period were 74, 77, 89 and 82% for children with any form of lymphoma from Eastern, Southern, Western and Northern Europe, respectively. Between 5 and 10 years after diagnosis, there were still deaths occurring, as seen in Figure 3 (5-year survival estimates were 78, 79, 89 and 84%, respectively).
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discussion |
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To our knowledge, this is the first international comparative analysis of survival of children with leukaemias and lymphomas using period analysis. Due to continued improvement, 10-year survival of around 80% has been achieved for children with ALL and almost 60% for those with ANLL in the North and West European regions with the best prognosis for the 1995–99 period. Despite improvements, 10-year survival was somewhat lower among children from the South, and markedly lower in the East.
We found respective period estimates of 10-year survival of 91, 79 and 83% for children with HL, NHL and other lymphomas in the 1995–99 period (all regions combined). The period survival estimates for children with NHL and other lymphomas were considerably higher than the cohort estimates for the children diagnosed in 1985–89. This difference between the two types of estimate indicates that major improvement in prognosis has been going on in the 1990s for children with these malignancies. The improvement was particularly pronounced for children from the East, for children with lymphomas other than HL and NHL, and for infants.
The period estimates of survival of children with leukaemias in Western and Northern European countries are in line with results of recent analyses from Germany and the United States [16, 17]. Our 1995–99 period estimates of 5-year survival are also higher than the 5-year cohort or complete survival estimates of children diagnosed in 1990–94, the most recently reported data from the EUROCARE study [5], which indicates further improvement in prognosis since the mid-1990s.
Our period estimate of 10-year survival for leukaemias (73%) is actually equal to the 5-year survival calculated by a cohort-based method for the patients diagnosed in 1988–97 in the ACCIS database in a previous study [2]. In our period analysis, 10-year survival estimates were on average about 5% units lower than 5-year survival estimates for children with ALL. Since survival probabilities for leukaemia continue to decline after 5 years of follow-up, as was shown in this and other studies [2, 18], the period estimates anticipate further improvement of prognosis. This emphasizes the importance of follow-up of children for long periods, in addition to the conventional 5-year follow-up, in comparative studies.
The period estimates obtained in our study are also considerably higher than the most up-to-date cohort and complete estimates that we derived from the same database. As discussed previously [19], this pattern suggests that further improvement in survival of children with leukaemia has occurred during the study period, and increasingly towards its end. Such improvements remain concealed when cohort-based methods of survival analysis are used. Differences between the different types of estimates (and the suggested favourable time trends) were seen for all age groups, both sexes, all diagnostic groups of leukaemias and all four European regions. However, for the European regions, the extent of these differences varied. For example, for ALL, the strongest effect was observed in the East, suggesting a fast improvement of the access to effective therapy in the most recent years. Despite this development though, survival of children with ALL in the East still lags behind that of children from other parts of Europe, indicating that investments in improvement of (access to) clinical care take a long time to show benefits.
By contrast, for children with ANLL, prognosis improved markedly over the study period in the North, West and South, but only modestly in the East. As a result, the gap between East and the rest of Europe has further increased for this form of leukaemia according to the period estimates for 1995–99. Again, major progress in therapy is the most likely explanation for the favourable trends in most of Europe [2].
The survival estimates obtained by the 1995–99 period analysis for children with HL are consistent with previous findings [8, 9]. The similarity of the survival estimates obtained by the various methods of survival analysis points to the maintenance (but not much further improvement) of the favourable prognosis achieved in previous decades. The focus of recent developments in therapy is on the minimisation of its potential late effects [20–22], such as secondary malignant neoplasms [23, 24]. Progress to this end cannot yet become visible in our 10-year survival estimates.
The 1995–99 10-year period survival estimates obtained in our study for children with NHL and other lymphomas are higher than the 5-year cohort survival estimates of 74% previously available for European children diagnosed up to 1994 [5, 8], and similar to the 5-year cohort estimate of 79% observed for children diagnosed in 1993–97 [10]. These findings, together with the higher 10-year period estimate, compared to the cohort and complete estimates obtained in our study, indicate that the previously reported steady improvement in prognosis in the 1970s and the 1980s [3, 6–8, 10, 18, 25] have continued in the 1990s [19]. This improvement, which seemed to be much stronger among children in the Northern and Eastern European countries than elsewhere, may reflect either further improvement in the availability of modern effective therapy, earlier diagnosis or changes in tumours’ classification [10], which could have resulted in including tumours with a more favourable prognosis in the later years in these two regions, as compared with the South and the West.
A particularly encouraging finding of our study is the apparent strong improvement of prognosis of infants with lymphoma, although further monitoring of this group of patients is required to confirm this result, due to the small number of patients diagnosed in this age group.
In the interpretation of our results, the following limitations should be kept in mind. Whereas data were included from 24 registries in 15 European countries, several European countries were not included, and some countries (Italy, France, Spain, Switzerland) were represented by regional data only. Reasons for exclusions were lack of cancer registration, lack of coverage of the time window from 1987 to 1997 required for this analysis, or failure to meet the quality criteria set up by the ACCIS Scientific Committee [26]. Thus, our data are not necessarily representative of Europe as a whole, although they provide a valuable estimate in the absence of more complete data availability. The region-specific results obtained in this study should be considered indicative of the differences existing within Europe, rather than exact characterization of distinct European areas, since the four regions were defined arbitrarily for this study, based on geographical location of the contributing registries. Nevertheless, we have no reasons to suppose that the persistent differences in survival of children with leukaemias and lymphomas between various parts of Europe are explained by selective inclusion of the populations covered, since the selection of registries and their allocation to the regions was based on a priori considerations and similar differences were observed for slightly different selection of registries in previous studies [5, 8, 18].
This international collaborative study was based on routine reporting by cancer registries. There is a potential of misclassification between HL and NHL, or between leukaemias and lymphomas, in addition to variations of practices between the registries. Such risks might lead to variable effects on estimated prognosis of patients with these neoplasms [27–29]. Our data did not include detailed prognostic indicators, obtained when patients are included in treatment protocols [30–32], so that we are only able to report prognosis for overall pooled groups of patients. Beside treatment protocols, the population-based survival estimates may also reflect, for example, ease and rapidity of access to diagnosis or well-designed referral systems. It would be desirable in the future to include prognostic factors in the data collection protocol, such as 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.
Although we were able to include data from more than 15 000 children with leukaemia and more than 5000 children with lymphoma in this European collaborative project, standard errors for survival estimates were quite large for some subgroups of patients. This stresses again the need for further expansion of this international database, both geographically and temporally. In most cases, standard errors were much smaller, however, than the very large differences in survival estimates seen between different regions, different subgroups or different types of analysis, which suggests that the major patterns seen in our results are unlikely to be explained by chance.
The period estimates for 1995–99 obtained in this study are the most up-to-date estimates of long-term survival in European children. However, they may still underestimate the long-term prognosis of children diagnosed with leukaemia or lymphoma in 1995–99 [19]. Together with wider application of the period method for up-to-date monitoring of survival of children with cancer, the faster availability of recent data from cancer registries is a priority.
This first application of period analysis in an international comparative study of survival of children with leukaemia or lymphoma, suggests further major improvement in long-term prognosis of children with leukaemia and NHL and stable development for those with HL in the 1990s in Europe. These findings are so far undetected in studies using cohort-based methods of survival analysis. This improvement most likely reflects improved access to effective therapy and, if this is so, further investments are required in the regions with lower survival, especially in the East, to ensure equity of the access to health care to all children across 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. Eva Steliarova-Foucher was partly supported by the Cancéropôle Lyon Auvergne Rhône Alpes and the Federal Ministry of Health of the Federal German Government. The authors are grateful to the following 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; and 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 Registry, Childhood Cancer Registry of Piedmont, Ragusa Cancer Registry and Tuscany Cancer Registry; Netherlands: The Netherlands Cancer Registry, Eindhoven Cancer Registry of Comprehensive Cancer Centre South and the Dutch Childhood Oncology Group, The Hague; 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.
Received for publication November 17, 2006. Revision received April 4, 2007. Accepted for publication April 11, 2007.
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