Ewing s sarcoma family tumours
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1 Oncology Ewing s sarcoma family tumours DIFFERENCES IN CLINICOPATHOLOGICAL CHARACTERISTICS AT PRESENTATION BETWEEN LOCALISED AND METASTATIC TUMOURS G. Bacci, A. Balladelli, C. Forni, A. Longhi, M. Serra, N. Fabbri, M. Alberghini, S. Ferrari, M. S. Benassi, P. Picci From the Istituti Ortopedici Rizzoli, Bologna, Italy Despite local treatment with systemic chemotherapy in Ewing s sarcoma family tumours (ESFT), patients with detectable metastases at presentation have a markedly worse prognosis than those with apparently localised disease. We investigated the clinical, pathological and laboratory differences in 888 patients with ESFT, 702 with localised disease and 186 with overt metastases at presentation, seen at our institution between 1983 and Multivariate analyses showed that location in the pelvis, a high level of serum lactic dehydrogenase, the presence of fever and a short interval between the onset of symptoms and diagnosis were indicative of metastatic disease. The rate of overt metastases at presentation was 10% without these four risk factors, 22.7% with one, 31.4% with two, and 50% for those with three or four factors. We concluded that in ESFT the site, the serum level of lactic dehydrogenase, fever, and the interval between the onset of symptoms and diagnosis are indicators of tumours having a particularly aggressive metastatic behaviour. G. Bacci, MD, Medical A. Balladelli, BA, Scientific Secretariat C. Forni, RN, Research Nurse A. Longhi, MD, Medical M. Serra, BSc, Biologist N. Fabbri, MD, Orthopaedic Surgeon M. Alberghini, MD, Pathologist S. Ferrari, MD, Medical M. S. Benassi, BSc, Biologist P. Picci, MD, Scientific Director Istituti Ortopedici Rizzoli, Via Pupilli 1, Bologna, Italy. Correspondence should be sent to Dr G. Bacci; gaetano.bacci@ior.it 2007 British Editorial Society of Bone and Joint Surgery doi: / x.89b $2.00 J Bone Joint Surg [Br] 2007;89-B: Received 8 March 2007; Accepted 18 May 2007 Ewing s sarcoma family tumour (ESFT) is one of the small round blue cell tumours. It is not a single condition, but a group of disorders which are both morphologically and clinically closely related, having a similar molecular biology, namely expression of tumour-specific chimeric oncoproteins through balanced chromosomal translocations involving the Ewing s sarcoma gene. Ewings sarcoma family tumours include typical Ewing s sarcoma of bone, extraosseous Ewing s sarcoma, Askin tumour and peripheral neuroectodermal tumours (PNET). In the last 30 years, with the addition of systemic therapy to local treatment, the prognosis for patients with ESFT has steadily improved. 1-6 The efficacy of chemotherapy appears to be closely dependent on the stage of the disease. The rate of long-term survival is 50% to 70% for patients with localised tumour, but only 15% to 20% for those with metastases at presentation The presence of overt metastases at diagnosis distinguishes a group of patients with a particularly adverse prognosis. We analysed patients with ESFT to assess the time between the onset of symptoms and diagnosis. We also reviewed the tumours and other host factors of the patients with localised disease and those with metastases. The same analyses were reported in a previous paper, 11 which included only patients with typical Ewing s sarcoma of bone, observed between 1972 and 1997, and therefore in part staged with less reliable methods than current imaging techniques of CT and MRI. Of the 618 patients cited in this previous analysis only 434 are included in the present series, and we did not investigate certain variables (PNET vs typical Ewing s sarcoma; bone vs soft tissue) that are considered here. Patients and Methods Between 1983 and 2006, a diagnosis of ESFT was made in 888 patients who were identified from our database. The patients clinical characteristics, general medical records, laboratory data, pathology and radiology reports were collected from these files. Slides and radiographs were reviewed for incomplete or inaccurate information. The diagnosis of ESFT was made from open biopsies, and evaluated by conventional morphological criteria. Histopathological diagnosis was based on the presence of a small round cell tumour with no histological, cytological, ultrastructural or immunohistochemical features of lymphoma, rhabdomyosarcoma, or neuroblastoma. The diagnostic material included haematoxylin and eosin (Bio-optica, Milan, Italy), periodic acid-schiff (Carlo Erba Reagenti, Milan, Italy), reticulum and silver trochrome VOL. 89-B, No. 9, SEPTEMBER
2 1230 G. BACCI, A. BALLADELLI, C. FORNI, A. LONGHI, M. SERRA, N. FABBRI, M. ALBERGHINI, S. FERRARI, M. S. BENASSI, P. PICCI Table I. Comparison of characteristics between patients with and without metastases at presentation Number of patients Localised Metastatic (%) Odds ratio 95% CI * p-value Gender Male (21.0) 0.95 Female (20.8) to 1.77 Site Other sites (15.5) Pelvis (37.6) to Age < 12 years (15.0) years (23.0) to 2.56 Serum LDH Normal (7.3) High (20.5) to 6.1 Anaemia No (10.3) 0.03 Yes (29.2) to 3.72 Volume ** < (18.3) (28.9) to 2.40 Histology PNET (23.8) 0.08 TES (16.3) to 1.96 Interval symptoms/ diagnosis < 2 months (35.3) months (15.9) to 4.7 Bone vs soft tissue Bone (20.5) 0.10 Soft tissue (36.0) to 1.76 Fever Yes (33.6) No (19.0) to 2.03 * 95% CI, confidence interval p-value, chi-square test LDH, lactic dehydrogenase (data mare missing for 146 patients two patients with severe anaemia were microcythaemic ** the data are missing for 301 patients PNET, peripheram neuroectodermal tumours (data are missing for 434 patients observed before 1991); TES, typical Ewings sarcoma of bone in 15 patients it was not possible to determine time interval between symptoms and diagnosis (Bio-optica), and other common histochemical stainings for all patients. More sophisticated immunohistochemical investigations to differentiate typical Ewing s sarcoma of bone and PNET were carried out in the 454 more recent cases. In these patients, the diagnosis of PNET was made when the specimen proved positive to at least one of these markers of neural differentiation, namely neuronon-specific enolase, S100, Leu-7 and secretogranin. Although cytogenetic analyses were performed in most cases, the results of these studies are not considered. All the specimens were reviewed by two pathologists (PB and MA), who were blinded to information regarding the stage of the disease. Clinical and radiological evaluation. The initial evaluation in all cases included a complete history, physical examination, haematological examination and several chemical laboratory tests, including the serum lactic dehydrogenase. The interval between the onset of symptoms and the final diagnosis was also investigated. Primary tumours were staged by use of plain radiographs, a technetium-99 ( 99 Tc) bone scan, a CT scan and, in the 300 most recent cases, MRI. Tumour size was estimated using CT scan measurements of the three diameters of the lesion and calculated according to the method reported by Gobel et al. 12 The presence of metastases was assessed by 99 Tc bone scan for bone lesions, and by THE JOURNAL OF BONE AND JOINT SURGERY
3 EWING S SARCOMA FAMILY TUMOURS 1231 Table II. Percentage of metastases at presentation according to tumour site Site of primary tumour Number of patients Pelvis Sacrum Rib Spine Other sites 6 25 Foot 9 22 Humerus Femur Scapula Radium Fibula Ulna 8 12 Clavicle 11 9 Tibia Jaw 2 0 Metastases at presentation conventional radiographs and CT scan of the chest for pulmonary deposits. Statistical analysis. Comparison between patients with metastatic and non-metastatic disease at presentation was investigated according to the following variables: gender and age; the presence of fever (> 37.9 C for at least two weeks before diagnosis), the interval between the onset of symptoms and histological diagnosis; serum haemoglobin (Hb); serum lactic dehydrogenase (normal (< 460 UI/L) vs elevated (> 460/UI/L)); tumour site (pelvis vs other sites); bone vs soft-tissue tumours; histology of typical Ewing s sarcoma of bone vs PNET; and tumour volume. For tumour volume the cut-off point of 150 ml was chosen according to the Cooperative Ewing Sarcoma Study For the continuous variables (age, Hb, interval between onset of symptoms and histological diagnosis) different levels were investigated to identify the value that best distinguished patients with metastases at presentation from those without. The following levels were investigated: for ages 11, 12, 13, 14, 15 and 16 years, for Hb 8, 9, 10, 11, 12 and 13 g/dl, and for the interval between onset of symptoms and diagnosis of one, two, three and four months. The levels with the strongest statistical significance were 12 years for age; 11 g/dl for male and 10 g/dl for female Hb, and two months for the interval between the onset of symptoms and diagnosis. The prevalence of different variables in patients with and without metastases was investigated by means of the chisquared test. The probability of metastatic disease at presentation of dichotomous variables was described by an odds ratio. Multivariate logistic regression analysis was performed to evaluate the influence on staging of the disease of variables that were statistically significant on univariate analysis. A p-value of 0.05 was considered significant. Results The characteristics of the 888 patients in the study are shown in Table I. Of these, 702 (79%) had a localised tumour at the time of diagnosis and 186 (21%) had metastases. In 16 of these cases metastases involved several sites, giving a total number of 202. The site was the lung in 127 cases (62.8%), bone in 72 (35.6%), and other sites (lymph-node, meninges, kidney) in three (1.5%). Metastases in the lung were seen on conventional radiographs in 110 cases (87%), but in 17 (13%) they were detected only by a CT scan of the chest. In the same site metastases were single in 41 (32.5%) of cases and multiple in 84 (67.5%). Univariate analysis showed that there were no significant differences between patients with either localised or metastatic tumours at presentation as regards gender (21% (440) for male vs 20.8% (69) for female; odds ratio, p = 0.95), histological subtype (16.3% (54) for typical Ewings sarcoma of bone vs 23.8% (29) for PNET; odds ratio, p = 0.08) and bone or soft-tissue locations (20.5% (177) vs 36.0% (9); odds ratio, p = 0.10). Metastatic disease occurred more frequently, (a) in patients with a primary tumour of the pelvis rather than at other sites (37.6% (82) vs 18.3% (104), odds ratio, p < ), (b) in patients older than 12 years than in younger patients (22.8% (166) vs 15.0% (24), odds ratio, p < 0.004); (c) in patients with high levels of lactic dehydrogenase rather than in those with normal values of this enzyme (20.5% (57) vs 7.3% (34), odds ratio, p < ); (d) in patients with anaemia than in patients with normal Hb values (29.2% (33) vs 19.8% (80)); (e) in patients with tumour volume > 150 ml than in those with smaller tumours (28.9% (97) vs 18.3% (46), odds ratio, p < 0.004); (f) in patients with an interval between the onset of symptoms and diagnosis of less than two months rather than in patients with an interval of more than two months (35.5% (76) vs 15.9% (105), (odds ratio, p < ); and (g) in patients with fever than in patients with a normal temperature (33.6% (40) vs 19.0% (146), odds ratio, p < ). The rate of metastatic cases at diagnosis according to the site of the primary tumour in single bones is shown in Table II. Excluding the two cases in the VOL. 89-B, No. 9, SEPTEMBER 2007
4 1232 G. BACCI, A. BALLADELLI, C. FORNI, A. LONGHI, M. SERRA, N. FABBRI, M. ALBERGHINI, S. FERRARI, M. S. BENASSI, P. PICCI Table III. Multivariate analysis Parameter Relative risk 95% CI * p-value Pelvis to Other sites 1 High serum lactic dehydrogenase to Normal serum lactic dehydrogenase 1 Interval symptoms to diagnosis < 2 months to Interval symptoms 2 months 1 Presence of fever to No fever 1 * 95% CI, 95% confidence interval Table IV. Percentage of patients with metastatic disease at presentation according to unfavourable prognostic factors Number unfavourable prognostic factors Number of cases Metastatic at presentation p-value None One Two Three to four jaw, metastatic tumours at presentation ranged between 36% (82) for primary tumours located in the pelvis or sacrum and 8% (120) for those located in the tibia. In the 27 patients with values of serum lactic dehydrogenase times higher than normal, 25 (92.5%) presented with metastases. The seven variables significant at univariate analysis were included in a multivariate logistic regression analysis (Table III). Age, the presence of anaemia and tumour volume lost statistical significance on univariate analysis, whereas the tumour site, serum values of lactic dehydrogenase, the interval between the onset of symptoms and the diagnosis, and the presence of fever were found to be independent predictive variables of metastatic disease at presentation. The four variables significantly related to metastatic disease on multivariate analysis were investigated to see whether and how their absence or the contemporaneous presence of two or more unfavourable variables could be associated with the presence of metastases at diagnosis (Table IV). Of the 888 patients, 339 (38.1%) showed none of these four variables; only one was present in 321 patients (36.1%), two in 185 patients (20.8%), and three or four in 42 (4.7%). The rate of metastatic disease at presentation was 10% in the subset of patients with no risk variables, 22.7% in those with one factor, 31.4% in those with two risk variables, and 50% in those with three and four factors. The differences between these four groups were all statistically significant (p < ). Discussion Before the 1970s, even in patients with ESFT apparently still localised at diagnosis, when the treatment was only local therapy (surgery, radiotherapy or both), the prognosis was very poor, with a cure rate of less than 15% This indicates that most patients had micrometastases undetectable by radiography and bone scintigraphy. For this group of patients the combination of systemic chemo therapy with local treatment has dramatically improved the prognosis in the last 35 years. However, although the cure rate for patients without overt metastases has risen to more than 50% to 60%, 1-6 for those who have metastases at diagnosis the prognosis remains poor and not more than 15% to 25% are cured. 7-9 Although the majority of patients with ESFT have microscopic metastases at diagnosis, the presence of grossly detectable metastatic disease distinguishes those patients with a particularly adverse prognosis. In our study, the characteristics of patients with detectable metastases at presentation were investigated and compared with those without overt metastases. A significantly different distribution of some characteristics between the two groups of patients was found. At multivariate analysis the former group was characterised by a significant prevalence of pelvic location of the tumour, a high level of serum lactic dehydrogenase, the presence of fever, and a shorter interval between onset of symptoms and diagnosis. The incidence of metastatic disease at presentation shows a significant correlation with one or more of these unfavourable factors, being 22.7% with only one, 31.4% with two, and 50% with three or four. In the subset of patients presenting with none of these unfavourable prognostic factors, evident metastatic disease at presentation was only 10%. It would have been interesting to compare our current data on patients with metastatic disease at THE JOURNAL OF BONE AND JOINT SURGERY
5 EWING S SARCOMA FAMILY TUMOURS 1233 presentation against those of other series, but the published articles on ESFT with overt metastases do not give such detailed information. 7-9 A primary tumour in the pelvis, a high level of serum lactic dehydrogenase, and the presence of fever 20 have been stated to indicate a significantly worse prognosis also in patients with ESFT localised at presentation and treated with adjuvant or neoadjuvant chemotherapy. In our study the time to diagnosis was not found to be positively associated with the stage of the disease, but, on the contrary, patients with metastatic tumour at presentation were diagnosed significantly earlier than those with localised disease. In patients with a tumour it is generally believed that the presence of metastases at presentation is a consequence of delayed diagnosis, which offers a greater opportunity for tumour cells to metastasise. However, the association between advanced disease and delay in diagnosis has been demonstrated in some tumours but not others. 11,25,26 With the exception of osteosarcoma, 27 there is no tumour where staging at onset is inversely correlated to the symptoms and diagnosis. A possible explanation could be that an early presentation by patients with metastatic disease probably reflects more rapid growth of the tumour, of which its biological phenotype is an expression and may differ between subgroups of apparently similar ESFT. Such aggressive behaviour may be reflected by the clinical course of the tumour and its propensity to respond to treatment. It is tempting to speculate that in patients with ESFT who present with overt disease at diagnosis, it may be the biological characteristics of the tumour or host that make them ultimately less susceptible to treatment. The authors thank P. Bacchini, for histological review, and Ms C. Ghinelli for all graphic work done in this manuscript. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. References 1. Burgert EO, Nesbit ME, Garnsey LA, et al. Multimodal therapy for the management of nonpelvic, localized Ewing s sarcoma of bone: intergroup study IESS-II. J Clin Oncol 1990;8: Nesbit ME, Gehan EA, Burgert EO, et al. Multimodal therapy for the management of primary nonmetastatic Ewing s sarcoma of bone: a long-term follow-up of the First Intergroup study. J Clin Oncol 1990;8: Oberlin O, Deley MC, Bui BN, et al. Prognostic factors in localized Ewing s tumours and peripheral neuroectodermal tumours: the third study of the French Society of Paediatric Oncology (EW88 study). Br J Cancer 2001;85: Craft AW, Cotterill SJ, Bullimore JA, Pearson D. Long-term results from the first UKCCSG Ewing s Tumour Study (ET-1): United Kingdom children s cancer study group (UKCCSG) and the medical research council bone sarcoma working party. 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