Editorial article
Systemic lupus erythematosus criteria nowadays
Los criterios del lupus eritematoso sistémico en la actualidad
Ricard Cervera
Servicio de Enfermedades Autoinmunes, Hospital Clínic de Barcelona, Barcelona, Spain
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For years, this has increased the interest in developing criteria that prove to be useful, if not for diagnosing all patients with these conditions, at least for classifying these entities in a uniform way and enabling their homologous identification in scientific studies, clinical trials, patient registries, and case analyses or, in other words, to “speak a common language” when referring to a given disease.</p><p id="par0010" class="elsevierStylePara elsevierViewall">Systemic lupus erythematosus (SLE) constitutes one of the most paradigmatic cases of this problem. The absence of defined etiological factors, its multifactorial and complex pathogenesis, as well as the great variability in its clinical manifestations and laboratory findings have meant that the diagnosis and classification of this disease can only be established by assessing the combined presence of certain clinical and biological parameters considered to be most characteristic of this ailment.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1,2</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">First of all, it should be emphasized that the concept of classification differs from that of diagnosis. Classification is a scientific approach that uses a positive definition based on a limited number of elements and the aim of which is to combine relatively homogeneous groups of patients with a given disease. Diagnosis, on the other hand, is a highly individualized approach that affects a single patient and may include all available information. It is often iterative and relies heavily on ruling out other entities. In essence, a diagnosis is always tentative, whereas a classification is more specific and, therefore, should not be wrong very often. In scientific terms, specificity is crucial for the classification, while sensitivity is more important for the diagnosis, as an undiagnosed patient will be left untreated. For these reasons, classification criteria should not be abused when making a diagnosis, even though the diagnosis and classification often match.<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">The above facts led a group of experts from the American Rheumatism Association (ARA) (the current American College of Rheumatology [ACR]) to draw up the first classification criteria for SLE in 1971.<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> Eleven years later, in 1982, these criteria were modified and transformed into new criteria<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> that represented a remarkable advance in diagnostic sensitivity, without compromising specificity, with a high discriminatory power compared with other systemic diseases. The classification of a patient as having LES required the presence, whether simultaneously or over time, of at least four of the 11 classificatory criteria that were chosen as being more typical of this disease. The description of antiphospholipid antibodies a few years later led to the withdrawal, in 1997, of a laboratory criterion that was obsolete due to its complexity and low sensitivity (lupus erythematosus [LE] cells) and its replacement with positivity for these new antibodies.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">These criteria, however, presented several important problems from the outset.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> Firstly, the existence of initial mono- or paucisymptomatic forms, which could occasionally be severe, such as those with renal or neurological involvement, which could not be classified as a SLE due to the fact that they failed to meet the minimum four criteria required. A second aspect that hampered the application of these criteria is the different forms of presentation of SLE in specific groups of patients. Thus, the behavior of this disease tends to differ during childhood, in men, or in postmenopausal women (in which case the incidence seems to have increased over the past few years), as well as in patients of different ethnicities or races (African Americans, mixed Latin Americans, etc.), owing to which the efficacy of these criteria to correctly classify patients was reduced. Finally, the interpretation of many clinical manifestations of the disease is often complex. For example, the first three classification criteria of the ACR referred to cutaneous manifestations (malar rash, discoid lesions, and photosensitivity), whose assessment can sometimes be difficult for clinicians not specializing in dermatology, such as correctly distinguishing a “butterfly” malar rash from other problems that are similar in both shape and location (eczema, rosacea, etc.). Another group of clinical manifestations, such as neurological, and, in particular, psychiatric ones, constitute an important challenge, basically due to their multiple clinical forms, as well as to the diversity of the pathogenetic mechanisms involved and their difficult pathological verification. The ACR itself defined 19 neuropsychiatric syndromes in SLE,<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> only two (seizures and psychosis) of which were part of the classificatory criteria.</p><p id="par0030" class="elsevierStylePara elsevierViewall">In an attempt to overcome these problems, the Systemic Lupus International Collaborating Clinics (SLICC) collaborative working group carried out extensive work on the generation and validation of variables leading to the publication of new classification criteria in 2012.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> As with those of the ACR, at least four criteria had to be met, although in this case, at least one clinical and another laboratory criterion had to be satisfied. These new criteria also allowed for classifying patients with exclusively renal involvement as positive for SLE or included the different neuropsychiatric syndromes of SLE. Several validation studies carried out in different geographic areas of the world showed that these criteria are reproducible and have a slightly higher sensitivity than those of the ACR, albeit with similar specificity, thus allowing some patients to be classified as having SLE earlier in the clinical course of their disease.<a class="elsevierStyleCrossRefs" href="#bib0050"><span class="elsevierStyleSup">10,11</span></a> In recent years, other independent groups have also proposed other classification criteria based on sequential or branching schemes<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> or weighted according to the specificity of the variables for SLE.<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> However, the main international scientific societies did not endorse any of these criteria to warrant recommending their widespread use in scientific studies, trials, registries, or official diagnostic and treatment guidelines.</p><p id="par0035" class="elsevierStylePara elsevierViewall">For this reason, the two main international scientific societies including specialists in SLE; that is, the European Alliance of Associations for Rheumatology (EULAR) and the ACR, decided to jointly undertake the daunting task of creating and validating classificatory criteria for this disease using a widely tested method for this task. The goals of this project were ambitious, including preserving the high specificity of the ACR criteria<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> while achieving a sensitivity similar to that of the SLICC criteria.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> In the end, this all led to the publication of the new EULAR/ACR classificatory criteria for SLE in 2019.<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> As a mandatory criterion (entry criterion), these include the presence of antinuclear antibodies, together with a score above 10 points based on the clinical manifestations and pathological findings, which are assigned a different weight according to their specificity (from 2 points in the presence of a fever of non-infectious origin, delirium, alopecia, oral ulcers, or antiphospholipid antibody positivity, to 10 points for the finding of local or diffuse nephropathy in a kidney biopsy). Items are categorized into domains (constitutional, hematologic, neuropsychiatric, mucocutaneous, etc.), within which only the item with the highest score must be counted. In addition, instead of many defined exclusions, a rule that the items must be attributed to SLE and only counted if there is no other likely alternative diagnosis is applied. This classification also allows for making a diagnosis when the involvement predominantes in a single organ (for example, renal or neurological), which facilitates an early detection and treatment of the disease. Initial validation data indicate that the new criteria met the intended targets with a specificity of 93% (as in the case of the ACR criteria) and a sensitivity of 96% (versus 97% of the SLICC criteria).<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> These criteria are now expected to be validated externally in several other patient cohorts.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">In any case, the possibility of excluding, at least initially, some patients with clinical or laboratory data with a high specificity for SLE (such as the isolated presence of a malar rash, discoid lupus, or anti-native DNA or anti-Sm antibodies) still persists. Furthermore, the differential diagnosis of SLE manifestations is broad and must be adjusted to the patient’s clinical picture, owing to which it should be emphasized that the classificatory elements should only be counted in the absence of a more likely alternative diagnosis. For example, the disease’s articular manifestations may share similarities with rheumatoid arthritis or Sjögren’s syndrome and, on the other hand, its neurological manifestations share similarities with infectious processes, stroke, multiple sclerosis, or the Guillain–Barre syndrome.</p><p id="par0045" class="elsevierStylePara elsevierViewall">The interest of defining classificatory criteria is not only conceptual, but is explained, fundamentally, by the importance of improving the treatment and prognosis of the disease. However, it should be noted that the need to use classificatory criteria also confirms our ignorance about the ethiopathogenesis of the disease and the lack of sensitive and specific diagnostic biomarkers. Although scientific molecular studies (proteomic, genomic, epigenomic, etc.) will change this approach at some point, we do not expect any disruptive changes in the near future. However, we do expect that additional markers, such as, for example, the type I interferon signature or other biomarkers detected in the multiple “omic” studies that are currently underway,<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> may well be added relatively quickly to the current repertoire of classificatory elements. Finally, it is hoped that the team spirit and collegiality that has characterized this effort to generate and validate the EULAR/ACR classification criteria, which has involved several hundreds of “lupologists” from all over the world, will facilitate future international collaborative projects concerning SLE.</p></span>" "pdfFichero" => "main.pdf" "tienePdf" => true "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:17 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Systemic lupus erythematosus" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "R. Furie" 1 => "R. 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