Salivary gland ultrasound: Update | Medicina Clínica (English Edition)

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This lymphocytic infiltrate causes the destruction of the glandular parenchyma and its subsequent fibrosis, resulting in the classic symptoms of dry mouth and dry eyes. According to the last three classification criteria developed<a class="elsevierStyleCrossRefs" href="#bib0005">1–3</a> in patients with negative autoimmunity (negative anti-Ro antibodies), histological confirmation of the lymphocytic infiltrate by a minor salivary gland or parotid gland biopsy is necessary to confirm the diagnosis of SS. Biopsy is a diagnostic tool with acceptable specificity, however, it is invasive and not very sensitive, as well as having variable interobserver reliability.<a class="elsevierStyleCrossRefs" href="#bib0020">4,5</a> On the other hand, salivary gland scintigraphy is used to evaluate glandular function in patients with sicca syndrome and is included in the classification criteria.<a class="elsevierStyleCrossRefs" href="#bib0005">1–3</a> Several studies have evaluated the diagnostic capacity of salivary scintigraphy showing high sensitivity (up to 89% in some studies) but very low specificity (around 50%).<a class="elsevierStyleCrossRef" href="#bib0030">6</a> These data show that salivary scintigraphy is not able to distinguish typical functional anomalies of SS from other causes of sicca syndrome.In this context, for years there has been great interest in the introduction of a diagnostic tool for rapid, sensitive, and non-invasive screening such as salivary gland ultrasound (SGUS), which allows direct visualization of the structural abnormalities caused by the SS's lymphocytic infiltrate.<a class="elsevierStyleCrossRef" href="#bib0035">7</a> Recently, numerous publications have emerged that support its value in the diagnosis of SS, which will possibly allow its inclusion in the classification criteria in the coming years.<a class="elsevierStyleCrossRef" href="#bib0040">8</a>Throughout this manuscript we will review the examination technique, indications, grading, and reliability of SGUS, as well as studies on its correlation with salivary biopsy, correlation with classification criteria, its prognostic value, and its sensitivity to change.Anatomical description and sono-anatomyThe major salivary glands are made up of the parotid, submandibular, and sublingual glands. The parotid glands are the largest salivary glands, attached to the surface of the masseter muscle and anterior to the auditory canal. They can be divided into a superficial portion and a deep portion to the retromandibular vein. The facial nerve runs from posterior to anterior and at mid-height of the parotid gland. The parotid glands drain through the parotid duct (Stensen’s duct) that starts at the anterior part of the gland, crosses the buccinator and ends on the lateral aspect of the mouth near the upper first or second molar. The submandibular glands are found under the body of the mandible, between the two bellies of the digastric muscle, and sometimes there is a deeper glandular bundle that rests on the mylohyoid muscle. It is in contact with the facial artery and vein that run from posterior to anterior, with the facial artery becoming superficial above the body of the mandible near the submandibular gland; sometimes the facial artery can pass through the submandibular gland itself. The submandibular glands drain through the submandibular duct (Wharton's) into the floor of the mouth. Finally, the sublingual glands are located in the anterior part of the mandible, deep to the mylohyoid muscle and drain in the lower part of the mouth under the tongue, through multiple direct communications (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).<elsevierMultimedia ident="fig0005"></elsevierMultimedia>Ultrasound is the ideal imaging technique for evaluating the structure of the major salivary glands, especially the submandibular and parotid glands. The echotexture of the normal glandular parenchyma is homogeneous, well defined, hyperechogenic compared to surrounding tissues (subcutaneous tissue, muscle, and vessels) and comparable with that of the normal thyroid<a class="elsevierStyleCrossRef" href="#bib0045">9</a> (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>). The salivary ducts are not usually visible; however, the presence of lymph nodes is common around both salivary glands and sometimes even intraparotid. Ultrasound shows lymphadenopathies as a round or oval hypoechogenic image with a vascularized hyperechogenic hilum.<elsevierMultimedia ident="fig0010"></elsevierMultimedia>Examination techniqueThe complete ultrasound examination of all four glands takes five to 10 min in total and requires no preparation on the part of the patient. The glands are evaluated with a linear probe in mode B and a frequency range between 8 and 15 MHz, and it is advisable to use frequencies higher than 12 MHz. With the patient in a supine position, the neck hyperextended and rotated to the side opposite the glands examined (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>). Both glands are examined, starting with the submandibular gland below the body of the mandible, both longitudinally and transversely. The longitudinal section of the parotid gland is the most representative, with the probe located anterior to the tragus, on the ramus of the mandible and tilting towards the posterior side to avoid the cortical bone. A representative image or video of each examination should be saved for later controls or comparisons.<a class="elsevierStyleCrossRef" href="#bib0050">10</a> It has been proposed that since SS glandular lesions are symmetrical, one-sided evaluation may be sufficient, however, it is worth doing as it is not too time consuming to perform a full scan of all four glands.<elsevierMultimedia ident="fig0015"></elsevierMultimedia>Caution should be exercised during a Doppler mode assessment, adjusting the parameters to the type of vessel under evaluation. For example, the facial artery, a high-flow vessel, requires a higher pulse repetition frequency (PRF) (generally between 1.2–1.5 MHz) than that used to evaluate tissue inflammation, where there is a prevalence of low-flow vessels. In acute inflammatory processes, an increase in the diffuse Doppler signal can be detected throughout the gland under evaluation, both in the parotid and submandibular glands. However, there is no consensual grading of the Doppler signal for the salivary glands, with low interobserver reliability in the studies that have evaluated it.<a class="elsevierStyleCrossRef" href="#bib0055">11</a>Indications for salivary gland ultrasoundThe main indication for SGUS is the diagnostic evaluation of patients with suspected SS, both primary and secondary, because the ultrasound findings are very specific (> 90%).<a class="elsevierStyleCrossRef" href="#bib0060">12</a> However, these findings are not pathognomonic, and we can find similar lesions in other inflammatory diseases such as sarcoidosis, amyloidosis, and hyper-IgG4 syndrome.Other indications for SGUS are the suspicion of salivary lithiasis, which will show one or multiple hyperechogenic images inside the parenchyma and/or glandular ducts, and the evaluation of acute parotitis, of infectious origin in many cases.<a class="elsevierStyleCrossRef" href="#bib0045">9</a> In parotitis and acute submandibular gland swelling, a diffuse glandular enlargement is observed with an increase in the Doppler signal, also diffuse (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>).In addition, it can be useful in the diagnosis of parotid tumours, and it is necessary to refer to an evaluation by an expert radiologist when we see suspicious images if there is not enough experience.Ultrasound findings and grading scaleThe first articles that described ultrasound lesions present in the salivary glands of patients with SS were published in 1988,<a class="elsevierStyleCrossRefs" href="#bib0065">13,14</a> but it was not until 1992 that De Vita et al.<a class="elsevierStyleCrossRef" href="#bib0075">15</a> published the first study that evaluated the diagnostic capacity of ultrasound in the evaluation of SS, both primary and secondary. Initially, glandular size, homogeneity, and echogenicity of the parenchyma, as well as the visibility of the posterior glandular border were evaluated. The results concluded that an abnormality in parenchymal homogeneity was the parameter that best related to the presence of SS (both primary and secondary), for which they proposed a simple grading scale taking into account only the homogeneity of the parenchyma (0−3 grades for each pair of glands, 0−6 in total).Later in the year 2000 Salaffi et al.<a class="elsevierStyleCrossRef" href="#bib0080">16</a> developed another scale that evaluated each gland from 0 to 4 grades (0−16 in total) according to the homogeneity of the parenchyma, echogenicity, glandular size, and definition of the posterior glandular border. The cut-off point with the best sensitivity and specificity was a score of 8 or higher.Hocevar et al.<a class="elsevierStyleCrossRef" href="#bib0085">17</a> developed a more complex scale in 2005, which independently evaluated five aspects of the gland: Echogenicity of the parenchyma (from 0 to 1), homogeneity (from 0 to 3), the presence and quantity of hypoechogenic areas (from 0 to 3), of hyperechogenic reflexes (from 0 to 3 in the parotid glands and from 0 to 1 in the submandibular glands) and the definition of the glandular borders in the image (from 0 to 3). The total score was 0−48, with 17 or higher being the score with the best sensitivity and specificity to define a gland as SS-compatible.Cornec et al.<a class="elsevierStyleCrossRef" href="#bib0090">18</a> published in 2012 a new scale that only took into account the parenchymal echotexture, grading it from 0−4 for each gland (total score 0−16), considering the presence and size of intraparenchymal hypoechogenic lesions. The definition of each grade is specified below: Grade 0: Homogeneous normal gland; Grade 1: Punctate hypoechogenic areas without hyperechogenic bands; Grade 2: Multiple hypoechogenic areas <2 mm with hyperechogenic bands; Grade 3: Multiple 2−6 mm hypoechogenic areas with hyperechogenic bands; Grade 4: Multiple hypoechogenic areas >6 mm or multiple calcifications with hyperechogenic bands.In 2016, Damjanov et al.<a class="elsevierStyleCrossRef" href="#bib0055">11</a> published the interobserver reliability results of a new grading scale that focused on parenchymal homogeneity and the presence or absence of focal hypoechogenic areas (semi-quantitative grading from 0 to 3 for each gland). Unlike Cornec et al.,<a class="elsevierStyleCrossRef" href="#bib0090">18</a> they did not take into account the size of the hypoechogenic areas. A grading of 2 or more was characteristic of SS.Finally, in 2019 Jousse-Joulin et al. (OMERACT group)<a class="elsevierStyleCrossRef" href="#bib0050">10</a> published a grading scale obtained by consensus among experts which is based on the study by De Vita et al.<a class="elsevierStyleCrossRef" href="#bib0075">15</a> and very similar to that published by Damjanov et al.<a class="elsevierStyleCrossRef" href="#bib0055">11</a> It takes into account parenchymal homogeneity and evaluates each gland from 0 to 3. The definition of each grade is specified below: Grade 0: Normal homogeneous glandular parenchyma; grade I: Minimal glandular heterogeneity without recognizable hypoechogenic images; grade II: Moderate heterogeneity of the parenchyma with hypoechogenic images; grade III: Severe heterogeneity with hypoechogenic lesions occupying the entire glandular parenchyma<a class="elsevierStyleCrossRef" href="#bib0055">11</a> (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>). As an important limitation of this scale, the authors point out that neither the presence of fibrosis nor fat replacement of the gland has been taken into account, with the importance of these aspects not being clear at present.<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> summarizes the grading scales of the salivary glands and their characteristics.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>Intra and interobserver reliabilityIntraobserver reliability has been evaluated in a few studies by reassessing images or videos and the results have always been good or excellent (k: 0.66−0.88).<a class="elsevierStyleCrossRef" href="#bib0055">11</a>Interobserver reliability has been evaluated in many studies, most of them between two observers, with good or excellent results (k: 0.69−0.95).<a class="elsevierStyleCrossRef" href="#bib0055">11</a> The studies with the best results correspond to those that assessed the glands in a dichotomous way (normal or pathological); the rest of the studies include the different grading scales mentioned previously, with similar results among them. Studies that evaluated interobserver reliability with more than two observers also showed good or excellent results (k: 0.66−0.81), including the last study from the OMERACT group that used the previously discussed four-degree grading scale (0−3).Learning about salivary gland ultrasound examination and interpretation can be achieved through a theoretical course of two to three hours and the evaluation of a small number (between five and 10) of healthy controls and patients with SS, obtaining an acceptable interobserver reliability, even in the case of ultrasound users with limited experience<a class="elsevierStyleCrossRef" href="#bib0055">11</a>. However, more studies on SGUS learning are needed.Classification criteriaSGUS has been proposed as a relevant item in future SS classification criteria.<a class="elsevierStyleCrossRefs" href="#bib0090">18–25</a> Evaluation of the structure or function of the salivary glands is done so far with salivary gland sialography and scintigraphy, which involve radiation and are invasive. On the contrary, ultrasound does not require preparation by the patient or administration of contrast, it is cheaper compared to previous examinations, and it is safe because it does not use radiation.The diagnostic capacity of SGUS has been studied by substituting scintigraphy and sialography in the American/European Collaborative Group (AECG) of 2002<a class="elsevierStyleCrossRef" href="#bib0005">1</a> and those of American College of Rheumatology (ACR) 2012<a class="elsevierStyleCrossRef" href="#bib0010">2</a> classification criteria. The correlation between the different classification criteria developed is good<a class="elsevierStyleCrossRefs" href="#bib0110">22,23</a> and its diagnostic capacity remains stable when replacing sialography or scintigraphy for SGUS.<a class="elsevierStyleCrossRefs" href="#bib0095">19,20,23</a>The addition of SGUS in the classification criteria has been evaluated with all the criteria developed (AECG 2002, ACR 2012 and ACR/EULAR 2016), improving to a greater or lesser extent the diagnostic capacity of the criteria (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>).<elsevierMultimedia ident="tbl0010"></elsevierMultimedia>AutoimmunityThe relationship between pathological SGUS and autoantibody-positive results has been described in most of the published studies.<a class="elsevierStyleCrossRefs" href="#bib0035">7,15,24,26</a> This relationship includes all the antibodies present in SS, antinuclear antibodies, rheumatoid factor, anti-Ro, and anti-La antibodies.<a class="elsevierStyleCrossRefs" href="#bib0130">26,27</a> It has also been linked to hypergammaglobulinemia. The positive status of all the antibodies mentioned is related to a higher probability of presenting ultrasound lesions compared to the positive antibody status individually.<a class="elsevierStyleCrossRef" href="#bib0135">27</a> This strong correlation between pathological SGUS and the autoantibody-positive status reinforces the idea that the lesions evidenced by ultrasound are caused by autoimmune inflammatory disease, such as SS.Salivary gland biopsyUltrasound lesions have been associated with the presence of an inflammatory infiltrate in the biopsy of the minor salivary gland (absolute agreement 78.6%) and the parotid gland (absolute agreement 83.3%),<a class="elsevierStyleCrossRef" href="#bib0140">28</a> in addition to a good correlation between the presence of ultrasound lesions and a positive biopsy in several previous studies.<a class="elsevierStyleCrossRefs" href="#bib0110">22,28</a> Having demonstrated the good correlation between SGUS and the different diagnostic tests in SS (sialography, scintigraphy and autoimmunity) together with the invasive nature of the biopsy, it has been proposed that the first diagnostic tests in patients with sicca syndrome should be auto-antibody determination (especially anti-Ro antibody) and SGUS.<a class="elsevierStyleCrossRef" href="#bib0110">22</a> However, since there is no complete agreement, a normal SGUS does not rule out SS, so a salivary gland biopsy is still a useful diagnostic technique in the diagnostic process of patients with suspected SS, especially in those with a normal SGUS.Sensitivity to changeUltrasound lesions appear early in patients with SS and indicate asymptomatic glandular damage throughout the course of the disease until the onset of dryness symptoms. Sensitivity to change in SGUS has been evaluated in patients with a recent diagnosis of SS without finding differences between baseline and 2-year findings.<a class="elsevierStyleCrossRef" href="#bib0145">29</a> Perhaps the time evaluated is too short to be able to detect ultrasound worsening or the four-degree grading scale used in the aforementioned study was not sufficiently sensitive to change.On the other hand, two prospective studies have evaluated the sensitivity to ultrasound change in patients with pSS treated with rituximab at six and 12 months.<a class="elsevierStyleCrossRefs" href="#bib0150">30,31</a> The French study (within the TEARS clinical trial)<a class="elsevierStyleCrossRef" href="#bib0150">30</a> included patients from a single center which evaluated and graded each salivary gland, from 0 to 12 as previously mentioned, at baseline and at six months. At the end of follow-up, they found an improvement of 1 grade on average in patients treated with rituximab compared to those treated with placebo.The English Study (TRACTISS)<a class="elsevierStyleCrossRef" href="#bib0155">31</a> also graded various gland components in a similar way to the French study at baseline and at 12 months, finding an improvement of 1 point in patients treated with rituximab. The improvement corresponded to the better definition of the posterior glandular border, a finding with low interobserver agreement.The small sample of patients included in both studies (28 and 56 patients, respectively), the fact the TEARS study is single-centre and the unreliability of the evaluation of the posterior glandular border on which the improvement in the TRACTISS study depends, in addition to the short follow-up time (maximum 12 months), means that more studies are needed to confirm the appropriate sensitivity to change in the ultrasound findings.Prognostic valueThe association that some authors have found between ultrasound salivary gland lesions and lymphomas or cryoglobulinemic vasculitis, suggests a possible prognostic factor for SGUS. The higher frequency of extra-glandular manifestations and the higher mean ESSDAI in patients with pathological SGUS compared to patients with normal ultrasound have been published in several studies.<a class="elsevierStyleCrossRef" href="#bib0160">32</a>Although the possible role of ultrasound in detecting patients with a worse prognosis (greater risk of extra-glandular manifestations and lymphoma, mainly) is promising for the moment, the scientific evidence remains insufficient to confirm this.ConclusionsSGUS is a safe, inexpensive, highly available, reproducible, and easy-to-learn test that provides reliable information on the glandular structure. Glandular heterogeneity is the most important finding related to the diagnosis of SS, and the most accepted classification divides abnormalities of the glandular parenchyma into four grades (from 0 to 3). Ultrasound has shown a good correlation with autoimmunity and glandular biopsy, but its sensitivity to change and its relationship with extra-glandular manifestations has yet to be determined. Scientific evidence regarding the validity and reliability of salivary gland ultrasound has increased substantially in recent years, and its inclusion in future SS classification criteria is likely.FundingThe authors have not received any funding for the conduct and publication of this review.Conflict of interestsThe authors declare no conflict of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:16 [ 0 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "sec0010" "titulo" => "Anatomical description and sono-anatomy" ] 2 => array:2 [ "identificador" => "sec0015" "titulo" => "Examination technique" ] 3 => array:2 [ "identificador" => "sec0020" "titulo" => "Indications for salivary gland ultrasound" ] 4 => array:2 [ "identificador" => "sec0025" "titulo" => "Ultrasound findings and grading scale" ] 5 => array:2 [ "identificador" => "sec0030" "titulo" => "Intra and interobserver reliability" ] 6 => array:2 [ "identificador" => "sec0035" "titulo" => "Classification criteria" ] 7 => array:2 [ "identificador" => "sec0040" "titulo" => "Autoimmunity" ] 8 => array:2 [ "identificador" => "sec0045" "titulo" => "Salivary gland biopsy" ] 9 => array:2 [ "identificador" => "sec0050" "titulo" => "Sensitivity to change" ] 10 => array:2 [ "identificador" => "sec0055" "titulo" => "Prognostic value" ] 11 => array:2 [ "identificador" => "sec0060" "titulo" => "Conclusions" ] 12 => array:2 [ "identificador" => "sec0065" "titulo" => "Funding" ] 13 => array:2 [ "identificador" => "sec0070" "titulo" => "Conflict of interests" ] 14 => array:2 [ "identificador" => "xack515633" "titulo" => "Acknowledgement" ] 15 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2020-02-07" "fechaAceptado" => "2020-03-16" "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "Please cite this article as: Nieto-González JC, Serrano Benavente B, Molina Collada J. Ecografía de glándulas salivales: puesta al día. Med Clin (Barc). 2021;156:81–87." ] ] "multimedia" => array:5 [ 0 => array:8 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1605 "Ancho" => 2175 "Tamanyo" => 423205 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0005" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "Head and neck anatomy showing the salivary glands and their relationship with vessels and nerves." ] ] 1 => array:8 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 4341 "Ancho" => 2506 "Tamanyo" => 1206055 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0010" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "Examples of normal ultrasound (grade 0), pathological ultrasound (grades I, II and III) and example of infectious parotitis." ] ] 2 => array:8 [ "identificador" => "fig0015" "etiqueta" => "Fig. 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 1414 "Ancho" => 1505 "Tamanyo" => 191686 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0015" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "Ultrasound examination of major salivary glands. Right submandibular gland in longitudinal section (a) and in cross section (b). Parotid gland in longitudinal section (c) and in cross section (d)." ] ] 3 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0020" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Author and year \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">De Vita et al.<a class="elsevierStyleCrossRef" href="#bib0075">15</a>1992 \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Salaffi et al.<a class="elsevierStyleCrossRef" href="#bib0080">16</a>2000 \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Hocevar et al.<a class="elsevierStyleCrossRef" href="#bib0085">17</a>2005 \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Cornec et al.<a class="elsevierStyleCrossRef" href="#bib0090">18</a>2013 \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Damjanov et al.<a class="elsevierStyleCrossRef" href="#bib0055">11</a>2016 \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Jousse-Joulin et al.<a class="elsevierStyleCrossRef" href="#bib0050">10</a>2019 \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Total and per gland grading \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0−6 total (0−3 for each glandular pair) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0−16 total (0−4 for each gland) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0−48 total (maximum score for the parotids 13 points and for the submandibular 11 points) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0−16 total (0−4 for each gland) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0−3 each glandSemi-quantitative scale \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0−3 each glandSemi-quantitative scale \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Glandular aspects evaluated \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Glandular homogeneity (according to the presence and number of hypoechogenic areas; also consider the presence of linear densities, cysts, or calcifications) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EchogenicityParenchymal homogeneity (presence or absence of hypoechogenic areas and their size, calcifications, and echogenic bands)Glandular size.Definition of the posterior glandular border \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">EchogenicityHomogeneityPresence and quantity of hypoechogenic areas.Presence of hyperechogenic reflexes.Definition of the glandular borders \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Parenchymal echotexture (according to presence and size of hypoechogenic areas) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Parenchymal homogeneity and presence or absence of hypoechogenic areas.It does not evaluate glandular size. \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Parenchymal homogeneity and presence or absence of hypoechogenic areas.Does not take glandular size into account \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab2532256.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Salivary gland ultrasound lesion grading scales." ] ] 4 => array:8 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0025" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "SGUS: salivary gland ultrasound." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Classification criteria \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Classification criteria (sensitivity/specificity) \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Classification criteria + SGUS (sensitivity/specificity) \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Cornec et al.<a class="elsevierStyleCrossRef" href="#bib0090">18</a> 2013 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2002 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">77.7%/98.7% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">85.7%/96.1% \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Cornec et al.<a class="elsevierStyleCrossRef" href="#bib0120">24</a> 2014 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2012 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">64.4%/91.1% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">84.4%/89.3% \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Le Goff et al. <a class="elsevierStyleCrossRef" href="#bib0115">23</a> 2017 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2002 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">82.2%/98.1% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">– \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2016 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">87.4%/95.4% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">91.1%/93.8% \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Takagi et al. <a class="elsevierStyleCrossRef" href="#bib0125">25</a> 2018 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2016 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">85%/64% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">95%/86% \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Mossel et al.<a class="elsevierStyleCrossRef" href="#bib0110">22</a> 2017 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2016 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">95.9%/92.2% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">97.3%/90.2% \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab2532255.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Diagnostic capacity of the classification criteria when replacing or adding SGUS." ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:32 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Classification criteria for Sjögren’s syndrome: a revised version of the European criteria proposed by the American-European Consensus Group" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "C. 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Salivary gland ultrasound: Update

Ecografía de glándulas salivales: puesta al día

Juan Carlos Nieto-González

Corresponding author

juancarlos.nietog@gmail.com

Corresponding author.

, Belén Serrano Benavente, Juan Molina Collada

Servicio de Reumatología, Hospital General Universitario Gregorio Marañón, Madrid, Spain

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    "titulo" => "Salivary gland ultrasound&#58; Update"
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        "autoresLista" => "Juan Carlos Nieto-Gonz&#225;lez, Bel&#233;n Serrano Benavente, Juan Molina Collada"
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          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Examples of normal ultrasound &#40;grade 0&#41;&#44; pathological ultrasound &#40;grades I&#44; II and III&#41; and example of infectious parotitis&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Primary Sj&#246;gren&#39;s syndrome &#40;pSS&#41; is a chronic autoimmune disease caused by a lymphocytic dysregulation that infiltrates exocrine glands&#44; mainly the salivary and lacrimal glands&#46; This lymphocytic infiltrate causes the destruction of the glandular parenchyma and its subsequent fibrosis&#44; resulting in the classic symptoms of dry mouth and dry eyes&#46; According to the last three classification criteria developed<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#8211;3</span></a> in patients with negative autoimmunity &#40;negative anti-Ro antibodies&#41;&#44; histological confirmation of the lymphocytic infiltrate by a minor salivary gland or parotid gland biopsy is necessary to confirm the diagnosis of SS&#46; Biopsy is a diagnostic tool with acceptable specificity&#44; however&#44; it is invasive and not very sensitive&#44; as well as having variable interobserver reliability&#46;<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4&#44;5</span></a> On the other hand&#44; salivary gland scintigraphy is used to evaluate glandular function in patients with sicca syndrome and is included in the classification criteria&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#8211;3</span></a> Several studies have evaluated the diagnostic capacity of salivary scintigraphy showing high sensitivity &#40;up to 89&#37; in some studies&#41; but very low specificity &#40;around 50&#37;&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> These data show that salivary scintigraphy is not able to distinguish typical functional anomalies of SS from other causes of sicca syndrome&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">In this context&#44; for years there has been great interest in the introduction of a diagnostic tool for rapid&#44; sensitive&#44; and non-invasive screening such as salivary gland ultrasound &#40;SGUS&#41;&#44; which allows direct visualization of the structural abnormalities caused by the SS&#39;s lymphocytic infiltrate&#46;<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> Recently&#44; numerous publications have emerged that support its value in the diagnosis of SS&#44; which will possibly allow its inclusion in the classification criteria in the coming years&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Throughout this manuscript we will review the examination technique&#44; indications&#44; grading&#44; and reliability of SGUS&#44; as well as studies on its correlation with salivary biopsy&#44; correlation with classification criteria&#44; its prognostic value&#44; and its sensitivity to change&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Anatomical description and sono-anatomy</span><p id="par0020" class="elsevierStylePara elsevierViewall">The major salivary glands are made up of the parotid&#44; submandibular&#44; and sublingual glands&#46; The parotid glands are the largest salivary glands&#44; attached to the surface of the masseter muscle and anterior to the auditory canal&#46; They can be divided into a superficial portion and a deep portion to the retromandibular vein&#46; The facial nerve runs from posterior to anterior and at mid-height of the parotid gland&#46; The parotid glands drain through the parotid duct &#40;Stensen&#8217;s duct&#41; that starts at the anterior part of the gland&#44; crosses the buccinator and ends on the lateral aspect of the mouth near the upper first or second molar&#46; The submandibular glands are found under the body of the mandible&#44; between the two bellies of the digastric muscle&#44; and sometimes there is a deeper glandular bundle that rests on the mylohyoid muscle&#46; It is in contact with the facial artery and vein that run from posterior to anterior&#44; with the facial artery becoming superficial above the body of the mandible near the submandibular gland&#59; sometimes the facial artery can pass through the submandibular gland itself&#46; The submandibular glands drain through the submandibular duct &#40;Wharton&#39;s&#41; into the floor of the mouth&#46; Finally&#44; the sublingual glands are located in the anterior part of the mandible&#44; deep to the mylohyoid muscle and drain in the lower part of the mouth under the tongue&#44; through multiple direct communications &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">Ultrasound is the ideal imaging technique for evaluating the structure of the major salivary glands&#44; especially the submandibular and parotid glands&#46; The echotexture of the normal glandular parenchyma is homogeneous&#44; well defined&#44; hyperechogenic compared to surrounding tissues &#40;subcutaneous tissue&#44; muscle&#44; and vessels&#41; and comparable with that of the normal thyroid<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; The salivary ducts are not usually visible&#59; however&#44; the presence of lymph nodes is common around both salivary glands and sometimes even intraparotid&#46; Ultrasound shows lymphadenopathies as a round or oval hypoechogenic image with a vascularized hyperechogenic <span class="elsevierStyleItalic">hilum</span>&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Examination technique</span><p id="par0030" class="elsevierStylePara elsevierViewall">The complete ultrasound examination of all four glands takes five to 10&#8239;min in total and requires no preparation on the part of the patient&#46; The glands are evaluated with a linear probe in mode B and a frequency range between 8 and 15&#8239;MHz&#44; and it is advisable to use frequencies higher than 12&#8239;MHz&#46; With the patient in a supine position&#44; the neck hyperextended and rotated to the side opposite the glands examined &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; Both glands are examined&#44; starting with the submandibular gland below the body of the mandible&#44; both longitudinally and transversely&#46; The longitudinal section of the parotid gland is the most representative&#44; with the probe located anterior to the tragus&#44; on the ramus of the mandible and tilting towards the posterior side to avoid the cortical bone&#46; A representative image or video of each examination should be saved for later controls or comparisons&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> It has been proposed that since SS glandular lesions are symmetrical&#44; one-sided evaluation may be sufficient&#44; however&#44; it is worth doing as it is not too time consuming to perform a full scan of all four glands&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0035" class="elsevierStylePara elsevierViewall">Caution should be exercised during a Doppler mode assessment&#44; adjusting the parameters to the type of vessel under evaluation&#46; For example&#44; the facial artery&#44; a high-flow vessel&#44; requires a higher <span class="elsevierStyleItalic">pulse repetition frequency</span> &#40;PRF&#41; &#40;generally between 1&#46;2&#8211;1&#46;5&#8239;MHz&#41; than that used to evaluate tissue inflammation&#44; where there is a prevalence of low-flow vessels&#46; In acute inflammatory processes&#44; an increase in the diffuse Doppler signal can be detected throughout the gland under evaluation&#44; both in the parotid and submandibular glands&#46; However&#44; there is no consensual grading of the Doppler signal for the salivary glands&#44; with low interobserver reliability in the studies that have evaluated it&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Indications for salivary gland ultrasound</span><p id="par0040" class="elsevierStylePara elsevierViewall">The main indication for SGUS is the diagnostic evaluation of patients with suspected SS&#44; both primary and secondary&#44; because the ultrasound findings are very specific &#40;&#62; 90&#37;&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> However&#44; these findings are not pathognomonic&#44; and we can find similar lesions in other inflammatory diseases such as sarcoidosis&#44; amyloidosis&#44; and hyper-IgG4 syndrome&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">Other indications for SGUS are the suspicion of salivary lithiasis&#44; which will show one or multiple hyperechogenic images inside the parenchyma and&#47;or glandular ducts&#44; and the evaluation of acute parotitis&#44; of infectious origin in many cases&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> In parotitis and acute submandibular gland swelling&#44; a diffuse glandular enlargement is observed with an increase in the Doppler signal&#44; also diffuse &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">In addition&#44; it can be useful in the diagnosis of parotid tumours&#44; and it is necessary to refer to an evaluation by an expert radiologist when we see suspicious images if there is not enough experience&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Ultrasound findings and grading scale</span><p id="par0055" class="elsevierStylePara elsevierViewall">The first articles that described ultrasound lesions present in the salivary glands of patients with SS were published in 1988&#44;<a class="elsevierStyleCrossRefs" href="#bib0065"><span class="elsevierStyleSup">13&#44;14</span></a> but it was not until 1992 that De Vita et al&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> published the first study that evaluated the diagnostic capacity of ultrasound in the evaluation of SS&#44; both primary and secondary&#46; Initially&#44; glandular size&#44; homogeneity&#44; and echogenicity of the parenchyma&#44; as well as the visibility of the posterior glandular border were evaluated&#46; The results concluded that an abnormality in parenchymal homogeneity was the parameter that best related to the presence of SS &#40;both primary and secondary&#41;&#44; for which they proposed a simple grading scale taking into account only the homogeneity of the parenchyma &#40;0&#8722;3 grades for each pair of glands&#44; 0&#8722;6 in total&#41;&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">Later in the year 2000 Salaffi et al&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> developed another scale that evaluated each gland from 0 to 4 grades &#40;0&#8722;16 in total&#41; according to the homogeneity of the parenchyma&#44; echogenicity&#44; glandular size&#44; and definition of the posterior glandular border&#46; The cut-off point with the best sensitivity and specificity was a score of 8 or higher&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Hocevar et al&#46;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> developed a more complex scale in 2005&#44; which independently evaluated five aspects of the gland&#58; Echogenicity of the parenchyma &#40;from 0 to 1&#41;&#44; homogeneity &#40;from 0 to 3&#41;&#44; the presence and quantity of hypoechogenic areas &#40;from 0 to 3&#41;&#44; of hyperechogenic reflexes &#40;from 0 to 3 in the parotid glands and from 0 to 1 in the submandibular glands&#41; and the definition of the glandular borders in the image &#40;from 0 to 3&#41;&#46; The total score was 0&#8722;48&#44; with 17 or higher being the score with the best sensitivity and specificity to define a gland as SS-compatible&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">Cornec et al&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> published in 2012 a new scale that only took into account the parenchymal echotexture&#44; grading it from 0&#8722;4 for each gland &#40;total score 0&#8722;16&#41;&#44; considering the presence and size of intraparenchymal hypoechogenic lesions&#46; The definition of each grade is specified below&#58; Grade 0&#58; Homogeneous normal gland&#59; Grade 1&#58; Punctate hypoechogenic areas without hyperechogenic bands&#59; Grade 2&#58; Multiple hypoechogenic areas &#60;2&#8239;mm with hyperechogenic bands&#59; Grade 3&#58; Multiple 2&#8722;6&#8239;mm hypoechogenic areas with hyperechogenic bands&#59; Grade 4&#58; Multiple hypoechogenic areas &#62;6&#8239;mm or multiple calcifications with hyperechogenic bands&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">In 2016&#44; Damjanov et al&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> published the interobserver reliability results of a new grading scale that focused on parenchymal homogeneity and the presence or absence of focal hypoechogenic areas &#40;semi-quantitative grading from 0 to 3 for each gland&#41;&#46; Unlike Cornec et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> they did not take into account the size of the hypoechogenic areas&#46; A grading of 2 or more was characteristic of SS&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Finally&#44; in 2019 Jousse-Joulin et al&#46; &#40;OMERACT group&#41;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> published a grading scale obtained by consensus among experts which is based on the study by De Vita et al&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> and very similar to that published by Damjanov et al&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> It takes into account parenchymal homogeneity and evaluates each gland from 0 to 3&#46; The definition of each grade is specified below&#58; Grade 0&#58; Normal homogeneous glandular parenchyma&#59; grade I<span class="elsevierStyleSmallCaps">&#58;</span> Minimal glandular heterogeneity without recognizable hypoechogenic images&#59; grade II<span class="elsevierStyleSmallCaps">&#58;</span> Moderate heterogeneity of the parenchyma with hypoechogenic images&#59; grade III<span class="elsevierStyleSmallCaps">&#58;</span> Severe heterogeneity with hypoechogenic lesions occupying the entire glandular parenchyma<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; As an important limitation of this scale&#44; the authors point out that neither the presence of fibrosis nor fat replacement of the gland has been taken into account&#44; with the importance of these aspects not being clear at present&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> summarizes the grading scales of the salivary glands and their characteristics&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Intra and interobserver reliability</span><p id="par0090" class="elsevierStylePara elsevierViewall">Intraobserver reliability has been evaluated in a few studies by reassessing images or videos and the results have always been good or excellent &#40;k&#58; 0&#46;66&#8722;0&#46;88&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">Interobserver reliability has been evaluated in many studies&#44; most of them between two observers&#44; with good or excellent results &#40;k&#58; 0&#46;69&#8722;0&#46;95&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> The studies with the best results correspond to those that assessed the glands in a dichotomous way &#40;normal or pathological&#41;&#59; the rest of the studies include the different grading scales mentioned previously&#44; with similar results among them&#46; Studies that evaluated interobserver reliability with more than two observers also showed good or excellent results &#40;k&#58; 0&#46;66&#8722;0&#46;81&#41;&#44; including the last study from the OMERACT group that used the previously discussed four-degree grading scale &#40;0&#8722;3&#41;&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">Learning about salivary gland ultrasound examination and interpretation can be achieved through a theoretical course of two to three hours and the evaluation of a small number &#40;between five and 10&#41; of healthy controls and patients with SS&#44; obtaining an acceptable interobserver reliability&#44; even in the case of ultrasound users with limited experience<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a>&#46; However&#44; more studies on SGUS learning are needed&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Classification criteria</span><p id="par0105" class="elsevierStylePara elsevierViewall">SGUS has been proposed as a relevant item in future SS classification criteria&#46;<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">18&#8211;25</span></a> Evaluation of the structure or function of the salivary glands is done so far with salivary gland sialography and scintigraphy&#44; which involve radiation and are invasive&#46; On the contrary&#44; ultrasound does not require preparation by the patient or administration of contrast&#44; it is cheaper compared to previous examinations&#44; and it is safe because it does not use radiation&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">The diagnostic capacity of SGUS has been studied by substituting scintigraphy and sialography in the <span class="elsevierStyleItalic">American&#47;European Collaborative Group</span> &#40;AECG&#41; of 2002<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> and those of <span class="elsevierStyleItalic">American College of Rheumatology</span> &#40;ACR&#41; 2012<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> classification criteria&#46; The correlation between the different classification criteria developed is good<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">22&#44;23</span></a> and its diagnostic capacity remains stable when replacing sialography or scintigraphy for SGUS&#46;<a class="elsevierStyleCrossRefs" href="#bib0095"><span class="elsevierStyleSup">19&#44;20&#44;23</span></a></p><p id="par0115" class="elsevierStylePara elsevierViewall">The addition of SGUS in the classification criteria has been evaluated with all the criteria developed &#40;AECG 2002&#44; ACR 2012 and ACR&#47;EULAR 2016&#41;&#44; improving to a greater or lesser extent the diagnostic capacity of the criteria &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Autoimmunity</span><p id="par0120" class="elsevierStylePara elsevierViewall">The relationship between pathological SGUS and autoantibody-positive results has been described in most of the published studies&#46;<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7&#44;15&#44;24&#44;26</span></a> This relationship includes all the antibodies present in SS&#44; antinuclear antibodies&#44; rheumatoid factor&#44; anti-Ro&#44; and anti-La antibodies&#46;<a class="elsevierStyleCrossRefs" href="#bib0130"><span class="elsevierStyleSup">26&#44;27</span></a> It has also been linked to hypergammaglobulinemia&#46; The positive status of all the antibodies mentioned is related to a higher probability of presenting ultrasound lesions compared to the positive antibody status individually&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a> This strong correlation between pathological SGUS and the autoantibody-positive status reinforces the idea that the lesions evidenced by ultrasound are caused by autoimmune inflammatory disease&#44; such as SS&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Salivary gland biopsy</span><p id="par0125" class="elsevierStylePara elsevierViewall">Ultrasound lesions have been associated with the presence of an inflammatory infiltrate in the biopsy of the minor salivary gland &#40;absolute agreement 78&#46;6&#37;&#41; and the parotid gland &#40;absolute agreement 83&#46;3&#37;&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a> in addition to a good correlation between the presence of ultrasound lesions and a positive biopsy in several previous studies&#46;<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">22&#44;28</span></a> Having demonstrated the good correlation between SGUS and the different diagnostic tests in SS &#40;sialography&#44; scintigraphy and autoimmunity&#41; together with the invasive nature of the biopsy&#44; it has been proposed that the first diagnostic tests in patients with sicca syndrome should be auto-antibody determination &#40;especially anti-Ro antibody&#41; and SGUS&#46;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> However&#44; since there is no complete agreement&#44; a normal SGUS does not rule out SS&#44; so a salivary gland biopsy is still a useful diagnostic technique in the diagnostic process of patients with suspected SS&#44; especially in those with a normal SGUS&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Sensitivity to change</span><p id="par0130" class="elsevierStylePara elsevierViewall">Ultrasound lesions appear early in patients with SS and indicate asymptomatic glandular damage throughout the course of the disease until the onset of dryness symptoms&#46; Sensitivity to change in SGUS has been evaluated in patients with a recent diagnosis of SS without finding differences between baseline and 2-year findings&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a> Perhaps the time evaluated is too short to be able to detect ultrasound worsening or the four-degree grading scale used in the aforementioned study was not sufficiently sensitive to change&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">On the other hand&#44; two prospective studies have evaluated the sensitivity to ultrasound change in patients with pSS treated with rituximab at six and 12 months&#46;<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">30&#44;31</span></a> The French study &#40;within the TEARS clinical trial&#41;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a> included patients from a single center which evaluated and graded each salivary gland&#44; from 0 to 12 as previously mentioned&#44; at baseline and at six months&#46; At the end of follow-up&#44; they found an improvement of 1 grade on average in patients treated with rituximab compared to those treated with placebo&#46;</p><p id="par0140" class="elsevierStylePara elsevierViewall">The English Study &#40;TRACTISS&#41;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> also graded various gland components in a similar way to the French study at baseline and at 12 months&#44; finding an improvement of 1 point in patients treated with rituximab&#46; The improvement corresponded to the better definition of the posterior glandular border&#44; a finding with low interobserver agreement&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">The small sample of patients included in both studies &#40;28 and 56 patients&#44; respectively&#41;&#44; the fact the TEARS study is single-centre and the unreliability of the evaluation of the posterior glandular border on which the improvement in the TRACTISS study depends&#44; in addition to the short follow-up time &#40;maximum 12 months&#41;&#44; means that more studies are needed to confirm the appropriate sensitivity to change in the ultrasound findings&#46;</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Prognostic value</span><p id="par0150" class="elsevierStylePara elsevierViewall">The association that some authors have found between ultrasound salivary gland lesions and lymphomas or cryoglobulinemic vasculitis&#44; suggests a possible prognostic factor for SGUS&#46; The higher frequency of extra-glandular manifestations and the higher mean ESSDAI in patients with pathological SGUS compared to patients with normal ultrasound have been published in several studies&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">32</span></a></p><p id="par0155" class="elsevierStylePara elsevierViewall">Although the possible role of ultrasound in detecting patients with a worse prognosis &#40;greater risk of extra-glandular manifestations and lymphoma&#44; mainly&#41; is promising for the moment&#44; the scientific evidence remains insufficient to confirm this&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Conclusions</span><p id="par0160" class="elsevierStylePara elsevierViewall">SGUS is a safe&#44; inexpensive&#44; highly available&#44; reproducible&#44; and easy-to-learn test that provides reliable information on the glandular structure&#46; Glandular heterogeneity is the most important finding related to the diagnosis of SS&#44; and the most accepted classification divides abnormalities of the glandular parenchyma into four grades &#40;from 0 to 3&#41;&#46; Ultrasound has shown a good correlation with autoimmunity and glandular biopsy&#44; but its sensitivity to change and its relationship with extra-glandular manifestations has yet to be determined&#46; Scientific evidence regarding the validity and reliability of salivary gland ultrasound has increased substantially in recent years&#44; and its inclusion in future SS classification criteria is likely&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Funding</span><p id="par0165" class="elsevierStylePara elsevierViewall">The authors have not received any funding for the conduct and publication of this review&#46;</p></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Conflict of interests</span><p id="par0170" class="elsevierStylePara elsevierViewall">The authors declare no conflict of interest&#46;</p></span></span>"
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          "titulo" => "Anatomical description and sono-anatomy"
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        2 => array:2 [
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          "titulo" => "Indications for salivary gland ultrasound"
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        4 => array:2 [
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Nieto-Gonz&#225;lez JC&#44; Serrano Benavente B&#44; Molina Collada J&#46; Ecograf&#237;a de gl&#225;ndulas salivales&#58; puesta al d&#237;a&#46; Med Clin &#40;Barc&#41;&#46; 2021&#59;156&#58;81&#8211;87&#46;</p>"
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          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Examples of normal ultrasound &#40;grade 0&#41;&#44; pathological ultrasound &#40;grades I&#44; II and III&#41; and example of infectious parotitis&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Author and year&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">De Vita et al&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a>1992&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Salaffi et al&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a>2000&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Hocevar et al&#46;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a>2005&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Cornec et al&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a>2013&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Damjanov et al&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a>2016&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Jousse-Joulin et al&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a>2019&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Total and per gland grading&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#8722;6 total &#40;0&#8722;3 for each glandular pair&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#8722;16 total &#40;0&#8722;4 for each gland&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">0&#8722;48 total &#40;maximum score for the parotids 13 points and for the submandibular 11 points&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#8722;16 total &#40;0&#8722;4 for each gland&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#8722;3 each glandSemi-quantitative scale&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#8722;3 each glandSemi-quantitative scale&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">Glandular aspects evaluated&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Glandular homogeneity &#40;according to the presence and number of hypoechogenic areas&#59; also consider the presence of linear densities&#44; cysts&#44; or calcifications&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">EchogenicityParenchymal homogeneity &#40;presence or absence of hypoechogenic areas and their size&#44; calcifications&#44; and echogenic bands&#41;Glandular size&#46;Definition of the posterior glandular border&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">EchogenicityHomogeneityPresence and quantity of hypoechogenic areas&#46;Presence of hyperechogenic reflexes&#46;Definition of the glandular borders&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Parenchymal echotexture &#40;according to presence and size of hypoechogenic areas&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Parenchymal homogeneity and presence or absence of hypoechogenic areas&#46;It does not evaluate glandular size&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Parenchymal homogeneity and presence or absence of hypoechogenic areas&#46;Does not take glandular size into account&nbsp;\t\t\t\t\t\t\n
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          "leyenda" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">SGUS&#58; salivary gland ultrasound&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Classification criteria&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Classification criteria &#40;sensitivity&#47;specificity&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Classification criteria&#8239;&#43;&#8239;SGUS &#40;sensitivity&#47;specificity&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
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                  \t\t\t\t">Cornec et al&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> 2013&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">2002&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">77&#46;7&#37;&#47;98&#46;7&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">85&#46;7&#37;&#47;96&#46;1&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Cornec et al&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">24</span></a> 2014&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2012&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">64&#46;4&#37;&#47;91&#46;1&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">84&#46;4&#37;&#47;89&#46;3&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Le Goff et al&#46; <a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> 2017&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">2002&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t">82&#46;2&#37;&#47;98&#46;1&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2016&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">87&#46;4&#37;&#47;95&#46;4&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">91&#46;1&#37;&#47;93&#46;8&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Takagi et al&#46; <a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> 2018&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">2016&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">85&#37;&#47;64&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">95&#37;&#47;86&#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Mossel et al&#46;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> 2017&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">2016&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">95&#46;9&#37;&#47;92&#46;2&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t">97&#46;3&#37;&#47;90&#46;2&#37;&nbsp;\t\t\t\t\t\t\n
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