Incidence of sarcoma histotypes and molecular subtypes in a prospective epidemiological study with central pathology review and molecular testing

Françoise Ducimetière, Antoine Lurkin, Dominique Ranchère-Vince, Anne-Valérie Decouvelaere, Michel Péoc'h, Luc Istier, Philippe Chalabreysse, Christine Muller, Laurent Alberti, Pierre-Paul Bringuier, Jean-Yves Scoazec, Anne-Marie Schott, Christophe Bergeron, Dominic Cellier, Jean-Yves Blay, Isabelle Ray-Coquard, Françoise Ducimetière, Antoine Lurkin, Dominique Ranchère-Vince, Anne-Valérie Decouvelaere, Michel Péoc'h, Luc Istier, Philippe Chalabreysse, Christine Muller, Laurent Alberti, Pierre-Paul Bringuier, Jean-Yves Scoazec, Anne-Marie Schott, Christophe Bergeron, Dominic Cellier, Jean-Yves Blay, Isabelle Ray-Coquard

Abstract

Background: The exact overall incidence of sarcoma and sarcoma subtypes is not known. The objective of the present population-based study was to determine this incidence in a European region (Rhone-Alpes) of six million inhabitants, based on a central pathological review of the cases.

Methodology/principal findings: From March 2005 to February 2007, pathology reports and tumor blocks were prospectively collected from the 158 pathologists of the Rhone-Alpes region. All diagnosed or suspected cases of sarcoma were collected, reviewed centrally, examined for molecular alterations and classified according to the 2002 World Health Organization classification. Of the 1287 patients screened during the study period, 748 met the criteria for inclusion in the study. The overall crude and world age-standardized incidence rates were respectively 6.2 and 4.8 per 100,000/year. Incidence rates for soft tissue, visceral and bone sarcomas were respectively 3.6, 2.0 and 0.6 per 100,000. The most frequent histological subtypes were gastrointestinal stromal tumor (18%; 1.1/100,000), unclassified sarcoma (16%; 1/100,000), liposarcoma (15%; 0.9/100,000) and leiomyosarcoma (11%; 0.7/100,000).

Conclusions/significance: The observed incidence of sarcomas was higher than expected. This study is the first detailed investigation of the crude incidence of histological and molecular subtypes of sarcomas.

Conflict of interest statement

Competing Interests: The authors would like to specify that Dr. Dominic Cellier is the scientific relationship director of Merck-Serono. Merck-Serono provides financial support. The authors confirm that this does not alter their adherence to all the PLoS ONE policies on sharing data and materials.

Figures

Figure 1. The French ADICAP coding system…
Figure 1. The French ADICAP coding system (http://www.adicap.asso.fr/).
Figure 2. Selection of patients eligible for…
Figure 2. Selection of patients eligible for inclusion.
Figure 3. Age-specific incidence rates (per 100,000).
Figure 3. Age-specific incidence rates (per 100,000).
(A) Age-specific rates by sarcoma type. (B) Age-specific rates within bone sarcomas, for the 3 most important histotypes. (C) Age-specific rates for liposarcoma subtypes.

References

    1. Clark MA, Fisher C, Judson I, Thomas JM. Soft-tissue sarcomas in adults. N Engl J Med. 2005;353:701–11.
    1. Jemal A, Siegel R, Ward E, Murray T, Xu J, et al. Cancer statistics, 2006. CA Cancer J Clin. 2006;56:106–30.
    1. Parkin DM, Stiller CA, Nectoux J. International variations in the incidence of childhood bone tumours. Int J Cancer. 1993;53:371–6.
    1. Stiller CA, Parkin DM. International variations in the incidence of childhood soft-tissue sarcomas. Paediatr Perinat Epidemiol. 1994;8:107–19.
    1. Fletcher CDM, Unni KK, Mertens F. World Health Organization Classification of Tumors. Pathology and Genetics of Tumors of Soft Tissue and Bone. 2002. IARC Press: Lyon.
    1. Corless CL, Schroeder A, Griffith D, Town A, McGreevey L, et al. PDGFRA mutations in gastrointestinal stromal tumors: frequency, spectrum and in vitro sensitivity to imatinib. J Clin Oncol. 2005;23:5357–64.
    1. De Vita V, Lawrence T, Rosenberg S. 2008. DeVita, Hellman and Rosenberg's Cancer: Principles and Practice of Oncology, Eighth ed.
    1. Nilsson B, Bumming P, Meis-Kindblom JM, Oden A, Dortok A, et al. Gastrointestinal stromal tumors: the incidence, prevalence, clinical course, and prognostication in the preimatinib mesylate era–a population-based study in western Sweden. Cancer. 2005;103:821–9.
    1. Zahm SH, Fraumeni JF., Jr The epidemiology of soft tissue sarcoma. Semin Oncol. 1997;24:504–14.
    1. Antonescu CR. The role of genetic testing in soft tissue sarcoma. Histopathology. 2006;48:13–21.
    1. Berger C, Trombert-Paviot B, Mitton N, Frappaz D, Galambrun C, et al. [Childhood cancer incidence and survival rates in the Rhone-Alpes regional paediatric registry 1987–1999]. Arch Pediatr. 2006;13:121–9.
    1. Guillou L, Coindre JM, Bonichon F, Nguyen BB, Terrier P, et al. Comparative study of the National Cancer Institute and French Federation of Cancer Centers Sarcoma Group grading systems in a population of 410 adult patients with soft tissue sarcoma. J Clin Oncol. 1997;15:350–62.
    1. Fletcher CD, Berman JJ, Corless C, Gorstein F, Lasota J, et al. Diagnosis of gastrointestinal stromal tumors: A consensus approach. Hum Pathol. 2002;33:459–65.
    1. Miettinen M, Lasota J. Gastrointestinal stromal tumors: pathology and prognosis at different sites. Semin Diagn Pathol. 2006;23:70–83.
    1. Hamilton SR, Aaltonen LA. World Health Organization Classification of Tumors. Pathology and Genetics of Tumors of the Digestive System. 2000. IARC Press: Lyon.
    1. Tavassoli FA, Devilee P. World Health Organization Classification of Tumors. Pathology and Genetics of Tumors of the Breast and female genital organs. 2003. IARC Press: Lyon.
    1. Peter M, Gilbert E, Delattre O. A multiplex real-time pcr assay for the detection of gene fusions observed in solid tumors. Lab Invest. 2001;81:905–12.
    1. Ahmad O, Boschi-Pinto C, Lopez AD, Murray CJL, Lozano R, et al. 2001. Age standardization of rates: a new WHO standard. Geneva, World Health Organization, 2001 (GPE Discussion Paper No. 31). 2001.
    1. Cassier PA, Ducimetiere F, Lurkin A, Ranchere-Vince D, Scoazec JY, et al. A prospective epidemiological study of new incident GISTs during two consecutive years in Rhone Alpes region: incidence and molecular distribution of GIST in a European region. Br J Cancer. 2010;103:165–70.
    1. Levi F, La Vecchia C, Randimbison L, Te VC. Descriptive epidemiology of soft tissue sarcomas in Vaud, Switzerland. Eur J Cancer. 1999;35:1711–6.
    1. Toro JR, Travis LB, Wu HJ, Zhu K, Fletcher CD, Devesa SS. Incidence patterns of soft tissue sarcomas, regardless of primary site, in the surveillance, epidemiology and end results program, 1978–2001: An analysis of 26,758 cases. Int J Cancer. 2006;119:2922–30.
    1. Pastore G, Peris-Bonet R, Carli M, Martinez-Garcia C, Sanchez de Toledo J, et al. Childhood soft tissue sarcomas incidence and survival in European children (1978–1997): report from the Automated Childhood Cancer Information System project. Eur J Cancer. 2006;42:2136–49.
    1. Stiller CA, Bielack SS, Jundt G, Steliarova-Foucher E. Bone tumours in European children and adolescents, 1978–1997. Report from the Automated Childhood Cancer Information System project. Eur J Cancer. 2006;42:2124–35.
    1. Colonna M, Bossard N, Mitton N, Remontet L, Belot A, et al. [Some interpretation of regional estimates of the incidence of cancer in France over the period 1980–2005]. Rev Epidemiol Sante Publique. 2008;56:434–40.
    1. Curado MP, Edwards B, Shin HR, Storm H, Ferlay J, et al. 2007. Cancer Incidence in Five Continents, Vol. IX. IARC Scientific Publications No.160,Lyon, IARC.
    1. Ries LAG, Smith MA, Gurney JG, Linet M, Tamra T, et al. Cancer Incidence and Survival among Children and Adolescents: United States SEER Program 1975–1995. 1999. National Cancer Institute, SEER Program. NIH Pub. No. 99-4649. Bethesda MD.
    1. Pritchard-Jones K, Kaatsch P, Steliarova-Foucher E, Stiller CA, Coebergh JW. Cancer in children and adolescents in Europe: developments over 20 years and future challenges. Eur J Cancer. 2006;42:2183–90.
    1. Engholm G, Ferlay J, Christensen N, Gjerstorff ML, Klint A, et al. NORDCAN: Cancer Incidence, Mortality, Prevalence and Prediction in the Nordic Countries, Version 3.6. 2010. Association of the Nordic Cancer Registries. Danish Cancer Society. ( )
    1. Arbiser ZK, Folpe AL, Weiss SW. Consultative (expert) second opinions in soft tissue pathology. Analysis of problem-prone diagnostic situations. Am J Clin Pathol. 2001;116:473–6.
    1. Meis-Kindblom JM, Bjerkehage B, Bohling T, Domanski H, Halvorsen TB, et al. Morphologic review of 1000 soft tissue sarcomas from the Scandinavian Sarcoma Group (SSG) Register. The peer-review committee experience. Acta Orthop Scand Suppl. 1999;285:18–26.
    1. Lurkin A, Ducimetiere F, Ranchere VD, Decouvelaere AV, Cellier D, et al. Epidemiological evaluation of concordance between initial diagnosis and central pathology review in a comprehensive and prospective series of sarcoma patients in the Rhone-Alpes region. BMC Cancer. 2010;10:150.
    1. Kramarova E, Stiller CA. The international classification of childhood cancer. Int J Cancer. 1996;68:759–65.
    1. Steliarova-Foucher E, Stiller C, Lacour B, Kaatsch P. International Classification of Childhood Cancer, third edition. Cancer. 2005;103:1457–67.
    1. Menegoz F, Black RJ, Arveux P, Magne V, Ferlay J, et al. Cancer incidence and mortality in France in 1975–95. Eur J Cancer Prev. 1997;6:442–66.
    1. Worch J, Matthay KK, Neuhaus J, Goldsby R, DuBois SG. Ethnic and racial differences in patients with Ewing sarcoma. Cancer. 2010;116:983–8.
    1. Eyre R, Feltbower RG, James PW, Blakey K, Mubwandarikwa E, et al. The epidemiology of bone cancer in 0–39 year olds in northern England, 1981–2002. BMC Cancer. 2010;10:357:357.
    1. Wibmer C, Leithner A, Zielonke N, Sperl M, Windhager R. Increasing incidence rates of soft tissue sarcomas? A population-based epidemiologic study and literature review. Ann Oncol 2009
    1. Ross JA, Severson RK, Davis S, Brooks JJ. Trends in the incidence of soft tissue sarcomas in the United States from 1973 through 1987. Cancer. 1993;72:486–90.
    1. Kaatsch P, Steliarova-Foucher E, Crocetti E, Magnani C, Spix C, et al. Time trends of cancer incidence in European children (1978–1997): report from the Automated Childhood Cancer Information System project. Eur J Cancer. 2006;42:1961–71.
    1. Linabery AM, Ross JA. Trends in childhood cancer incidence in the U.S. (1992–2004). Cancer. 2004;112:416–32.
    1. Tryggvason G, Gislason HG, Magnusson MK, Jonasson JG. Gastrointestinal stromal tumors in Iceland, 1990–2003: the icelandic GIST study, a population-based incidence and pathologic risk stratification study. Int J Cancer. 2005;117:289–93.
    1. Coindre JM. Immunohistochemistry in the diagnosis of soft tissue tumours. Histopathology. 2003;43:1–16.
    1. Daugaard S. Current soft-tissue sarcoma classifications. Eur J Cancer. 2004;40:543–8.
    1. Goettsch WG, Bos SD, Breekveldt-Postma N, Casparie M, Herings RM, et al. Incidence of gastrointestinal stromal tumours is underestimated: results of a nation-wide study. Eur J Cancer. 2005;41:2868–72.
    1. Perez EA, Livingstone AS, Franceschi D, Rocha-Lima C, Lee DJ, et al. Current incidence and outcomes of gastrointestinal mesenchymal tumors including gastrointestinal stromal tumors. J Am Coll Surg. 2006;202:623–9.
    1. Lazar AJ, Trent JC, Lev D. Sarcoma molecular testing: diagnosis and prognosis. Curr Oncol Rep. 2007;9:309–15.
    1. Andersson J, Bumming P, Meis-Kindblom JM, Sihto H, Nupponen N, et al. Gastrointestinal stromal tumors with KIT exon 11 deletions are associated with poor prognosis. Gastroenterology. 2006;130:1573–81.
    1. Sorensen PH, Lynch JC, Qualman SJ, Tirabosco R, Lim JF, et al. PAX3-FKHR and PAX7-FKHR gene fusions are prognostic indicators in alveolar rhabdomyosarcoma: a report from the children's oncology group. J Clin Oncol. 2002;20:2672–9.
    1. Ladanyi M, Antonescu CR, Leung DH, Woodruff JM, Kawai A, et al. Impact of SYT-SSX fusion type on the clinical behavior of synovial sarcoma: a multi-institutional retrospective study of 243 patients. Cancer Res. 2002;62:135–40.
    1. Corless CL, Fletcher JA, Heinrich MC. Biology of gastrointestinal stromal tumors. J Clin Oncol. 2004;22:3813–25.
    1. Williamson D, Missiaglia E, de Reynies A, Pierron G, Thuille B, et al. Fusion gene-negative alveolar rhabdomyosarcoma is clinically and molecularly indistinguishable from embryonal rhabdomyosarcoma. J Clin Oncol. 2010;28:2151–8.
    1. Vauhkonen H, Savola S, Kaur S, Larramendy ML, Knuutila S. Molecular karyotyping in sarcoma diagnostics and research. Adv Exp Med Biol. 2006;587:53–63.
    1. Nielsen TO, West RB, Linn SC, Alter O, Knowling MA, et al. Molecular characterisation of soft tissue tumours: a gene expression study. Lancet. 2002;359:1301–7.
    1. Nielsen TO, West RB. Translating gene expression into clinical care: sarcomas as a paradigm. J Clin Oncol. 2010;28:1796–805.
    1. Miettinen M. From morphological to molecular diagnosis of soft tissue tumors. Adv Exp Med Biol. 2006;587:99–113.
    1. Wolden SL, Alektiar KM. Sarcomas across the age spectrum. Semin Radiat Oncol. 2010;20:45–51.
    1. Ferrari A, Casanova M, Collini P, Meazza C, Luksch R, et al. Adult-type soft tissue sarcomas in pediatric-age patients: experience at the Istituto Nazionale Tumori in Milan. J Clin Oncol. 2005;23:4021–30.
    1. Soliman H, Ferrari A, Thomas D. Sarcoma in the young adult population: an international view. Semin Oncol. 2009;36:227–36.

Source: PubMed

Sponsor e collaboratori

Condizioni mediche

Interventi farmacologici

3
Sottoscrivi