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Persistent Osteoarticular Pain in Children

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Persistent Osteoarticular Pain in Children Louvigné et al. Pediatric Rheumatology (2020) 18:1 https://doi.org/10.1186/s12969-019-0376-8 RESEARCH ARTICLE Open Access Persistent osteoarticular pain in children: early clinical and laboratory findings suggestive of acute lymphoblastic leukemia (a multicenter case-control study of 147 patients) Mathilde Louvigné1* , Josué Rakotonjanahary1, Laurence Goumy2, Aude Tavenard3, Jean-François Brasme1, Fanny Rialland4, André Baruchel5, Marie-Françoise Auclerc5,6, Véronique Despert7, Marie Desgranges7, Sylvie Jean7, Albert Faye6,8, Ulrich Meinzer8, Mathie Lorrot8, Chantal Job-Deslandre8, Brigitte Bader-Meunier9, Virginie Gandemer3, Isabelle Pellier1 and on behalf of the GOCE Group Abstract Background: The aim of this study was to identify early clinical and laboratory features that distinguish acute lymphoblastic leukemia (ALL) from juvenile idiopathic arthritis (JIA) in children presenting with persistent bone or joint pain for at least 1 month. Methods: We performed a multicenter case-control study and reviewed medical records of children who initially presented with bone or joint pain lasting for at least 1 month, all of whom were given a secondary diagnosis of JIA or ALL, in four French University Hospitals. Each patient with ALL was paired by age with two children with JIA. Logistic regression was used to compare clinical and laboratory data from the two groups. Results: Forty-nine children with ALL and 98 with JIA were included. The single most important feature distinguishing ALL from JIA was the presence of hepatomegaly, splenomegaly or lymphadenopathy; at least one of these manifestations was present in 37 cases with ALL, but only in 2 controls with JIA, for an odds ratio (OR) of 154 [95%CI: 30–793] (regression coefficient: 5.0). If the presence of these findings is missed or disregarded, multivariate analyses showed that non-articular bone pain and/or general symptoms (asthenia, anorexia or weight loss) (regression coefficient: 4.8, OR 124 [95%CI: 11.4–236]), neutrophils < 2 × 109/L (regression coefficient: 3.9, OR 50 [95%CI: 4.3–58]), and platelets < 300 × 109/L (regression coefficient: 2.6, OR 14 [95%CI: 2.3–83.9]) were associated with the presence of ALL (area under the ROC curve: 0.96 [95%CI: 0.93–0.99]). Conclusions: Based on our findings we propose the following preliminary decision tree to be tested in prospective studies: in children presenting with at least 1 month of osteoarticular pain and no obvious ALL in peripheral smear, perform a bone marrow examination if hepatomegaly, splenomegaly or lymphadenopathy is present. If these manifestations are absent, perform a bone marrow examination if there is fever or elevated inflammatory markers associated with non-articular bone pain, general symptoms (asthenia, anorexia or weight loss), neutrophils < 2 × 109/L or platelets < 300 × 109/L. Keywords: Childhood acute lymphoblastic leukemia, Juvenile idiopathic arthritis, Diagnosis, Bone pain, Arthralgia * Correspondence: [email protected] 1Unité d’Onco-Hémato-Immunologie pédiatrique, CHU Angers, 4 rue Larrey, 49933 Angers, France Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Louvigné et al. Pediatric Rheumatology (2020) 18:1 Page 2 of 8 Background Methods Acute lymphoblastic leukemia (ALL) is the most com- This is a multicenter case-control study of children pre- mon childhood malignancy, accounting for 25% of can- senting with at least 1 month of persistent bone or joint cers in children [1, 2]. In 15–30% of cases, ALL is pain and who were ultimately diagnosed with ALL or diagnosed because of isolated and persistent osteoarticu- JIA. In this study we included children under the age of lar complaints without clear laboratory features which 18 who were diagnosed with ALL on the basis of bone could direct the diagnosis (normal blood count and ab- marrow examination results, after at least 1 month of sence of blasts in peripheral blood smear) [3]. Moreover, persistent bone or joint pain without associated pancyto- this form of ALL is associated with a lower incidence of penia or blasts in peripheral blood smear at the begin- hepatomegaly, splenomegaly or lymphadenopathy [4]. ning of complaints, between October 1, 2000 and March The time between the first episode of bone or joint pain 31, 2011, in the French University Hospitals of Angers, and a bone marrow examination is sometimes a period Nantes, Rennes and Robert Debré (Paris). All patients of several months [5, 6] and there can be a long succes- were included in the French national protocol FRALLE sion of visits to either the orthopedist or the rheuma- 2000. Pancytopenia was defined as the association of tologist pediatrician [7]. The first diagnosis, proposed for neutrophils, hemoglobin and platelets below the normal 76.5% of cases of bone and articular manifestations, is values for the age and gender. Each patient was paired juvenile idiopathic arthritis (JIA) [5], the most common by age with two children with JIA, followed up at rheumatic disease in children [8, 9], defined according to Rennes, Angers and Robert Debré University Hospitals the International League of Associations for Rheumatol- (competence centers for pediatric rheumatological dis- ogy (ILAR) criteria [10]. However, this is a diagnosis of eases), who presented with at least 1 month of isolated exclusion that rules out other rheumatic or infectious bone or joint pain, and who were diagnosed between diseases and malignancies, such as ALL [10]. ALL and September 1, 1998 and November 31, 2014. JIA was di- JIA can both present with chronic joint and periarticular agnosed according to the ILAR criteria defined in 2001 complaints, fever, hepatosplenomegaly or lymphadenop- [10]. All JIA children were within 2 years of age of their athy, anemia and elevated inflammatory markers [11, respective ALL patients. 12]. A bone marrow examination is the best way for the For each child, we identified information pertaining to clinician to diagnose ALL, especially when blasts are their demographic profile, symptoms and clinical mani- absent in peripheral blood smear [13]. When there is no festations at diagnosis and laboratory investigations car- hepatosplenomegaly or lymphadenopathy, and when ried out since the onset of pain was recorded. The term osteoarticular complaints are localized, it seems to be “localized initial presentation” was used if only one bone harder to distinguish ALL from non-systemic forms of or joint was painful at the onset of symptoms. In other JIA. cases, we considered the initial presentation as “diffuse”. Some studies have compared clinical and laboratory “Time to diagnosis” was defined as the interval between data obtained before the diagnosis of ALL or JIA in chil- the first symptoms and diagnosis. “General symptoms” dren presenting with chronic osteoarticular manifesta- were defined as the presence of at least one of the fol- tions. In the case of ALL, most of them described lowing parameters: anorexia, weight loss or asthenia. sudden, intense and localized periarticular pain, whereas “Weight loss” was defined as a weight decrease of more in the case of JIA, articular complaints appear in a more than 5%. “Elevated inflammatory markers” were defined progressive manner, with morning stiffness and arthritis as C-reactive protein (CRP) > 6 mg/L and/or the first [11, 14–16]. With regard to laboratory data, it has been hour’s erythrocyte sedimentation rate (ESR) > 20 mm. described that in the event of ALL, platelets and leuko- For each child, we calculated the mean and median cytes are normal or decreased, whereas their rate is often values of all laboratory data collected prior to the diag- elevated in the case of JIA [11, 12, 14]. Nevertheless, nosis. The study was approved by the ethics committee these different parameters seem to be insufficient for cli- of Angers University Hospital (a signed consent form nicians to distinguish ALL from JIA. was not required prior to patients’ inclusion because of The aim of this study was to describe early clinical and the retrospective character of the study and the non- laboratory features associated with ALL in children pre- nominal data collection). The reporting of the study was senting with isolated persistent osteoarticular pain for at performed according to TRIPOD recommendations [17]. least one month. These criteria could efficiently lead to the diagnosis of ALL rather than JIA, and allow physi- Statistical analysis cians to perform a bone marrow examination as early as Descriptive statistics were used to summarize the char- possible, before the appearance of hepatomegaly, spleno- acteristics of children with ALL and children with JIA. megaly or lymphadenopathy, high lymphocyte levels, cy- Variables related to disease and laboratory, demographic, topenia and blasts in peripheral blood smear [3]. and clinical characteristics were analyzed and described. Louvigné et al. Pediatric Rheumatology (2020) 18:1 Page 3 of 8 A multivariate analysis was performed using a logistic Table 1 Demographical and clinical characteristics of patients regression model to study factors associated with ALL with ALL or JIA in children with persistent bone or joint pain. Two ana- ALL JIA p lyses with two separate models were performed. In the N4998 first one, the following factors were considered as pos- Age, y (median 7.3 [3.6–12.4] 7.6 [3.1–12.4] NS** sible variables: gender, non-articular bone pain, joint [interquartile range]) pain, general symptoms, arthritis, fever and the pres- Sex ratio, males per 1.9 0.7 < 0.01* ence of at least one of the following manifestations: female hepatomegaly, splenomegaly or lymphadenopathy.
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