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Elastography in Dermatology
Elastografía en dermatología
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Alfageme Roldán" "autores" => array:1 [ 0 => array:2 [ "nombre" => "F." 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Parte II: mutilación genital, escrofulodermia, sarna, erisipela y los males del Rey Alfonso" ] ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 637 "Ancho" => 999 "Tamanyo" => 255879 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Illustration of Charles II of England extending the royal touch. This king is estimated to have performed the ceremony with some 92<span class="elsevierStyleHsp" style=""></span>000 patients with scrofula over the course of his reign. Engraving by Robert White (1864). The image, in the public domain, is available from <span class="elsevierStyleInterRef" id="intr0005" href="https://en.wikipedia.org/wiki/royal_touch">https://en.wikipedia.org/wiki/royal_touch</span>.</p>" ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "J. Romaní, X. Sierra, A. Casson" "autores" => array:3 [ 0 => array:2 [ "nombre" => "J." "apellidos" => "Romaní" ] 1 => array:2 [ "nombre" => "X." "apellidos" => "Sierra" ] 2 => array:2 [ "nombre" => "A." "apellidos" => "Casson" ] ] ] ] ] "idiomaDefecto" => "en" "Traduccion" => array:1 [ "es" => array:9 [ "pii" => "S0001731016300448" "doi" => "10.1016/j.ad.2016.02.014" "estado" => "S300" "subdocumento" => "" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:1 [ "total" => 0 ] "idiomaDefecto" => "es" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0001731016300448?idApp=UINPBA000044" ] ] "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1578219016301676?idApp=UINPBA000044" "url" => "/15782190/0000010700000008/v2_201704100057/S1578219016301676/v2_201704100057/en/main.assets" ] "itemAnterior" => array:19 [ "pii" => "S1578219016301652" "issn" => "15782190" "doi" => "10.1016/j.adengl.2016.07.011" "estado" => "S300" "fechaPublicacion" => "2016-10-01" "aid" => "1433" "copyright" => "Elsevier España, S.L.U. and AEDV" "documento" => "article" "crossmark" => 1 "subdocumento" => "ssu" "cita" => "Actas Dermosifiliogr. 2016;107:640-51" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 1971 "formatos" => array:3 [ "EPUB" => 58 "HTML" => 1377 "PDF" => 536 ] ] "en" => array:13 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">Review</span>" "titulo" => "Cutaneous Pseudolymphomas" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => array:2 [ 0 => "en" 1 => "es" ] "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "640" "paginaFinal" => "651" ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Pseudolinfomas cutáneos" ] ] "contieneResumen" => array:2 [ "en" => true "es" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0020" "etiqueta" => "Figure 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 746 "Ancho" => 998 "Tamanyo" => 417904 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Histologic image of the lymphocytoma cutis shown in <a class="elsevierStyleCrossRef" href="#fig0015">Figure 3</a>. Dense mixed dermal infiltrate. Note the merging germinal centers devoid of the mantel zone, simulating a B-cell lymphoma (hematoxylin-eosin, original magnification ×<span class="elsevierStyleHsp" style=""></span>20).</p>" ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "D. Romero-Pérez, M. Blanes Martínez, B. Encabo-Durán" "autores" => array:3 [ 0 => array:2 [ "nombre" => "D." "apellidos" => "Romero-Pérez" ] 1 => array:2 [ "nombre" => "M." "apellidos" => "Blanes Martínez" ] 2 => array:2 [ "nombre" => "B." "apellidos" => "Encabo-Durán" ] ] ] ] ] "idiomaDefecto" => "en" "Traduccion" => array:1 [ "es" => array:9 [ "pii" => "S0001731016301508" "doi" => "10.1016/j.ad.2016.05.003" "estado" => "S300" "subdocumento" => "" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:1 [ "total" => 0 ] "idiomaDefecto" => "es" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0001731016301508?idApp=UINPBA000044" ] ] "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1578219016301652?idApp=UINPBA000044" "url" => "/15782190/0000010700000008/v2_201704100057/S1578219016301652/v2_201704100057/en/main.assets" ] "en" => array:21 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">Review</span>" "titulo" => "Elastography in Dermatology" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "652" "paginaFinal" => "660" ] ] "autores" => array:1 [ 0 => array:3 [ "autoresLista" => "F. Alfageme Roldán" "autores" => array:1 [ 0 => array:4 [ "nombre" => "F." "apellidos" => "Alfageme Roldán" "email" => array:1 [ 0 => "dermalfageme@gmail.com" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Servicio de Dermatología, Hospital Universitario Puerta de Hierro, Majadahonda, Madrid, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Dermatologic Ultrasound Teaching Centre, Ultrasound Learning Centre (EFSUMB), Madrid, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Elastografía en dermatología" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1278 "Ancho" => 2253 "Tamanyo" => 96450 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">When tissue is compressed with a force F, the tissue particles (A) undergo a displacement (A′). The quotient of the displacement (d) of the structure being examined and its total initial length (D) is known as strain. The particles are displaced in perpendicular to this pressure wave, generating waves called shear waves.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Since antiquity, palpation has played an important role in the general physical examination of patients because it provides information about the physical characteristics of the tissues.<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">1</span></a> A loss of elasticity or increase in rigidity of organs or tissues has traditionally been associated with a poorer prognosis in inflammatory processes, which histologically tend to be associated with fibrosis, and in tumor processes, in which the elastic properties of healthy tissues decrease.<a class="elsevierStyleCrossRefs" href="#bib0230"><span class="elsevierStyleSup">2,3</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Estimation of the elasticity or rigidity of tissues could therefore facilitate early, noninvasive monitoring and treatment of inflammatory and tumor processes.<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">4</span></a> Elastography is a technique in which ultrasound is used to detect changes in the elasticity of tissues.<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">5</span></a> Since the late 20th century, elastography has been used in various diseases, including tumors of the breast, thyroid, and liver, as well as in inflammatory processes in the same organs.<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">6</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">The recent introduction of high-frequency linear ultrasound probes has made it possible for this technology to be applied to superficial tissues such as the bone and muscle system,<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">6</span></a> the superficial vascular system,<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">6</span></a> and the skin and adnexa.<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">7</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">This review details the basic physical concepts of elastography and the possible utility of this technique in the assessment of the skin and adnexa.</p><p id="par0025" class="elsevierStylePara elsevierViewall">It is important to note that most cutaneous elastography studies are small case series, a majority of which are observational and of limited scientific robustness. Nevertheless, a review that introduces elastography to dermatologists and encourages future studies of the practical utility of the technique in dermatology could still be useful.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Elastography: The Physical Concepts of Strain and Shear Wave</span><p id="par0030" class="elsevierStylePara elsevierViewall">When a tissue is subjected to pressure, it deforms and tends to recover its initial shape (elasticity). The resistance of the tissue to deformation is called <span class="elsevierStyleItalic">rigidity</span> or <span class="elsevierStyleItalic">stiffness</span>.<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">8</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">The term <span class="elsevierStyleItalic">strain</span> describes the change in the relative length of a structure subjected to pressure with respect to the surrounding tissue<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">9</span></a> (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0040" class="elsevierStylePara elsevierViewall">In addition to this physical phenomenon, a series of waves perpendicular to the displacement of the pressure wave—known as <span class="elsevierStyleItalic">shear waves</span>—are also generated in the tissue.<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">10</span></a> It is possible to determine the velocity of the shear wave, which provides indirect quantitative information about the stiffness of the tissue (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Types of Elastography and Their Limitations</span><p id="par0045" class="elsevierStylePara elsevierViewall">According to the clinical guidelines on elastography published by the European Federation of Societies for Ultrasound in Medicine and Biology (EFSUMB),<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">11</span></a> there are two basic types of elastography: strain elastography (SE), which assesses tissue deformation, and shear wave elastography (SWE), which characterizes the shear waves (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). Types of elastography can also be classified according to the physical force that produces the tissue deformation. This force can be mechanical (manual or automatic) or it can be produced by an ultrasound pulse called acoustic radiation force impulse (ARFI). Each of these elastography methods offers qualitative or quantitative information about the rigidity or stiffness (terms used interchangeably in this review) of tissues.</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0050" class="elsevierStylePara elsevierViewall">Semiquantitative measurement scales normally associate a number from 1 to 5 with the rigidity percentage of a structure, with 1 being softest and 5 being stiffest.<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">11</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall">Another way to quantify the stiffness of a structure is to express it in relation to the surrounding parenchyma. This quotient is known as the strain ratio.<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">12</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">In SWE, which determines shear wave displacement velocities, measurements are quantitative and can be expressed in either kPa or m/s.<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">13</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">This technique has certain limitations. Because of the great variability of the various types of elastography, studies of the technique have been isolated and there are no universal measures used by all elastography equipment.<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">11</span></a></p><p id="par0070" class="elsevierStylePara elsevierViewall">Inter- and intraobserver variability is greater in SE (especially the manual variant) than in SWE.<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">11</span></a></p><p id="par0075" class="elsevierStylePara elsevierViewall">Because it uses ultrasound waves, elastography—like conventional ultrasound—generates artifacts. In areas with acoustic shadowing or cystic structures, the information provided about tissue characteristics may not reflect reality.<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">14</span></a> However, as in the case of conventional ultrasound, these artifacts also provide information about the structure being examined.<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">14</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Elastography in Dermatology: Technique and Peculiarities</span><p id="par0080" class="elsevierStylePara elsevierViewall">According to the EFSUMB clinical guidelines on elastography,<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">11</span></a> the following recommendations should be taken into account when elastography is performed on any organ:<ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">1.</span><p id="par0085" class="elsevierStylePara elsevierViewall">The structure should be in close proximity to the transducer (<<span class="elsevierStyleHsp" style=""></span>4<span class="elsevierStyleHsp" style=""></span>cm).</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">2.</span><p id="par0090" class="elsevierStylePara elsevierViewall">The structure should be nearly homogeneous.</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">3.</span><p id="par0095" class="elsevierStylePara elsevierViewall">When pressure is applied, there should be no slippage in the structure over deeper planes.</p></li><li class="elsevierStyleListItem" id="lsti0020"><span class="elsevierStyleLabel">4.</span><p id="par0100" class="elsevierStylePara elsevierViewall">Pressure should be applied by a surface larger than the structure being examined.</p></li><li class="elsevierStyleListItem" id="lsti0025"><span class="elsevierStyleLabel">5.</span><p id="par0105" class="elsevierStylePara elsevierViewall">No structures that damp compression—such as large blood vessels—should be present.</p></li><li class="elsevierStyleListItem" id="lsti0030"><span class="elsevierStyleLabel">6.</span><p id="par0110" class="elsevierStylePara elsevierViewall">The structures being examined should be completely included within the region of interest.</p></li><li class="elsevierStyleListItem" id="lsti0035"><span class="elsevierStyleLabel">7.</span><p id="par0115" class="elsevierStylePara elsevierViewall">The direction of the compression force should be known.</p></li><li class="elsevierStyleListItem" id="lsti0040"><span class="elsevierStyleLabel">8.</span><p id="par0120" class="elsevierStylePara elsevierViewall">The number of structures being examined should be limited.</p></li></ul></p><p id="par0125" class="elsevierStylePara elsevierViewall">When elastography is used on the skin, gel should not be used in the region of interest.<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">11</span></a> As we can infer, the skin is an organ that adapts to the conditions in which elastography can be carried out with the appropriate technique and technology—that is, high-frequency linear probes applied to the skin and adnexa.<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">15</span></a></p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Elastography of Normal Skin and Adnexa</span><p id="par0130" class="elsevierStylePara elsevierViewall">The stiffness of healthy skin varies according to the cutaneous layer being studied. The dermis is more rigid than the subcutaneous cellular tissue<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">16</span></a> (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>, A, B). In the subcutaneous cellular tissue, the septa are more rigid than the fat lobules. Blood vessels, like the peripheral nerves, are not very rigid in comparison to the surrounding subcutaneous cellular tissue.<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">16</span></a></p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0135" class="elsevierStylePara elsevierViewall">In a healthy nail, the nail plate is more rigid than the nail bed<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">17</span></a> (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>).</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Elastography of Skin Tumors</span><p id="par0140" class="elsevierStylePara elsevierViewall">The most widely investigated application in elastography of skin tumors is the differentiation of benign and malignant tumors.<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">18</span></a></p><p id="par0145" class="elsevierStylePara elsevierViewall">In tumors, the mechanical properties of the tissue are generally altered in a way that allows the tumor to be differentiated from the adjacent healthy tissue.<a class="elsevierStyleCrossRefs" href="#bib0315"><span class="elsevierStyleSup">19,20</span></a></p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Benign Skin Tumors and Neck Masses</span><p id="par0150" class="elsevierStylePara elsevierViewall">Although benign subcutaneous tumors have a recognizable appearance in B-mode ultrasound,<a class="elsevierStyleCrossRef" href="#bib0325"><span class="elsevierStyleSup">21</span></a> in doubtful cases elastography could play a useful role in the differential diagnosis.</p><p id="par0155" class="elsevierStylePara elsevierViewall">In a study by Bhatia et al.,<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">22</span></a> 52 non-nodal neck masses were evaluated using real-time qualitative ultrasound elastography. The diagnosis of the lesions was later corroborated by cytology and histology. The lesions were evaluated semiquantitatively on a scale of 0 to 3, where 0 was completely soft and 3 was completely stiff. Lipomas were less stiff than other types of lesions, most of which were cysts, malformations, and neurogenic tumors (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>). In an extension of the study, SWE was used to assess malignant and benign neck tumors.<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">23</span></a> The mean stiffness of the malignant tumors (226.4<span class="elsevierStyleHsp" style=""></span>kPa) was higher than that of the benign lesions (28.3<span class="elsevierStyleHsp" style=""></span>kPa) and the difference was statistically significant. With a cut-off of 174.4<span class="elsevierStyleHsp" style=""></span>kPa, sensitivity of 83.3% and specificity of 97.5% were achieved in the differentiation of benign and malignant lesions. The authors noted that all tumors were correctly diagnosed with conventional ultrasound and that elastography would not have altered the treatment, but they argued that less experienced operators could find the technique helpful in the diagnosis of neck lesions.</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia><p id="par0160" class="elsevierStylePara elsevierViewall">Park et al.<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">24</span></a> used elastography to differentiate inflamed and unruptured epidermal cysts (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>, B), the latter being stiffer than the former.</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Malignant Skin Tumors</span><p id="par0165" class="elsevierStylePara elsevierViewall">Elastography shows that malignant skin tumors are stiffer than the surrounding tissue<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">18</span></a> (<a class="elsevierStyleCrossRef" href="#fig0025">Fig. 5</a>).</p><elsevierMultimedia ident="fig0025"></elsevierMultimedia><p id="par0170" class="elsevierStylePara elsevierViewall">Dasgeb et al.<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">25</span></a> studied 55 patients with a total of 67 epithelial tumors, of which 29 were malignant (17 basal cell carcinomas and 12 squamous cell carcinomas) and 19 were benign. In this study, the strain ratio was > 3.9 in all malignant skin tumors and < 3 in all benign skin tumors. For strain ratio values between 3.00 and 3.9, sensitivity and specificity were 100% in the diagnosis of malignant lesions.</p><p id="par0175" class="elsevierStylePara elsevierViewall">Elastography has been used to study melanoma. In a pilot study by Botar et al.,<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">26</span></a> 42 melanomas in 39 patients were studied using SE and color Doppler ultrasound to assess vascularization.</p><p id="par0180" class="elsevierStylePara elsevierViewall">The melanomas were hypervascularized and had multiple vascular pedicles, and SE showed that the lesions were stiffer than the adjacent skin. The lesions with the highest degree of vascularization had the greatest stiffness.</p><p id="par0185" class="elsevierStylePara elsevierViewall">The correlation between melanoma neovascularization and prognosis is well known in the literature.<a class="elsevierStyleCrossRefs" href="#bib0355"><span class="elsevierStyleSup">27,28</span></a> Therefore, lesion stiffness could be a prognostic factor in melanoma.<a class="elsevierStyleCrossRef" href="#bib0365"><span class="elsevierStyleSup">29</span></a></p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Lymph Node Enlargement</span><p id="par0190" class="elsevierStylePara elsevierViewall">The aim of ultrasound assessment of lymph nodes is to noninvasively diagnose malignant lymph nodes in patients with clinically suspicious lesions.<a class="elsevierStyleCrossRef" href="#bib0370"><span class="elsevierStyleSup">30</span></a></p><p id="par0195" class="elsevierStylePara elsevierViewall">Lymph nodes have an elastic structure in which the cortex tends to be less rigid than the capsule and the hilum (<a class="elsevierStyleCrossRef" href="#fig0030">Fig. 6</a>).</p><elsevierMultimedia ident="fig0030"></elsevierMultimedia><p id="par0200" class="elsevierStylePara elsevierViewall">To assess the stiffness of lymph nodes, SE is used to classify nodes in 4 or 5 categories according to the proportion of stiff areas they present.<a class="elsevierStyleCrossRef" href="#bib0375"><span class="elsevierStyleSup">31</span></a> Benign enlarged nodes generally tend to be soft, whereas malignant nodes tend to be stiffer.<a class="elsevierStyleCrossRef" href="#bib0380"><span class="elsevierStyleSup">32</span></a> However, lymphomas are less stiff than metastatic nodes and similar in stiffness to inflamed nodes. Therefore, benign and lymphomatous nodes cannot be distinguished with elastography alone.<a class="elsevierStyleCrossRef" href="#bib0385"><span class="elsevierStyleSup">33</span></a></p><p id="par0205" class="elsevierStylePara elsevierViewall">In the case of melanoma (<a class="elsevierStyleCrossRef" href="#fig0035">Fig. 7</a>), Hinz et al.<a class="elsevierStyleCrossRef" href="#bib0390"><span class="elsevierStyleSup">34</span></a> found that elastography in addition to conventional B-mode sonography combined with color Doppler sonography increased sensitivity in the detection of metastatic disease in clinically suspicious enlarged lymph nodes from 80.9% to 95.2% but found no increase in specificity (76.2%). Similar results were obtained in later studies such as that of Ogata et al.<a class="elsevierStyleCrossRef" href="#bib0395"><span class="elsevierStyleSup">35</span></a></p><elsevierMultimedia ident="fig0035"></elsevierMultimedia></span></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Elastography in Inflammatory Skin Diseases</span><p id="par0210" class="elsevierStylePara elsevierViewall">Not only does inflammation cause changes in the sonographic structure of the skin and adnexa in B-mode and Doppler ultrasound,<a class="elsevierStyleCrossRef" href="#bib0400"><span class="elsevierStyleSup">36</span></a> it also affects the stiffness of the structures<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">7</span></a> (<a class="elsevierStyleCrossRef" href="#fig0040">Fig. 8</a>).</p><elsevierMultimedia ident="fig0040"></elsevierMultimedia><p id="par0215" class="elsevierStylePara elsevierViewall">In a study by Gaspari et al.,<a class="elsevierStyleCrossRef" href="#bib0405"><span class="elsevierStyleSup">37</span></a> 50 patients who visited the emergency department for abscess drainage were examined using B-mode ultrasound and SE. With elastography, it was possible to observe stiff areas around the abscesses that were not visible with B-mode ultrasound.</p><p id="par0220" class="elsevierStylePara elsevierViewall">Cucoş et al.<a class="elsevierStyleCrossRef" href="#bib0410"><span class="elsevierStyleSup">38</span></a> measured the effects of topical corticosteroid treatment on epidermal and dermal thickness and elasticity in 16 psoriatic plaques. Epidermal thickness decreased, whereas dermal thickness increased slightly and there was no change in plaque elasticity. Despite the small number of patients in this study, the results seem to indicate that the sensitivity of SE in the treatment of psoriatic plaques is low.</p><p id="par0225" class="elsevierStylePara elsevierViewall">Elastography has been more extensively developed in fibrotic and sclerotic processes that are primarily cutaneous or systemic (morphea/systemic sclerosis), in which clinical measurement scales have very limited sensitivity and specificity<a class="elsevierStyleCrossRef" href="#bib0415"><span class="elsevierStyleSup">39</span></a> (<a class="elsevierStyleCrossRef" href="#fig0045">Fig. 9</a>).</p><elsevierMultimedia ident="fig0045"></elsevierMultimedia><p id="par0230" class="elsevierStylePara elsevierViewall">Initial studies carried out with SE in systemic sclerosis, such as that of Iagnocco et al.,<a class="elsevierStyleCrossRef" href="#bib0415"><span class="elsevierStyleSup">39</span></a> have indicated that dermal stiffness is greater in patients with systemic sclerosis than in controls. However, the reproducibility of the technique at other sites, such as the fingers, was variable, perhaps because of the proximity of the bony surface of the phalanges. Di Geso et al.<a class="elsevierStyleCrossRef" href="#bib0420"><span class="elsevierStyleSup">40</span></a> repeated this exercise to determine the degree of correlation between measurements with SE and with B-mode ultrasound. The authors concluded that elastography reduces inter- and intraobserver variability in the assessment of dermal thickness of the fingers in patients with systemic sclerosis.</p><p id="par0235" class="elsevierStylePara elsevierViewall">Perioral involvement is frequent in patients with systemic sclerosis.<a class="elsevierStyleCrossRef" href="#bib0425"><span class="elsevierStyleSup">41</span></a> In a pilot study, Cannaò et al.<a class="elsevierStyleCrossRef" href="#bib0425"><span class="elsevierStyleSup">41</span></a> described an elastographic scale based on perioral segments and showed that perioral stiffness is greater in patients with systemic sclerosis than in controls.</p><p id="par0240" class="elsevierStylePara elsevierViewall">Elastography has also been used in other fibrotic processes, such as cutaneous processes secondary to irradiation. Using SWE to measure stiffness in the skin and subcutaneous cellular tissue in the neck, Liu et al.<a class="elsevierStyleCrossRef" href="#bib0430"><span class="elsevierStyleSup">42</span></a> found differences between patients who had undergone radiation therapy and age-matched healthy controls (64.6<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>46.8<span class="elsevierStyleHsp" style=""></span>kPa vs 19.9<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>7.8<span class="elsevierStyleHsp" style=""></span>kPa). The authors correlated these changes with the degree of atrophy of the neck muscles and with the decrease in thickness of the subcutaneous cellular tissue of the neck.</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Application of Elastography in Other Skin Conditions</span><p id="par0245" class="elsevierStylePara elsevierViewall">A SE study by Suehiro et al.<a class="elsevierStyleCrossRef" href="#bib0435"><span class="elsevierStyleSup">43</span></a> found lower strain values in patients with lipodermatosclerosis than in patients with lymphedema, regardless of the degree of lymphedema.</p><p id="par0250" class="elsevierStylePara elsevierViewall">Elastography has also been used to assess pressure ulcers. Experimental studies in phantoms and animals have found that the stiffness of the surface skin increases quickly after sustained pressure and that this could be an early marker for the detection of areas at risk of ulceration.<a class="elsevierStyleCrossRef" href="#bib0440"><span class="elsevierStyleSup">44</span></a></p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Conclusions</span><p id="par0255" class="elsevierStylePara elsevierViewall">Elastography in dermatology is an emerging technique that has great potential in the physical characterization of the tissues of the skin and adnexa. The various elastography techniques offer complementary and synergistic information in the assessment of cutaneous tissues. Dermatologists can consider scenarios in which elastography can offer complementary information that would improve patient care.</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Conflicts of Interest</span><p id="par0260" class="elsevierStylePara elsevierViewall">The author declares that he has no conflicts of interest.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:15 [ 0 => array:3 [ "identificador" => "xres826638" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec822946" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres826637" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec822945" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Elastography: The Physical Concepts of Strain and Shear Wave" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Types of Elastography and Their Limitations" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Elastography in Dermatology: Technique and Peculiarities" ] 8 => array:3 [ "identificador" => "sec0025" "titulo" => "Elastography of Normal Skin and Adnexa" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "sec0030" "titulo" => "Elastography of Skin Tumors" ] 1 => array:2 [ "identificador" => "sec0035" "titulo" => "Benign Skin Tumors and Neck Masses" ] 2 => array:2 [ "identificador" => "sec0040" "titulo" => "Malignant Skin Tumors" ] 3 => array:2 [ "identificador" => "sec0045" "titulo" => "Lymph Node Enlargement" ] ] ] 9 => array:2 [ "identificador" => "sec0050" "titulo" => "Elastography in Inflammatory Skin Diseases" ] 10 => array:2 [ "identificador" => "sec0055" "titulo" => "Application of Elastography in Other Skin Conditions" ] 11 => array:2 [ "identificador" => "sec0060" "titulo" => "Conclusions" ] 12 => array:2 [ "identificador" => "sec0065" "titulo" => "Conflicts of Interest" ] 13 => array:2 [ "identificador" => "xack277333" "titulo" => "Acknowledgments" ] 14 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2016-01-27" "fechaAceptado" => "2016-05-01" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec822946" "palabras" => array:3 [ 0 => "Elastography" 1 => "Skin ultrasound" 2 => "Dermatologic ultrasound" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec822945" "palabras" => array:3 [ 0 => "Elastografía" 1 => "Ecografía cutánea" 2 => "Ecografía dermatológica" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Elastography is a recently developed ultrasound technique applicable to various medical specialties. It provides information on the physical properties of tissues in the context of physiologic and pathologic alterations. In this review we explain the physical principles of the method, the information provided by the different elastography techniques, and its new applications in clinical dermatology.</p></span>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">La elastografía es una técnica ecográfica de reciente desarrollo en varias especialidades médicas que aporta información sobre las propiedades físicas de los tejidos en procesos fisiológicos y patológicos. En esta revisión se explican los principios físicos de la técnica, la información que aportan las distintas modalidades de elastografía y las nuevas aplicaciones en dermatología clínica.</p></span>" ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as: Alfageme Roldán F. Elastografía en dermatología. Actas Dermosifiliogr. 2016;107:652–660.</p>" ] ] "multimedia" => array:10 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1278 "Ancho" => 2253 "Tamanyo" => 96450 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">When tissue is compressed with a force F, the tissue particles (A) undergo a displacement (A′). The quotient of the displacement (d) of the structure being examined and its total initial length (D) is known as strain. The particles are displaced in perpendicular to this pressure wave, generating waves called shear waves.</p>" ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1553 "Ancho" => 1543 "Tamanyo" => 311208 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">A, Strain elastography of normal skin. Note the strain ratio of the dermis and the fat (SR<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>1.86), which indicates that the dermis is stiffer than the subcutaneous tissue.</p> <p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">E indicates epidermis; D, dermis; TCS, subcutaneous cellular tissue.</p> <p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">B, Shear wave elastography of the dermis of the scalp. In the lower right corner, note the parameters of velocity and pressure in the region of interest (yellowish-green rectangle).</p>" ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 754 "Ancho" => 1605 "Tamanyo" => 127272 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Strain elastography of a nail. The nail plate (T) is stiffer than the nail bed (L) and similar in stiffness to the distal phalanx (D).</p>" ] ] 3 => array:7 [ "identificador" => "fig0020" "etiqueta" => "Figure 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 2145 "Ancho" => 1558 "Tamanyo" => 339020 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">A, Strain elastography of a lipoma (L). B, Elastography of a cyst (Q).</p>" ] ] 4 => array:7 [ "identificador" => "fig0025" "etiqueta" => "Figure 5" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr5.jpeg" "Alto" => 1052 "Ancho" => 1605 "Tamanyo" => 168512 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Strain elastography of a squamous cell carcinoma of the cheek (CE). The strain ratio (SR<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>2.36) indicates that the lesion is stiffer than the adjacent subcutaneous cellular tissue.</p>" ] ] 5 => array:7 [ "identificador" => "fig0030" "etiqueta" => "Figure 6" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr6.jpeg" "Alto" => 708 "Ancho" => 1405 "Tamanyo" => 136462 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Strain elastography of an inflamed lymph node (A). Note that the medulla is stiffer than the cortex.</p>" ] ] 6 => array:7 [ "identificador" => "fig0035" "etiqueta" => "Figure 7" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr7.jpeg" "Alto" => 762 "Ancho" => 1605 "Tamanyo" => 155059 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Strain elastography of a lymph node metastasis of melanoma (M). Note the complete rigidity of the lesion and the lack of soft areas.</p>" ] ] 7 => array:7 [ "identificador" => "fig0040" "etiqueta" => "Figure 8" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr8.jpeg" "Alto" => 959 "Ancho" => 1707 "Tamanyo" => 205275 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">Shear wave elastography of a post-surgical inflammatory area of the scalp (blue region). On the left-hand side, note the velocities and pressures in the region of interest.</p>" ] ] 8 => array:7 [ "identificador" => "fig0045" "etiqueta" => "Figure 9" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr9.jpeg" "Alto" => 961 "Ancho" => 1505 "Tamanyo" => 174766 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Elastography of morphea (M). An increase in stiffness can be observed in the dermal-subdermal interface of the plaque in comparison with the surrounding tissue (SR<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>3.4).</p>" ] ] 9 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "<p id="spar0075" class="elsevierStyleSimplePara elsevierViewall">Source: Adapted from the clinical guidelines on elastography of the European Federation of Societies for Ultrasound in Medicine and Biology (EFSUMB).</p><p id="spar0080" class="elsevierStyleSimplePara elsevierViewall">Abbreviations: ARFI, acoustic radiation force impulse; SE, strain elastography; SWE, shear wave elastography.</p>" "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="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Method \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Type of Force \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Quantitative/Qualitative \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Strain imaging (SE) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Mechanical<br>ARFI \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Qualitative \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Shear wave imaging/velocity measurement (SWE) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Mechanical<br>ARFI \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Quantitative \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1390595.png" ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">Types of Elastography.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:44 [ 0 => array:3 [ "identificador" => "bib0225" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Neurosurgical classic" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:1 [ 0 => "R. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 8 | 12 | 20 |
| 2024 October | 109 | 43 | 152 |
| 2024 September | 133 | 33 | 166 |
| 2024 August | 133 | 86 | 219 |
| 2024 July | 89 | 37 | 126 |
| 2024 June | 112 | 46 | 158 |
| 2024 May | 89 | 58 | 147 |
| 2024 April | 113 | 32 | 145 |
| 2024 March | 105 | 45 | 150 |
| 2024 February | 90 | 40 | 130 |
| 2024 January | 112 | 40 | 152 |
| 2023 December | 85 | 19 | 104 |
| 2023 November | 107 | 33 | 140 |
| 2023 October | 97 | 23 | 120 |
| 2023 September | 104 | 37 | 141 |
| 2023 August | 72 | 23 | 95 |
| 2023 July | 93 | 39 | 132 |
| 2023 June | 73 | 29 | 102 |
| 2023 May | 95 | 44 | 139 |
| 2023 April | 75 | 26 | 101 |
| 2023 March | 121 | 28 | 149 |
| 2023 February | 68 | 18 | 86 |
| 2023 January | 67 | 47 | 114 |
| 2022 December | 80 | 42 | 122 |
| 2022 November | 65 | 34 | 99 |
| 2022 October | 40 | 24 | 64 |
| 2022 September | 30 | 38 | 68 |
| 2022 August | 37 | 35 | 72 |
| 2022 July | 43 | 40 | 83 |
| 2022 June | 35 | 32 | 67 |
| 2022 May | 52 | 59 | 111 |
| 2022 April | 63 | 32 | 95 |
| 2022 March | 71 | 67 | 138 |
| 2022 February | 52 | 43 | 95 |
| 2022 January | 83 | 52 | 135 |
| 2021 December | 49 | 48 | 97 |
| 2021 November | 64 | 61 | 125 |
| 2021 October | 90 | 88 | 178 |
| 2021 September | 69 | 44 | 113 |
| 2021 August | 85 | 44 | 129 |
| 2021 July | 82 | 25 | 107 |
| 2021 June | 93 | 44 | 137 |
| 2021 May | 103 | 58 | 161 |
| 2021 April | 305 | 44 | 349 |
| 2021 March | 132 | 46 | 178 |
| 2021 February | 111 | 31 | 142 |
| 2021 January | 94 | 32 | 126 |
| 2020 December | 80 | 30 | 110 |
| 2020 November | 57 | 24 | 81 |
| 2020 October | 46 | 18 | 64 |
| 2020 September | 48 | 24 | 72 |
| 2020 August | 51 | 23 | 74 |
| 2020 July | 30 | 15 | 45 |
| 2020 June | 48 | 34 | 82 |
| 2020 May | 33 | 23 | 56 |
| 2020 April | 56 | 25 | 81 |
| 2020 March | 39 | 21 | 60 |
| 2020 February | 6 | 0 | 6 |
| 2020 January | 4 | 0 | 4 |
| 2019 December | 9 | 0 | 9 |
| 2019 November | 4 | 0 | 4 |
| 2019 September | 9 | 0 | 9 |
| 2019 August | 4 | 0 | 4 |
| 2019 July | 4 | 0 | 4 |
| 2019 June | 4 | 0 | 4 |
| 2019 May | 8 | 1 | 9 |
| 2019 April | 4 | 3 | 7 |
| 2019 March | 3 | 1 | 4 |
| 2019 February | 2 | 0 | 2 |
| 2018 December | 6 | 0 | 6 |
| 2018 November | 3 | 0 | 3 |
| 2018 October | 7 | 0 | 7 |
| 2018 September | 3 | 0 | 3 |
| 2018 February | 27 | 8 | 35 |
| 2018 January | 46 | 10 | 56 |
| 2017 December | 59 | 17 | 76 |
| 2017 November | 50 | 7 | 57 |
| 2017 October | 37 | 10 | 47 |
| 2017 September | 32 | 12 | 44 |
| 2017 August | 26 | 15 | 41 |
| 2017 July | 32 | 4 | 36 |
| 2017 June | 49 | 15 | 64 |
| 2017 May | 44 | 11 | 55 |
| 2017 April | 27 | 15 | 42 |
| 2017 March | 30 | 12 | 42 |
| 2017 February | 70 | 25 | 95 |
| 2017 January | 31 | 7 | 38 |
| 2016 December | 45 | 25 | 70 |
| 2016 November | 55 | 28 | 83 |
| 2016 October | 57 | 40 | 97 |
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