Case and Research Letter
Off-White Perifollicular Halo Around the Salt and Pepper Sign in the Dermoscopic Diagnosis of Systemic Sclerosis and Interstitial Lung Disease
Halo perifolicular blanquecino a la dermatoscopia del signo de sal y pimienta en el diagnóstico de esclerosis sistémica y enfermedad pulmonar intersticial
A.A. Hernández Collazoa,
, M.H. Capilla Garcíab, F. Barba Hernándezc, R. Quiñones Venegasd
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a Dermatología, Nuevo Hospital “Miguel Hidalgo” y Universidad Autónoma de Aguascalientes, Aguascalientes, Mexico
b Facultad de Medicina, Universidad Autónoma de Aguascalientes, Aguascalientes, Mexico
c Medicina Interna, Hospital ABC, Ciudad de México, Mexico
d Instituto Dermatológico de Jalisco “Dr. José Barba Rubio”, Mexico
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A, Accentuated pigment network surrounding a whitish perifollicular circle against an achromic background. B, Accentuated pigment network surrounding a uniform whitish perifollicular halo against white areas with telangiectasias.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Systemic sclerosis is a multisystem disease characterized by skin sclerosis and fibrosis of internal organs secondary to microvascular damage. Diagnosis is often delayed, resulting in advanced disease and organ dysfunction.<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">1</span></a> Diffuse depigmentation in a salt and pepper pattern can help in the early diagnosis of certain cases.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">2</span></a> This sign, however, can often be overlooked or confused with other types of dyschromia such as vitiligo.</p><p id="par0010" class="elsevierStylePara elsevierViewall">The salt and pepper sign is a dyschromia associated with progressive systemic sclerosis. It is characterized by vitiligo-like depigmentation with perifollicular pigmentary retention, as the periadnexal capillary network preserves melanogenesis (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">2</span></a> This sign is one of the earliest and most frequent findings in progressive systemic sclerosis in patients with Fitzpatrick skin types IV, V, or VI, and it may sometimes be the only manifestation in patients without cutaneous sclerosis plaques (systemic sclerosis sine scleroderma).<a class="elsevierStyleCrossRefs" href="#bib0050"><span class="elsevierStyleSup">3,4</span></a> Pigmentary changes in scleroderma have been identified as an early manifestation of systemic damage in up to 30% of patients; most of these patients have pulmonary involvement due to interstitial fibrosis and pulmonary hypertension, which is usually the main cause of mortality.<a class="elsevierStyleCrossRefs" href="#bib0045"><span class="elsevierStyleSup">2,5</span></a> The lesions are most often located on the head (forehead, scalp, and retroauricular region), followed by the neck and the dorsum of the fingers.<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">3</span></a> Histologic findings of sclerosis in areas of dyschromia are inconsistent, while signs of follicular fibrosis are rare. Other findings are similar to those seen in vitiligo: pigmentary incontinence, a periadnexal lymphocytic infiltrate, and absence of melanocytes at the periphery of the follicle. Biopsy findings in salt and pepper areas are therefore not diagnostic.<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">6</span></a></p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0015" class="elsevierStylePara elsevierViewall">The clinical and dermoscopic characteristics of 4 patients with systemic sclerosis and salt and pepper skin are shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>. A whitish perifollicular halo was seen on dermoscopy in all cases. All the patients met the 2013 diagnostic criteria for progressive systemic sclerosis according to the American College of Rheumatology/European League Against Rheumatism, and they all had lung involvement in imaging studies. Based on these findings, they were referred to the rheumatology department, where they were treated with mycophenolate and systemic corticosteroids.</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0020" class="elsevierStylePara elsevierViewall">Because the salt and pepper sign shares clinical features (visible to the naked eye and under Wood's lamp) and histologic and pathophysiologic characteristics with vitiligo, it is usually diagnosed late, and is often confused with follicular repigmentation in vitiligo. Patients with a delayed diagnosis develop progressive systemic disease, including vascular disease, interstitial lung fibrosis, myocarditis, acute renal failure, lower esophageal incompetence, and arthritis.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">2</span></a> More effective techniques (such as dermoscopy) are therefore required for early diagnosis. In patients with vitiligo, dermoscopy shows a pseudo pigment network with ill-defined borders in areas of follicular repigmentation (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>).<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">7</span></a> All 4 patients whose details are shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> had a whitish perifollicular halo on dermoscopy (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>). This halo could be a hallmark sign that might be clinically helpful in distinguishing between salt and pepper skin in progressive systemic sclerosis and repigmentation around the hair follicles in vitiligo. Its recognition could therefore help accelerate the diagnosis of severe sclerosis and systemic involvement (mainly pulmonary). The salt and pepper sign might correspond to early perifollicular fibrosis, similar to that seen in lichen planopilaris. Our findings confirm the usefulness of dermoscopy in clinical dermatology.</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Conflicts of Interest</span><p id="par0025" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflict of interest.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0005" "titulo" => "Conflicts of Interest" ] 1 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "multimedia" => array:4 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1240 "Ancho" => 752 "Tamanyo" => 204760 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Dot-like perifollicular dyschromia: the salt and pepper sign. A, At the edge of the frontal hairline in a 62-year-old patient initially diagnosed with vitiligo repigmentation. B, On the right scapula in a 42-year-old patient initially diagnosed with friction melanosis.</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" => 461 "Ancho" => 753 "Tamanyo" => 42593 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Dermoscopic features of perifollicular repigmentation in stable vitiligo. A, Structureless white areas, diffuse pigment network, and perifollicular erythema. B, Perifollicular repigmentation in a pigment network with ill-defined borders.</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" => 461 "Ancho" => 753 "Tamanyo" => 70015 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Dermoscopic features of dyschromia in salt and pepper skin. A, Accentuated pigment network surrounding a whitish perifollicular circle against an achromic background. B, Accentuated pigment network surrounding a uniform whitish perifollicular halo against white areas with telangiectasias.</p>" ] ] 3 => 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="spar0025" class="elsevierStyleSimplePara elsevierViewall">Abbreviation: F, female.</p>" "tablatextoimagen" => array:1 [ 0 => array:1 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Sex/age, y \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">Location \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">Other cutaneous signs of scleroderma \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">Previous diagnosis \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">Dermoscopic findings \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">Systemic findings \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">F/38 \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">Chest (intermammary cleft) \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">SclerodactylyMorphea plaques on dorsal aspect of forearms \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">Vitiligo \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">Perifollicular pigmentation with a whitish halo and a white area with a pseudo perifollicular network surrounding a milky red area \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">Pulmonary fibrosis: Bilateral patchy, ground glass pattern \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">F/48 \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">Cheeks \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">None \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">Melasma and confetti-like depigmentation due to hydroquinone \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">Whitish perifollicular halo surrounded by a pseudo pigment network \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">Interstitial pulmonary fibrosis \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">F/64 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Forehead (frontal hairline) \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">Sclerosis plaques on thighsLipodermatosclerosis on right leg \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">Vitiligo \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">Whitish perifollicular halo surrounded by a pseudo pigment network \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">Pulmonary fibrosis \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">F/42 \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">Back, midline \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">None \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">Friction melanosis \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">Whitish perifollicular halo surrounded by a pseudo pigment network \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">Pulmonary fibrosis \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Clinical and Dermoscopic Characteristics in Patients With Progressive Systemic Sclerosis and Salt and Pepper Skin.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:7 [ 0 => array:3 [ "identificador" => "bib0040" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Systemic sclerosis" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:1 [ 0 => "Y. 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