Abstract
Purpose
Acute lymphoblastic leukemia (ALL) is a rare hematological malignancy. With the recent introduction of a classification system for hematopoietic and lymphoid neoplasms, more comprehensive assessment of ALL epidemiology is now possible. In this study, we describe recent international incidence of ALL and project the annual number of diagnoses to 2025. We also estimate relative survival and average potential years of life lost (AYLL) to assess the societal burden of ALL.
Methods
Age-specific incidence data for ALL from select cancer registries in different geographies were obtained from the International Agency for Research on Cancer’s Cancer Incidence in Five Continents Database. Country-specific age-standardized rates were calculated to allow for direct comparisons between countries. ALL-specific mortality and relative survival data were only available from the United States (US) National Cancer Institute’s Surveillance, Epidemiology, and End Results program; mortality rates were estimated for other countries.
Results
The age-standardized incidence rate of ALL during 2003–2007 ranged from 1.08 to 2.12 per 100,000 person-years in selected countries. Incidence was generally higher in the Americas and Oceania and lower in Asia and Eastern Europe. In most countries, the incidence rate of ALL in children was approximately four times that in adults. Survival was particularly poor among adults. In selected countries, the estimated AYLL ranged from 30 to 48 years for all ages and from 23 to 39 years for adults.
Conclusions
Although a rare disease, ALL presents a significant public health burden given poor survival outcomes among adults, AYLL, and its importance as the most common pediatric cancer.
Similar content being viewed by others
References
Wartenberg D, Groves FD, Adelman AS (2008) Acute lymphoblastic leukemia: epidemiology and etiology. In: Estey EH, Faderl S, Kantarjian H (eds) Acute leukemias, 1st edn. Springer, Berlin, pp 77–93
Groves FD, Linet MS, Devesa SS (1995) Patterns of occurrence of the leukaemias. Eur J Cancer 31a:941–949
Hunger SP, Lu X, Devidas M, Camitta BM, Gaynon PS, Winick NJ et al (2012) Improved survival for children and adolescents with acute lymphoblastic leukemia between 1990 and 2005: a report from the children’s oncology group. J Clin Oncol 30:1663–1669. doi:10.1200/jco.2011.37.8018
Pui CH, Campana D, Pei D, Bowman WP, Sandlund JT, Kaste SC et al (2009) Treating childhood acute lymphoblastic leukemia without cranial irradiation. N Engl J Med 360:2730–2741. doi:10.1056/NEJMoa0900386
Rowe JM, Buck G, Burnett AK, Chopra R, Wiernik PH, Richards SM et al (2005) Induction therapy for adults with acute lymphoblastic leukemia: results of more than 1500 patients from the international ALL trial: MRC UKALL XII/ECOG E2993. Blood 106:3760–3767. doi:10.1182/blood-2005-04-1623
Huguet F, Leguay T, Raffoux E, Thomas X, Beldjord K, Delabesse E et al (2009) Pediatric-inspired therapy in adults with Philadelphia chromosome-negative acute lymphoblastic leukemia: the GRAALL-2003 study. J Clin Oncol 27:911–918. doi:10.1200/jco.2008.18.6916
Sive JI, Buck G, Fielding A, Lazarus HM, Litzow MR, Luger S et al (2012) Outcomes in older adults with acute lymphoblastic leukaemia (ALL): results from the international MRC UKALL XII/ECOG2993 trial. Br J Haematol 157:463–471. doi:10.1111/j.1365-2141.2012.09095.x
Thomas DA, O’Brien S, Faderl S, Garcia-Manero G, Ferrajoli A, Wierda W et al (2010) Chemoimmunotherapy with a modified hyper-CVAD and rituximab regimen improves outcome in de novo Philadelphia chromosome-negative precursor B-lineage acute lymphoblastic leukemia. J Clin Oncol 28:3880–3889. doi:10.1200/jco.2009.26.9456
Oriol A, Vives S, Hernandez-Rivas JM, Tormo M, Heras I, Rivas C et al (2010) Outcome after relapse of acute lymphoblastic leukemia in adult patients included in four consecutive risk-adapted trials by the PETHEMA Study Group. Haematologica 95:589–596. doi:10.3324/haematol.2009.014274
Fielding AK, Richards SM, Chopra R, Lazarus HM, Litzow MR, Buck G et al (2007) Outcome of 609 adults after relapse of acute lymphoblastic leukemia (ALL); an MRC UKALL12/ECOG 2993 study. Blood 109:944–950. doi:10.1182/blood-2006-05-018192
Gökbuget N, Stanze D, Beck J, Diedrich H, Horst HA, Huttmann A et al (2012) Outcome of relapsed adult lymphoblastic leukemia depends on response to salvage chemotherapy, prognostic factors, and performance of stem cell transplantation. Blood 120:2032–2041. doi:10.1182/blood-2011-12-399287
Campo E, Swerdlow SH, Harris NL, Pileri S, Stein H, Jaffe ES (2011) The 2008 WHO classification of lymphoid neoplasms and beyond: evolving concepts and practical applications. Blood 117:5019–5032. doi:10.1182/blood-2011-01-293050
American Cancer Society (2011) Global cancer facts and figures, 2nd edn. American Cancer Society, Atlanta
Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127:2893–2917. doi:10.1002/ijc.25516
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69–90. doi:10.3322/caac.20107
Dores GM, Devesa SS, Curtis RE, Linet MS, Morton LM (2012) Acute leukemia incidence and patient survival among children and adults in the United States, 2001–2007. Blood 119:34–43. doi:10.1182/blood-2011-04-347872
Dalmasso P, Pastore G, Zuccolo L, Maule MM, Pearce N, Merletti F et al (2005) Temporal trends in the incidence of childhood leukemia, lymphomas and solid tumors in north-west Italy, 1967–2001. A report of the Childhood Cancer Registry of Piedmont. Haematologica 90:1197–1204
Linabery AM, Ross JA (2008) Trends in childhood cancer incidence in the U.S. (1992–2004). Cancer 112:416–432. doi:10.1002/cncr.23169
Parkin DM, Stiller CA, Draper GJ, Bieber CA (1988) The international incidence of childhood cancer. Int J Cancer 42:511–520
Yamamoto JF, Goodman MT (2008) Patterns of leukemia incidence in the United States by subtype and demographic characteristics, 1997–2002. Cancer Causes Control 19:379–390. doi:10.1007/s10552-007-9097-2
Chihara D, Ito H, Matsuda T, Shibata A, Katsumi A, Nakamura S et al (2014) Differences in incidence and trends of haematological malignancies in Japan and the United States. Br J Haematol 164:536–545. doi:10.1111/bjh.12659
Marcos-Gragera R, Allemani C, Tereanu C, De Angelis R, Capocaccia R, Maynadie M et al (2011) Survival of European patients diagnosed with lymphoid neoplasms in 2000–2002: results of the HAEMACARE project. Haematologica 96:720–728. doi:10.3324/haematol.2010.034264
Sant M, Allemani C, Tereanu C, De Angelis R, Capocaccia R, Visser O et al (2010) Incidence of hematologic malignancies in Europe by morphologic subtype: results of the HAEMACARE project. Blood 116:3724–3734. doi:10.1182/blood-2010-05-282632
De Angelis R, Sant M, Coleman MP, Francisci S, Baili P, Pierannunzio D et al (2014) Cancer survival in Europe 1999–2007 by country and age: results of EUROCARE-5—a population-based study. Lancet Oncol 15:23–34. doi:10.1016/s1470-2045(13)70546-1
Gatta G, Botta L, Rossi S, Aareleid T, Bielska-Lasota M, Clavel J et al (2014) Childhood cancer survival in Europe 1999–2007: results of EUROCARE-5—a population-based study. Lancet Oncol 15:35–47. doi:10.1016/s1470-2045(13)70548-5
Svendsen AL, Feychting M, Klaeboe L, Langmark F, Schuz J (2007) Time trends in the incidence of acute lymphoblastic leukemia among children 1976–2002: a population-based Nordic study. J Pediatr 151:548–550. doi:10.1016/j.jpeds.2007.07.006
Coebergh JW, Reedijk AM, de Vries E, Martos C, Jakab Z, Steliarova-Foucher E et al (2006) Leukaemia incidence and survival in children and adolescents in Europe during 1978–1997. Report from the Automated Childhood Cancer Information System project. Eur J Cancer 42:2019–2036. doi:10.1016/j.ejca.2006.06.005
Fajardo-Gutierrez A, Juarez-Ocana S, Gonzalez-Miranda G, Palma-Padilla V, Carreon-Cruz R, Ortega-Alvarez MC et al (2007) Incidence of cancer in children residing in ten jurisdictions of the Mexican Republic: importance of the Cancer registry (a population-based study). BMC Cancer 7:68. doi:10.1186/1471-2407-7-68
Redaelli A, Laskin BL, Stephens JM, Botteman MF, Pashos CL (2005) A systematic literature review of the clinical and epidemiological burden of acute lymphoblastic leukaemia (ALL). Eur J Cancer Care (Engl) 14:53–62. doi:10.1111/j.1365-2354.2005.00513.x
Forman D, Bray F, Brewster DH, Gombe Mbalawa C, Kholer B, Piñeros M et al (2013) Cancer Incidence in Five Continents Volume X (IARC Scientific Publications No. 164). Lyon, IARC
Ahmad OB, Boschi-Pinto C, López AD, Murray CJLLR, Inoue M (2001) Age standardization of rates: a new WHO standard. World Health Organization, Geneva
United Nations, Department of Economic and Social Affairs, Population Division (2013) World Population Prospects: The 2012 Revision. http://esa.un.org/wpp/unpp/panel_indicators.htm. Accessed Feb 21, 2014
Chiaretti S, Vitale A, Cazzaniga G, Orlando SM, Silvestri D, Fazi P et al (2013) Clinico-biological features of 5202 patients with acute lymphoblastic leukemia enrolled in the Italian AIEOP and GIMEMA protocols and stratified in age cohorts. Haematologica 98:1702–1710. doi:10.3324/haematol.2012.080432
Toft N, Schmiegelow K, Klausen TW, Birgens H (2012) Adult acute lymphoblastic leukaemia in Denmark. A national population-based retrospective study on acute lymphoblastic leukaemia in Denmark 1998–2008. Br J Haematol 157:97–104. doi:10.1111/j.1365-2141.2011.09020.x
Li X, Li J, Hu Y, Xie W, Du W, Liu W et al (2012) A comprehensive cytogenetic classification of 1466 Chinese patients with de novo acute lymphoblastic leukemia. Leuk Res 36:720–726. doi:10.1016/j.leukres.2011.12.016
Chen B, Wang YY, Shen Y, Zhang WN, He HY, Zhu YM et al (2012) Newly diagnosed acute lymphoblastic leukemia in China (I): abnormal genetic patterns in 1346 childhood and adult cases and their comparison with the reports from Western countries. Leukemia 26:1608–1616. doi:10.1038/leu.2012.26
Dugas M, Messerer D, Hasford J, Haferlach T, Heinze B, Ludwig W et al (2003) German multicenter study group for adult ALL (GMALL): recruitment in comparison to ALL incidence and its impact on study results. Ann Hematol 82:83–87. doi:10.1007/s00277-002-0585-x
Moorman AV, Harrison CJ, Buck GA, Richards SM, Secker-Walker LM, Martineau M et al (2007) Karyotype is an independent prognostic factor in adult acute lymphoblastic leukemia (ALL): analysis of cytogenetic data from patients treated on the Medical Research Council (MRC) UKALLXII/Eastern Cooperative Oncology Group (ECOG) 2993 trial. Blood 109:3189–3197. doi:10.1182/blood-2006-10-051912
Tavernier E, Boiron JM, Huguet F, Bradstock K, Vey N, Kovacsovics T et al (2007) Outcome of treatment after first relapse in adults with acute lymphoblastic leukemia initially treated by the LALA-94 trial. Leukemia 21:1907–1914. doi:10.1038/sj.leu.2404824
Kantarjian H, Thomas D, O’Brien S, Cortes J, Giles F, Jeha S et al (2004) Long-term follow-up results of hyperfractionated cyclophosphamide, vincristine, doxorubicin, and dexamethasone (Hyper-CVAD), a dose-intensive regimen, in adult acute lymphocytic leukemia. Cancer 101:2788–2801. doi:10.1002/cncr.20668
Surveillance, Epidemiology, and End Results (SEER) Program (www.seer.cancer.gov) SEER*Stat Database: Incidence—SEER 18 Regs Research Data + Hurrican Katrina Impacted louisiana Cases, Nov 2013 Sub (1973–2011 varying)—Linked to County Attributes—Total U.S., 1969–2012 Counties, National Cancer Instisute, DCCPS, Surveillance Research Program, Surveillance Systems Branch, released April 2014 (updated 5/7/2017), based on the November 2013 submission
Surveillance, Epidemiology, and End Results (SEER) Program (www.seer.cancer.gov) SEER*Stat Database: Mortality—All COD, Aggregated With State, Total U.S. (1969–2010) <Katrina/Rita Population Adjustment>, National Cancer Instisute, DCCPS, Surveillance Research Program, Surveillance Systems Branch, released April 2013. Underlying mortality data provided by NCHS (www.cdc.gov/nchs)
World Health Organization (2013) Global Health Observatory Data Repository. http://apps.who.int/ghodata/. Accessed May 19, 2014
Burnet NG, Jefferies SJ, Benson RJ, Hunt DP, Treasure FP (2005) Years of life lost (YLL) from cancer is an important measure of population burden—and should be considered when allocating research funds. Br J Cancer 92:241–245. doi:10.1038/sj.bjc.6602321
Office for National Statistics (2015) Causes of Death. http://www.ons.gov.uk/ons/taxonomy/index.html?nscl=Causes+of+Death#tab-data-tables. Accessed Jan 8, 2015
NHS National Services Scotland, Information Services Division (2015) Data tables: cancer mortality by year. http://www.isdscotland.org/Health-Topics/Cancer/Publications/data-tables.asp?id=1314#1314. Accessed Jan 8, 2015
Instituto Nacional de Estadística (2015) Health: Deaths statistic according to cause of death. http://www.ine.es/jaxi/menu.do?type=pcaxis&path=%2Ft15%2Fp417&file=inebase&L=1. Accessed Jan 8, 2015
Australian Institute of Health and Welfare (AIHW) (2014) Australian Cancer Incidence and Mortality (ACIM) books: acute lymphoblastic leukemia. AIHW, Canberra. http://www.aihw.gov.au/acim-books. Accessed Jan 8, 2015
Ehngholm G, Ferlay J, Christensen N, Kejs AMT, Johannesen TB, Khan S, et al (2014) NORDCAN: Cancer incidence, mortality, prevalence and survival in the Nordic countries, version 7.0. Association of the Nordic Cancer Registries. Danish Cancer Society. http://www.ancr.nu. Accessed Jan 8, 2015
Linet MS, Dores GM, Kim CJ, Devesa SS, Morton LM (2013) Epidemiology and hereditary aspects of acute leukemia. In: Wiernik PH, Goldman JM, Dutcher J (eds) Neoplastic diseases of the blood, 5th edn. Springer, New York, pp 199–212
Perez-Saldivar ML, Fajardo-Gutierrez A, Bernaldez-Rios R, Martinez-Avalos A, Medina-Sanson A, Espinosa-Hernandez L et al (2011) Childhood acute leukemias are frequent in Mexico City: descriptive epidemiology. BMC Cancer 11:355. doi:10.1186/1471-2407-11-355
Novak I, Jaksic O, Kulis T, Batinjan K, Znaor A (2012) Incidence and mortality trends of leukemia and lymphoma in Croatia, 1988–2009. Croat Med J 53:115–123
Hjalgrim LL, Rostgaard K, Schmiegelow K, Soderhall S, Kolmannskog S, Vettenranta K et al (2003) Age- and sex-specific incidence of childhood leukemia by immunophenotype in the Nordic countries. J Natl Cancer Inst 95:1539–1544
Rowe JM (2010) Prognostic factors in adult acute lymphoblastic leukaemia. Br J Haematol 150:389–405. doi:10.1111/j.1365-2141.2010.08246.x
Faderl S, O’Brien S, Pui CH, Stock W, Wetzler M, Hoelzer D et al (2010) Adult acute lymphoblastic leukemia: concepts and strategies. Cancer 116:1165–1176. doi:10.1002/cncr.24862
Ludwig H, Bolejack V, Crowley J, Blade J, Miguel JS, Kyle RA et al (2010) Survival and years of life lost in different age cohorts of patients with multiple myeloma. J Clin Oncol 28:1599–1605. doi:10.1200/jco.2009.25.2114
Sant M, Minicozzi P, Mounier M, Anderson LA, Brenner H, Holleczek B et al (2014) Survival for haematological malignancies in Europe between 1997 and 2008 by region and age: results of EUROCARE-5, a population-based study. Lancet Oncol 15:931–942. doi:10.1016/s1470-2045(14)70282-7
Horibe K, Saito AM, Takimoto T, Tsuchida M, Manabe A, Shima M et al (2013) Incidence and survival rates of hematological malignancies in Japanese children and adolescents (2006–2010): based on registry data from the Japanese Society of Pediatric Hematology. Int J Hematol 98:74–88. doi:10.1007/s12185-013-1364-2
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The manuscript does not contain clinical studies, patient data, or research involving human participants or animals.
Conflict of interest
A.J.K., V.M.C., and M.A.K. are employees of Amgen Inc. W.M.S. is an employee of Amgen Ltd.
Appendix
Appendix
See Table 5.
Rights and permissions
About this article
Cite this article
Katz, A.J., Chia, V.M., Schoonen, W.M. et al. Acute lymphoblastic leukemia: an assessment of international incidence, survival, and disease burden. Cancer Causes Control 26, 1627–1642 (2015). https://doi.org/10.1007/s10552-015-0657-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10552-015-0657-6