Salivary gland ultrasound: Update

Nieto-González, Juan Carlos; Serrano Benavente, Belén; Molina Collada, Juan
doi:10.1016/j.medcle.2020.03.010
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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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                  \t\t\t\t\tvoid\n
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                  \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
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                  \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
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                  \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
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                  \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
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                  \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
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                  \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
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                  \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
                  \t\t\t\t\ttop\n
                  \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
                  \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&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
                  \t\t\t\t  " align="left" valign="\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
                  \t\t\t\t\ttop\n
                  \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
                  \t\t\t\t\ttop\n
                  \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
                  \t\t\t\t\ttop\n
                  \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
                  \t\t\t\t</td></tr></tbody></table>
                  """
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                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">&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">Classification criteria&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 &#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
                  \t\t\t\t\ttop\n
                  \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
                  \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="#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
                  \t\t\t\t\ttop\n
                  \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
                  \t\t\t\t\ttop\n
                  \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">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
                  \t\t\t\t\ttop\n
                  \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
                  \t\t\t\t\ttop\n
                  \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
                  \t\t\t\t\ttop\n
                  \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
                  \t\t\t\t\ttop\n
                  \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
                  \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
                  \t\t\t\t\ttop\n
                  \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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">95&#37;&#47;86&#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">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
                  \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
                  \t\t\t\t\ttop\n
                  \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
                  \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&#46;3&#37;&#47;90&#46;2&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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            0 => array:3 [
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                  "contribucion" => array:1 [
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                      "titulo" => "Classification criteria for Sj&#246;gren&#8217;s syndrome&#58; a revised version of the European criteria proposed by the American-European Consensus Group"
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                            0 => "C&#46; Vitali"
                            1 => "S&#46; Bombardieri"
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                            5 => "S&#46;E&#46; Carsons"
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                    0 => array:2 [
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                        "link" => array:1 [
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                            0 => "S&#46;C&#46; Shiboski"
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                0 => array:2 [
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                        "tituloSerie" => "J Clin Pathol&#46;"
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                      "titulo" => "Italian Study Group on Sj&#246;gren&#8217;s Syndrome of the Italian Society of Rheumatology&#46; Minor salivary gland biopsy and Sj&#246;gren&#8217;s syndrome&#58; comparative analysis of biopsies among different Italian rheumatologic centers"
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