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SARS-CoV-1 and Middle East Respiratory Syndrome coronavirus &#40;MERS-CoV&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#44;4</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Although SARS-CoV-2 is associated with a case fatality rate of 2&#46;3&#37;&#44;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> lower than that of SARS-CoV-1 &#40;9&#46;5&#37;&#41; and MERS-CoV &#40;34&#46;4&#37;&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> it is highly contagious and quickly spread outside China&#59; its high transmissibility&#8212;higher than that of SARS-CoV-1<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a>&#8212;can be partly explained by the higher viral loads in the respiratory tract&#46; SARS-CoV-2 can also survive in aerosols for more than 3&#8239;hours&#44; remains viable on a variety of surfaces for 72&#8239;hours&#44; and has a relatively short incubation period &#40;&#60;&#8239;2 weeks&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Early reports of coronavirus disease 2019 &#40;COVID-19&#41;&#44; the disease caused by SARS-CoV-2&#44; indicated that most patients experienced fever&#44; rhinorrhea&#44; a cough without expectoration&#44; asthenia&#44; and adynamia&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> A small proportion required hospitalization due to severe pneumonia&#46; In a cohort of 70&#8239;000 patients with SARS-CoV-2 infection in China&#44; Wu et al&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> reported that 14&#37; of patients developed severe pneumonia &#40;dyspnea&#44; tachypnea&#44; desaturation&#44; and a decreased arterial oxygen partial pressure to fractional inspired oxygen ratio&#41; and that 5&#37; required critical care&#46; The case fatality rate was 2&#46;3&#37; for the general population and 14&#37; for patients aged 80 years or older&#46; Their findings were corroborated by later reports from Europe&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">The main risk factors for severe COVID-19 include male sex&#44; diabetes&#44; high blood pressure&#44; chronic lung disease&#44; and cardiovascular disease&#46;<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">11&#44;12</span></a> Children younger than 10 years have mild symptoms and are much less likely than adults to develop complications or die&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">Reports from Asia&#44; Europe&#44; and the United States have described a wide range of cutaneous manifestations associated with COVID-19&#46; Although these manifestations were initially considered to be nonspecific&#44; the publication of an increasing number of cases revealed an apparent pattern and possibly even an association with prognosis&#46; In this article&#44; we review the literature on the diverse cutaneous manifestations described to date in patients with COVID-19&#46; We then outline the different pathophysiologic mechanisms and hypotheses proposed so far to explain their occurrence&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Results</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Cutaneous Manifestations in COVID-19</span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">SARS-CoV-2 Infection and Onset of Nonspecific Rashes</span><p id="par0030" class="elsevierStylePara elsevierViewall">There are 39 coronavirus species&#46; Seven of these&#44; including SARS-CoV-1&#44; SARS-CoV-2&#44; and MERS-CoV&#44; affect humans&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> The other viruses&#8212;HCoV-229E&#44; HCoV-OC43&#44; HCoV-NL63&#44; and HCoV-HKU1&#8212;cause mild respiratory conditions such as the common cold&#46; Like other respiratory viruses&#44; many coronaviruses probably also cause viral rashes that go undetected because of the lack of specific testing&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">The first report mentioning cutaneous manifestations in patients with COVID-19 was published by Guan et al&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> in February 2020&#46; The authors analyzed data for 1099 patients infected with SARS-CoV-2 and described 2 cases of skin lesions&#46; They did not&#44; however&#44; specify the type of lesions or describe their clinical characteristics or time of onset&#44; probably explaining why this early report was somewhat overlooked&#46; The publication was followed by a report of a patient in Thailand presenting with a &#8220;morbilliform rash and multiple petechiae&#8221; and a low platelet count who was initially diagnosed with dengue and assigned to outpatient care&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> The patient&#44; however&#44; returned with respiratory symptoms and was diagnosed with SARS-CoV-2 infection by reverse-transcript polymerase chain reaction &#40;PCR&#41;&#46; This report alerted physicians to the importance of investigating cutaneous manifestations in patients with COVID-19&#46;<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">17&#44;18</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">The first large report of cutaneous manifestations in COVID-19 came from a cohort of 88 patients in Italy&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> Of these&#44; 18 &#40;20&#46;4&#37;&#41; had developed cutaneous manifestations&#58; 8 during hospitalization and 10 following discharge&#46; There were 14 cases of &#8220;erythematous rash&#8221;&#44; 3 of &#8220;widespread urticaria&#8221;&#44; and 1 of &#8220;chickenpox-like vesicles&#8221;&#46; The vast majority of patients had trunk lesions&#44; which were largely asymptomatic&#44; resolved spontaneously&#44; and did not appear to be associated with disease severity&#46; Unfortunately&#44; no photographs were taken due to the hospital policies in place at the time of the study&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">As the days passed&#44; new reports emerged of patients with confirmed SARS-CoV-2 infection and a range of very different cutaneous manifestations&#44; including pruritic erythematous-yellowish plaques on the heels &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>A&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> a morbilliform rash sparing acral sites&#44;<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a> a generalized maculopapular morbilliform rash with cephalocaudal progress&#44;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> urticaria-like lesions&#44;<a class="elsevierStyleCrossRefs" href="#bib0115"><span class="elsevierStyleSup">23&#44;24</span></a> a rash reminiscent of symmetrical drug-related intertriginous flexural exanthema&#44;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> and even livedo reticularis on the lower extremities &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>B&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> As in the previous cases&#44; biopsies were not performed due to hospital policies and the mild&#44; self-limiting nature of the lesions&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0050" class="elsevierStylePara elsevierViewall">In April&#44; the <span class="elsevierStyleItalic">Journal of the American Academy of Dermatology</span> published a series of 22 patients with COVID-19 who developed a mild varicella-like rash after a median of 3 days from the onset of systemic symptoms&#59; the rash cleared after a median of 8 days&#44; leaving no residual scarring&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a> Most of the patients were male &#40;72&#46;7&#37;&#41; and the mean age was 60 years&#46; The varicella-like lesions were predominantly vesicles and were scattered in 72&#46;7&#37; of cases and diffuse in 27&#46;3&#37;&#46; The trunk was affected in all cases&#46; None of the reports mentioned facial or mucosal involvement &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>A and B&#41;&#46; The most common symptom&#44; present in almost half of the patients&#44; was mild pruritus&#46; A skin biopsy performed in 7 patients showed findings consistent with an acute viral infection &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>C and D&#41;&#46; The authors suggested that this type of rash might be a specific manifestation of SARS-CoV-2 infection and as such could be useful for raising suspicion of COVID-19 in patients with mild disease&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">A later publication described the case of a man in the fourth decade of life with PCR-confirmed SARS-CoV-2 infection&#44; fever&#44; and concomitant nonpruritic&#44; annular&#44; circinate&#44; erythematous-edematous fixed plaques on the neck&#44; thorax&#44; abdomen&#44; and upper limbs &#40;symmetric distribution&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>A-C&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a> The lesions cleared after 7 days&#46; The biopsy findings were consistent with a viral rash &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>D&#41;&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Cutaneous Manifestations Associated With Thrombosis or Microangiopathic Changes and Chilblain-like Lesions</span><p id="par0060" class="elsevierStylePara elsevierViewall">The Chinese group led by Zhang<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a> published a retrospective review of 7 patients with COVID-19 and pneumonia treated at an intensive care unit in Wuhan&#46; The patients had multiple acro-ischemic manifestations&#44; including acrocyanosis&#44; retiform purpura&#44; and gangrene &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>&#41;&#46; Clinical and laboratory data were evaluated on admission to hospital&#44; at the onset of the cutaneous manifestations&#44; and after the use of anticoagulation therapy&#46; They showed D-dimer&#44; fibrinogen&#44; and fibrinogen degradation product alterations related to the sequential events described&#46; Five of the patients &#40;71&#46;42&#37;&#41; died&#46; This was the first step in the formulation of a hypothesis on the existence of a hypercoagulable state per se in patients with SARS-CoV-2 infection&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia><p id="par0065" class="elsevierStylePara elsevierViewall">Around the same time&#44; multiple reports began to emerge from Europe&#44; the Middle East&#44; and the United States of chilblain-like lesions in young people who had been in close contact with a patient with confirmed or probable SARS-CoV-2 infection&#46; The symptoms varied&#44; but the chief complaints were pain and a burning sensation in the skin&#59; the lesions resolved spontaneously and none of the patients developed SARS-CoV-2 pneumonia&#46;<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">30&#8211;32</span></a></p><p id="par0070" class="elsevierStylePara elsevierViewall">Kolivras et al&#46;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">33</span></a> reported the case of a young man who developed painful&#44; acute-onset&#44; violaceous plaques on the toes and lateral aspect of the feet &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>A and B&#41; 3 days after the onset of upper respiratory symptoms&#46; A skin biopsy showed findings consistent with chilblain lupus &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>C and D&#41;&#46; The nasopharyngeal swab collected on admission was positive for SARS-CoV-2&#46;</p><elsevierMultimedia ident="fig0025"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">In view of the enormous impact of the pandemic on the European continent&#44; numerous groups started to publish studies aimed at characterizing the chilblain-like lesions observed in patients with COVID-19&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">34</span></a> In Italy&#44; Recalcati et al&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> and Tosti et al&#46;<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">35</span></a> reported that these lesions were more common in younger patients &#40;especially children &#91;78&#46;5&#37;&#93;&#41;&#44; predominantly involved the feet &#40;71&#37; of cases&#41;&#44; were self-limiting&#44; and were associated with normal blood tests and an absence of systemic symptoms&#46; A French study of skin lesions observed in 277 patients during 3 weeks of the COVID-19 pandemic found that 142 patients had acral lesions and that 106 of these &#40;75&#37;&#41; were painful erythematous-violaceous edematous macules and papules consistent with chilblain lupus&#46;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">36</span></a> Fern&#225;ndez-Nieto et al<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">37</span></a> studied 132 nonhospitalized patients who consulted for acro-ischemic lesions over a period of 5 weeks&#46; The mean age of the patients was 19&#46;9 years&#59; 40&#46;9&#37; had been in close contact with a patient with confirmed SARS-CoV-2 infection and 14&#46;4&#37; tested positive&#46; Over 90&#37; of the lesions affected the fingers or toes&#44; but mostly the toes &#40;81&#46;8&#37;&#41;&#46; Similarly to the other cases reported&#44; the patients experienced mild disease&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Magro et al&#46;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">38</span></a> reported on patients with COVID-19 who developed cutaneous manifestations consistent with a procoagulant or microangiopathic state&#46; A skin biopsy was performed in 3 patients who developed retiform purpura or livedo racemosa &#40;<a class="elsevierStyleCrossRef" href="#fig0030">Fig&#46; 6</a>A&#41; associated with elevated D-dimer levels during the course of their respiratory illness&#44; with findings showing pauci-inflammatory thrombogenic vasculopathy and C5b-9 and C4d deposition &#40;<a class="elsevierStyleCrossRef" href="#fig0030">Fig&#46; 6</a>B and C&#41;&#46; This observation sparked the hypothesis of a link between mechanisms dependent on the alternative or lectin complement pathways and thrombotic events in patients with SARS-CoV-2 infection&#44; and subsequently provided an explanation for the existence of procoagulant states in other organs&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">39</span></a></p><elsevierMultimedia ident="fig0030"></elsevierMultimedia></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Spanish Consensus on the Classification of Cutaneous Manifestations of COVID-19</span><p id="par0085" class="elsevierStylePara elsevierViewall">The <span class="elsevierStyleItalic">British Journal of Dermatology</span> published the results of a Spanish consensus study of 375 patients with confirmed or suspected SARS-CoV-2 infection who developed cutaneous manifestations without a clear explanation&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">40</span></a> Numerous factors were evaluated over a period of 2 weeks&#44; including clinical manifestations&#44; time of onset in relation to other symptoms&#44; demographics&#44; and associations with disease course and outcomes&#46; The group&#44; led by Galv&#225;n Casa&#44; divided the manifestations into 5 clinical patterns&#58; <span class="elsevierStyleItalic">1</span>&#41; pseudo-chilblains &#40;19&#37;&#41;&#44; <span class="elsevierStyleItalic">2</span>&#41; vesicular eruptions &#40;9&#37;&#41;&#44; <span class="elsevierStyleItalic">3</span>&#41; urticarial lesions &#40;19&#37;&#41;&#44; <span class="elsevierStyleItalic">4</span>&#41; maculopapular eruptions &#40;47&#37;&#41;&#44; and <span class="elsevierStyleItalic">5</span>&#41; livedoid or necrotic lesions &#40;6&#37;&#41;&#46; They found that livedoid and necrotic lesions affected older patients &#40;mean age&#44; 63 years&#41; with severe disease &#40;mortality rate&#44; 10&#37;&#41;&#44; while pseudo-chilblain lesions &#40;acral areas of erythema and edema with vesicles or pustules&#41; were more common after the onset of respiratory symptoms &#40;59&#37; of cases&#41; and occurred in young patients &#40;mean age&#44; 21&#46;8 years&#41; with mild COVID-19&#46; The survival rate of patients with maculopapular eruptions was 98&#37;&#46; The Spanish findings were consistent with reports from other authors&#44; especially in terms of the mild nature of these chilblain-like lesions&#46;<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">30&#8211;33</span></a></p></span></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Pathophysiological Findings</span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Pathophysiology of SARS-CoV-2 Infection and Possible Association With Cutaneous Manifestations</span><p id="par0090" class="elsevierStylePara elsevierViewall">Laboratory findings in patients with severe SARS-CoV-2 infection include leukocytosis&#44; neutrophilia&#44; lymphopenia&#44; thrombocytopenia&#44; increased lactate dehydrogenase and procalcitonin levels&#44; and D-dimer and fibrinogen degradation product alterations&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">41</span></a> In some cases&#44; these findings overlap with those observed in disseminated intravascular coagulation syndrome&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">42</span></a> Lippi and Favoro<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">43</span></a> reported a directly proportional association between D-dimer levels and severe respiratory illness in patients with SARS-CoV-2 infection&#44; supporting previous reports showing a link between elevated D-dimer levels and mortality in COVID-19&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">42</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">In humans&#44; ferritin exerts a protective function during infection by limiting the amount of iron available to numerous pathogens&#44;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">44</span></a> explaining also why ferritin levels increase during inflammatory states&#46;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">45</span></a> Very high ferritin levels have been observed in patients with severe COVID-19 and linked to high morbidity and mortality&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">46</span></a></p><p id="par0100" class="elsevierStylePara elsevierViewall">As mentioned&#44; COVID-19 is characterized by a diverse range of biochemical changes&#46; These changes&#44; however&#44; are reminiscent of findings observed in macrophage activation syndrome<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">47</span></a> and highlight the important role of white blood cells&#44; in particular T cells and macrophages&#44; in the exaggerated cytokine and thrombotic immune response associated with COVID-19&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Macrophages and T Cells at the Root of Acro-Ischemic Lesions in COVID-19</span><p id="par0105" class="elsevierStylePara elsevierViewall">Preliminary studies characterizing the novel coronavirus identified the angiotensin converting enzyme 2 &#40;ACE<span class="elsevierStyleInf">2</span>&#41; receptor as the main receptor in SARS-CoV-2 infection&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> SARS-CoV-2 uses the ACE<span class="elsevierStyleInf">2</span> receptor to enter human cells and has no affinity for receptors used by other coronavirus families&#44; such as the dipeptidyl peptidase 4 receptor&#46;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">48</span></a></p><p id="par0110" class="elsevierStylePara elsevierViewall">The ACE<span class="elsevierStyleInf">2</span> receptor is found on the surface of pulmonary epithelial cells&#44; in enterocytes of the small intestine&#44; in arterial and venous endothelial cells&#44; and in arterial smooth muscle cells in numerous organs&#44; including the skin&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">49</span></a> Viral replication within cells causes direct cell injury&#44; triggering the release of proinflammatory alarmins &#40;direct viral effect&#41;&#46; Viral particles can also trigger innate immune responses&#44; including the activation of alveolar macrophages and the complement cascade through the lectin pathway&#46;<a class="elsevierStyleCrossRefs" href="#bib0190"><span class="elsevierStyleSup">38&#44;50</span></a></p><p id="par0115" class="elsevierStylePara elsevierViewall">Complement activation and diverse immune responses promote the recruitment of leukocytes and an exaggerated proliferation of lymphocytes and massive release of proinflammatory cytokines &#40;interleukin &#91;IL&#93; 1B&#44; IL-6&#44; IL-8&#41;&#44; interferon-gamma &#40;IFN-&#947;&#41;&#44; and tumor necrosis factor alpha &#40;TNF-&#945;&#41;&#44; among others&#46; IFN-&#947;&#44; in large quantities&#44; drives macrophage activation and ferritin production&#44;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">45</span></a> IL-6 causes fever&#44;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">51</span></a> and hemophagocytosis causes pancytopenia&#46;<a class="elsevierStyleCrossRefs" href="#bib0235"><span class="elsevierStyleSup">47&#44;52</span></a> Macrophages also release plasminogen activator&#44; and this is possibly one of the many mechanisms that would explain the thrombotic events and elevated D-dimer levels observed in severe COVID-19&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">53</span></a> It could also explain other findings such as the presence of antiphospholipid antibodies in patients with severe disease in the absence of comorbidities&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">54</span></a> Bowles et al&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">55</span></a> in the United Kingdom and Connel et al&#46;<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">56</span></a> in the United States confirmed the presence of antiphospholipid antibodies &#40;especially lupus anticoagulant&#41; in patients with SARS-CoV-2 infection&#46; This might be linked to the observation of acro-ischemic presentations &#40;other than chilblain-like lesions&#41;&#44; necrosis&#44; and even livedo reticularis and racemosa in certain patients with COVID-19 and concomitant multisystemic thrombotic responses&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">Viral sepsis has also been proposed to explain the systemic and cutaneous changes associated with COVID-19&#46;<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">57</span></a> This hypothesis&#44; which came about following multiple reports of multiorgan damage in autopsy studies of patients who had died of severe COVID-19&#44;<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">58</span></a> holds that the massive release of cytokines&#44; in particular TNF-&#945;&#44; would promote the death of infected cells via apoptosis-dependent pathways&#46; In addition&#44; SARS-CoV-2 may also be capable of infecting T cells&#44; leading to lymphopenia&#46;</p><p id="par0125" class="elsevierStylePara elsevierViewall">There is sufficient evidence to support direct viral injury to endothelial cells followed by diffuse endothelial inflammation and consequently vascular endothelial apoptosis&#44;<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">59</span></a> raising the question of whether COVID-19 may actually be an endothelial disease&#46;<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">60</span></a> This theory is supported by reports of death in patients with COVID-19 who had a history of diabetes mellitus or chronic cardiovascular disease and the observation of ischemic cutaneous manifestations&#44; particularly at acral sites&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Association Between IFN and Chilblain-like Lesions</span><p id="par0130" class="elsevierStylePara elsevierViewall">Patients with chilblain-like lesions&#44;<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">30&#8211;32</span></a> apart from being apparently younger&#44; experience mild COVID-19&#44; while those with severe acro-ischemic manifestations&#44; such as gangrene<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a> and retiform purpura&#44;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">38</span></a> develop more severe disease&#46; The milder forms of disease associated with chilblain-like lesions may be linked to type I IFN&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">Kolivras et al&#46;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">33</span></a> highlighted the robust activation of type I IFN in SARS-CoV-2 infection&#44; stating that a similar response was induced in many other acute viral infections&#46;<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">61</span></a> Type I IFN levels are elevated in lupus erythematosus and interferonopathies such as Aicardi-Gouti&#232;res syndrome&#44; which is also characterized by microangiopathic changes at acral sites&#46;<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">62</span></a> The authors hypothesized that these changes are the result of early type I IFN responses&#44; which would also explain the mild disease course&#44; as IFN exerts an antiviral effect&#46; In addition&#44; because early type I IFN responses are capable of suppressing the uncontrolled release of diverse proinflammatory cytokines&#44; they would reduce the risk of a cytokine storm&#46; Elderly patients&#44; however&#44; or patients with comorbidities that alter the functioning of the immune system&#44; would generate a delayed type I IFN response&#44; leading to the release of cytokines&#44; macrophage activation syndrome&#44; elevated ferritin and D-dimer levels&#44; true acro-ischemic lesions&#44; and a much worse prognosis&#46;</p></span></span></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Discussion</span><p id="par0140" class="elsevierStylePara elsevierViewall">The COVID-19 pandemic has created enormous challenges for health care professionals&#44; including the need to keep abreast with the vast spectrum of clinical manifestations associated with this disease&#46; COVID-19 is a multisystemic disease that affects multiple organs&#44; including the skin&#46; The occurrence of cutaneous manifestations&#44; however&#44; represents an advantage&#44; as their recognition can lead to early suspicion of disease in some cases and provide clues about individual immune responses or complications in others&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">Based on the pathophysiological mechanisms hypothesized&#44; we propose classifying the various cutaneous manifestations of COVID-19 into 2 groups&#58; <span class="elsevierStyleItalic">1</span>&#41; manifestations primarily linked to a direct cytopathogenic effect on cells such as keratinocytes&#44; which are involved in many known viral infections &#40;morbilliform or urticarial rashes&#44; reactions similar to drug eruptions&#44; varicella-like lesions&#41; and <span class="elsevierStyleItalic">2</span>&#41; manifestations linked to an uncontrolled release of cytokines due to alterations in specific white blood cells&#44; such as T cells and macrophages&#46; This second group could be divided into a further 2 groups&#58; <span class="elsevierStyleItalic">1</span>&#41; manifestations characterized by features similar to those seen in macrophage activation syndrome &#40;acral ischemia&#44; gangrene&#44; retiform purple&#44; livedo racemosa&#41; and associated with poor outcomes in terms of morbidity and mortality and <span class="elsevierStyleItalic">2</span>&#41; cutaneous manifestations with a mild&#44; self-limiting disease course&#44; observed in young patients and linked to the activation of an early type I IFN response &#40;chilblain-like lesions&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0035">Fig&#46; 7</a>&#41;&#46; This hypothesis is one of the first in the literature to provide a possible explanation of the pathophysiological mechanisms underlying the main cutaneous manifestations of COVID-19&#59; it also provides a means of classifying these manifestations and establishing their possible prognostic value&#46;</p><elsevierMultimedia ident="fig0035"></elsevierMultimedia><p id="par0150" class="elsevierStylePara elsevierViewall">We believe that it is paramount for physicians&#44; nurses&#44; respiratory therapists&#44; health care professionals still in training&#44; and even members of the general population to be aware of the relationship between SARS-CoV-2 infection and the skin and its various manifestations&#46; Heightened awareness will promote an active search for manifestations and a detailed study of cases&#44; adding to the scientific knowledge and our understanding of the pathophysiology of COVID-19 and ultimately contributing to the development of effective treatments and protocols that will mitigate the complications of this infection&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Funding</span><p id="par0155" class="elsevierStylePara elsevierViewall">This study did not receive any specific funding from public sector bodies or commercial or nonprofit entities&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Conflicts of Interest</span><p id="par0160" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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              "titulo" => "Cutaneous Manifestations in COVID-19"
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                  "titulo" => "SARS-CoV-2 Infection and Onset of Nonspecific Rashes"
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                  "titulo" => "Pathophysiology of SARS-CoV-2 Infection and Possible Association With Cutaneous Manifestations"
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                1 => array:2 [
                  "identificador" => "sec0045"
                  "titulo" => "Macrophages and T Cells at the Root of Acro-Ischemic Lesions in COVID-19"
                ]
                2 => array:2 [
                  "identificador" => "sec0050"
                  "titulo" => "Association Between IFN and Chilblain-like Lesions"
                ]
              ]
            ]
          ]
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          "identificador" => "sec0055"
          "titulo" => "Discussion"
        ]
        8 => array:2 [
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          "titulo" => "Funding"
        ]
        9 => array:2 [
          "identificador" => "sec0065"
          "titulo" => "Conflicts of Interest"
        ]
        10 => array:2 [
          "identificador" => "xack522220"
          "titulo" => "Acknowledgments"
        ]
        11 => array:1 [
          "titulo" => "References"
        ]
      ]
    ]
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    "tienePdf" => true
    "fechaRecibido" => "2020-05-06"
    "fechaAceptado" => "2020-11-15"
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          "clase" => "keyword"
          "titulo" => "Keywords"
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          "palabras" => array:4 [
            0 => "Coronavirus"
            1 => "COVID-19"
            2 => "Severe acute respiratory syndrome-related coronavirus"
            3 => "Skin"
          ]
        ]
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        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Palabras claves"
          "identificador" => "xpalclavsec1354284"
          "palabras" => array:4 [
            0 => "Coronavirus"
            1 => "infecciones por coronavirus COVID-19"
            2 => "virus del S&#237;ndrome Respiratorio Agudo Severo"
            3 => "piel"
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        ]
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      "en" => array:2 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">The rapid spread of severe acute respiratory syndrome coronavirus 2 &#40;SARS-CoV-2&#41; infections soon led to a pandemic with serious health&#44; economic&#44; political&#44; and cultural repercussions across the globe&#46; The disease caused by SARS-CoV-2&#44; coronavirus disease 2019 &#40;COVID-19&#41;&#44; is a multisystemic disease that requires a multidisciplinary approach involving specialists from all fields and levels of care&#46; In this article&#44; we review the literature on the diverse cutaneous manifestations associated with COVID-19&#46; We also describe the pathophysiologic mechanisms proposed to date and their possible association with these manifestations&#46; Finally&#44; we propose a system for classifying the cutaneous manifestations of COVID-19 according to their underlying pathophysiologic mechanisms and prognosis&#46;</p></span>"
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        "titulo" => "Resumen"
        "resumen" => "<span id="abst0015" class="elsevierStyleSection elsevierViewall"><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">La infecci&#243;n por SARS-CoV-2 se ha convertido r&#225;pidamente en una pandemia con importantes implicaciones en &#225;mbitos sanitarios&#44; econ&#243;micos&#44; pol&#237;ticos y culturales en todo el planeta&#46; La enfermedad que produce&#44; llamada COVID-19&#44; es considerada actualmente una patolog&#237;a florida y de obligatorio manejo multidisciplinario por todas las especialidades m&#233;dicas y de servicios de salud&#46;</p><p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Este art&#237;culo presenta una revisi&#243;n bibliogr&#225;fica de las variadas manifestaciones cut&#225;neas a causa de la COVID-19&#46; Posteriormente&#44; se mencionan los diversos engranajes fisiopatol&#243;gicos que se han postulado hasta el momento y su posible relaci&#243;n con los hallazgos de la enfermedad en la piel&#46; Por &#250;ltimo&#44; se propone una clasificaci&#243;n de las manifestaciones cut&#225;neas seg&#250;n mecanismos fisiopatol&#243;gicos de base y pron&#243;stico de la enfermedad&#46;</p></span>"
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      0 => array:2 [
        "etiqueta" => "&#9734;"
        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Gonz&#225;lez Gonz&#225;lez F&#44; Cort&#233;s Correa C&#44; Pe&#241;aranda Contreras E&#46; Manifestaciones cut&#225;neas en pacientes con COVID-19&#58; caracter&#237;sticas cl&#237;nicas y mecanismos fisiopatol&#243;gicos postulados&#46; Actas Dermosifiliogr&#46; 2021&#59;112&#58;314&#8211;323&#46;</p>"
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">A&#44; Hardened erythematous-yellowish plaques on the heels&#46; Source&#58; Est&#233;banez et al&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> B&#44; 67-year-old man with unilateral livedo reticularis on the right thigh&#46; The patient also had gross hematuria&#46; The hematuria and livedo both resolved within 24&#8239;hours&#46; Source&#58; Manalo et al&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a></p>"
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                      "titulo" => "A novel coronavirus from patients with pneumonia in China&#44; 2019"
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                          "autores" => array:6 [
                            0 => "N&#46; Zhu"
                            1 => "D&#46; Zhang"
                            2 => "W&#46; Wang"
                            3 => "X&#46; Li"
                            4 => "B&#46; Yang"
                            5 => "J&#46; Song"
                          ]
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                      "doi" => "10.1056/NEJMoa2001017"
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                            0 => "P&#46; Zhou"
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                            2 => "X&#46; Wang"
                            3 => "B&#46; Hu"
                            4 => "L&#46; Zhang"
                            5 => "W&#46; Zhang"
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                          "autores" => array:5 [
                            0 => "N&#46; Petrosillo"
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                            2 => "O&#46; Ergonul"
                            3 => "G&#46; Ippolito"
                            4 => "E&#46; Petersen"
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                      "titulo" => "The incubation period of coronavirus disease 2019 &#40;COVID-19&#41; from publicly reported confirmed cases&#58; Estimation and application"
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        "texto" => "<p id="par0165" class="elsevierStylePara elsevierViewall">To all the frontline health care professionals involved in caring for patients with COVID-19&#59; their contribution to the history of medicine is invaluable&#46;</p>"
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Review
Cutaneous Manifestations in Patients With COVID-19: Clinical Characteristics and Possible Pathophysiologic Mechanisms
Manifestaciones cutáneas en pacientes con COVID-19: características clínicas y mecanismos fisiopatológicos postulados
F González Gonzáleza,
Autor para correspondencia
fegonzalezg@unal.edu.co

Corresponding author.
, C Cortés Correab,c, E Peñaranda Contrerasc,d
a Dermatología, Facultad de Medicina, Universidad Nacional de Colombia, Bogotá, Colombia
b Dermatología, Facultad de Medicina, Universidad Nacional de Colombia, Bogotá, Colombia
c Hospital Universitario de la Samaritana E.S.E., Bogotá, Colombia
d Dermatología - Oncología, Facultad de Medicina, Universidad Nacional de Colombia, Bogotá, Colombia
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SARS-CoV-1 and Middle East Respiratory Syndrome coronavirus &#40;MERS-CoV&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#44;4</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Although SARS-CoV-2 is associated with a case fatality rate of 2&#46;3&#37;&#44;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> lower than that of SARS-CoV-1 &#40;9&#46;5&#37;&#41; and MERS-CoV &#40;34&#46;4&#37;&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> it is highly contagious and quickly spread outside China&#59; its high transmissibility&#8212;higher than that of SARS-CoV-1<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a>&#8212;can be partly explained by the higher viral loads in the respiratory tract&#46; SARS-CoV-2 can also survive in aerosols for more than 3&#8239;hours&#44; remains viable on a variety of surfaces for 72&#8239;hours&#44; and has a relatively short incubation period &#40;&#60;&#8239;2 weeks&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Early reports of coronavirus disease 2019 &#40;COVID-19&#41;&#44; the disease caused by SARS-CoV-2&#44; indicated that most patients experienced fever&#44; rhinorrhea&#44; a cough without expectoration&#44; asthenia&#44; and adynamia&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> A small proportion required hospitalization due to severe pneumonia&#46; In a cohort of 70&#8239;000 patients with SARS-CoV-2 infection in China&#44; Wu et al&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> reported that 14&#37; of patients developed severe pneumonia &#40;dyspnea&#44; tachypnea&#44; desaturation&#44; and a decreased arterial oxygen partial pressure to fractional inspired oxygen ratio&#41; and that 5&#37; required critical care&#46; The case fatality rate was 2&#46;3&#37; for the general population and 14&#37; for patients aged 80 years or older&#46; Their findings were corroborated by later reports from Europe&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">The main risk factors for severe COVID-19 include male sex&#44; diabetes&#44; high blood pressure&#44; chronic lung disease&#44; and cardiovascular disease&#46;<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">11&#44;12</span></a> Children younger than 10 years have mild symptoms and are much less likely than adults to develop complications or die&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">Reports from Asia&#44; Europe&#44; and the United States have described a wide range of cutaneous manifestations associated with COVID-19&#46; Although these manifestations were initially considered to be nonspecific&#44; the publication of an increasing number of cases revealed an apparent pattern and possibly even an association with prognosis&#46; In this article&#44; we review the literature on the diverse cutaneous manifestations described to date in patients with COVID-19&#46; We then outline the different pathophysiologic mechanisms and hypotheses proposed so far to explain their occurrence&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Results</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Cutaneous Manifestations in COVID-19</span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">SARS-CoV-2 Infection and Onset of Nonspecific Rashes</span><p id="par0030" class="elsevierStylePara elsevierViewall">There are 39 coronavirus species&#46; Seven of these&#44; including SARS-CoV-1&#44; SARS-CoV-2&#44; and MERS-CoV&#44; affect humans&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> The other viruses&#8212;HCoV-229E&#44; HCoV-OC43&#44; HCoV-NL63&#44; and HCoV-HKU1&#8212;cause mild respiratory conditions such as the common cold&#46; Like other respiratory viruses&#44; many coronaviruses probably also cause viral rashes that go undetected because of the lack of specific testing&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">The first report mentioning cutaneous manifestations in patients with COVID-19 was published by Guan et al&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> in February 2020&#46; The authors analyzed data for 1099 patients infected with SARS-CoV-2 and described 2 cases of skin lesions&#46; They did not&#44; however&#44; specify the type of lesions or describe their clinical characteristics or time of onset&#44; probably explaining why this early report was somewhat overlooked&#46; The publication was followed by a report of a patient in Thailand presenting with a &#8220;morbilliform rash and multiple petechiae&#8221; and a low platelet count who was initially diagnosed with dengue and assigned to outpatient care&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> The patient&#44; however&#44; returned with respiratory symptoms and was diagnosed with SARS-CoV-2 infection by reverse-transcript polymerase chain reaction &#40;PCR&#41;&#46; This report alerted physicians to the importance of investigating cutaneous manifestations in patients with COVID-19&#46;<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">17&#44;18</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">The first large report of cutaneous manifestations in COVID-19 came from a cohort of 88 patients in Italy&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> Of these&#44; 18 &#40;20&#46;4&#37;&#41; had developed cutaneous manifestations&#58; 8 during hospitalization and 10 following discharge&#46; There were 14 cases of &#8220;erythematous rash&#8221;&#44; 3 of &#8220;widespread urticaria&#8221;&#44; and 1 of &#8220;chickenpox-like vesicles&#8221;&#46; The vast majority of patients had trunk lesions&#44; which were largely asymptomatic&#44; resolved spontaneously&#44; and did not appear to be associated with disease severity&#46; Unfortunately&#44; no photographs were taken due to the hospital policies in place at the time of the study&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">As the days passed&#44; new reports emerged of patients with confirmed SARS-CoV-2 infection and a range of very different cutaneous manifestations&#44; including pruritic erythematous-yellowish plaques on the heels &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>A&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> a morbilliform rash sparing acral sites&#44;<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a> a generalized maculopapular morbilliform rash with cephalocaudal progress&#44;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> urticaria-like lesions&#44;<a class="elsevierStyleCrossRefs" href="#bib0115"><span class="elsevierStyleSup">23&#44;24</span></a> a rash reminiscent of symmetrical drug-related intertriginous flexural exanthema&#44;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> and even livedo reticularis on the lower extremities &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>B&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> As in the previous cases&#44; biopsies were not performed due to hospital policies and the mild&#44; self-limiting nature of the lesions&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0050" class="elsevierStylePara elsevierViewall">In April&#44; the <span class="elsevierStyleItalic">Journal of the American Academy of Dermatology</span> published a series of 22 patients with COVID-19 who developed a mild varicella-like rash after a median of 3 days from the onset of systemic symptoms&#59; the rash cleared after a median of 8 days&#44; leaving no residual scarring&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a> Most of the patients were male &#40;72&#46;7&#37;&#41; and the mean age was 60 years&#46; The varicella-like lesions were predominantly vesicles and were scattered in 72&#46;7&#37; of cases and diffuse in 27&#46;3&#37;&#46; The trunk was affected in all cases&#46; None of the reports mentioned facial or mucosal involvement &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>A and B&#41;&#46; The most common symptom&#44; present in almost half of the patients&#44; was mild pruritus&#46; A skin biopsy performed in 7 patients showed findings consistent with an acute viral infection &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>C and D&#41;&#46; The authors suggested that this type of rash might be a specific manifestation of SARS-CoV-2 infection and as such could be useful for raising suspicion of COVID-19 in patients with mild disease&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">A later publication described the case of a man in the fourth decade of life with PCR-confirmed SARS-CoV-2 infection&#44; fever&#44; and concomitant nonpruritic&#44; annular&#44; circinate&#44; erythematous-edematous fixed plaques on the neck&#44; thorax&#44; abdomen&#44; and upper limbs &#40;symmetric distribution&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>A-C&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a> The lesions cleared after 7 days&#46; The biopsy findings were consistent with a viral rash &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>D&#41;&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Cutaneous Manifestations Associated With Thrombosis or Microangiopathic Changes and Chilblain-like Lesions</span><p id="par0060" class="elsevierStylePara elsevierViewall">The Chinese group led by Zhang<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a> published a retrospective review of 7 patients with COVID-19 and pneumonia treated at an intensive care unit in Wuhan&#46; The patients had multiple acro-ischemic manifestations&#44; including acrocyanosis&#44; retiform purpura&#44; and gangrene &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>&#41;&#46; Clinical and laboratory data were evaluated on admission to hospital&#44; at the onset of the cutaneous manifestations&#44; and after the use of anticoagulation therapy&#46; They showed D-dimer&#44; fibrinogen&#44; and fibrinogen degradation product alterations related to the sequential events described&#46; Five of the patients &#40;71&#46;42&#37;&#41; died&#46; This was the first step in the formulation of a hypothesis on the existence of a hypercoagulable state per se in patients with SARS-CoV-2 infection&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia><p id="par0065" class="elsevierStylePara elsevierViewall">Around the same time&#44; multiple reports began to emerge from Europe&#44; the Middle East&#44; and the United States of chilblain-like lesions in young people who had been in close contact with a patient with confirmed or probable SARS-CoV-2 infection&#46; The symptoms varied&#44; but the chief complaints were pain and a burning sensation in the skin&#59; the lesions resolved spontaneously and none of the patients developed SARS-CoV-2 pneumonia&#46;<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">30&#8211;32</span></a></p><p id="par0070" class="elsevierStylePara elsevierViewall">Kolivras et al&#46;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">33</span></a> reported the case of a young man who developed painful&#44; acute-onset&#44; violaceous plaques on the toes and lateral aspect of the feet &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>A and B&#41; 3 days after the onset of upper respiratory symptoms&#46; A skin biopsy showed findings consistent with chilblain lupus &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>C and D&#41;&#46; The nasopharyngeal swab collected on admission was positive for SARS-CoV-2&#46;</p><elsevierMultimedia ident="fig0025"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">In view of the enormous impact of the pandemic on the European continent&#44; numerous groups started to publish studies aimed at characterizing the chilblain-like lesions observed in patients with COVID-19&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">34</span></a> In Italy&#44; Recalcati et al&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> and Tosti et al&#46;<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">35</span></a> reported that these lesions were more common in younger patients &#40;especially children &#91;78&#46;5&#37;&#93;&#41;&#44; predominantly involved the feet &#40;71&#37; of cases&#41;&#44; were self-limiting&#44; and were associated with normal blood tests and an absence of systemic symptoms&#46; A French study of skin lesions observed in 277 patients during 3 weeks of the COVID-19 pandemic found that 142 patients had acral lesions and that 106 of these &#40;75&#37;&#41; were painful erythematous-violaceous edematous macules and papules consistent with chilblain lupus&#46;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">36</span></a> Fern&#225;ndez-Nieto et al<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">37</span></a> studied 132 nonhospitalized patients who consulted for acro-ischemic lesions over a period of 5 weeks&#46; The mean age of the patients was 19&#46;9 years&#59; 40&#46;9&#37; had been in close contact with a patient with confirmed SARS-CoV-2 infection and 14&#46;4&#37; tested positive&#46; Over 90&#37; of the lesions affected the fingers or toes&#44; but mostly the toes &#40;81&#46;8&#37;&#41;&#46; Similarly to the other cases reported&#44; the patients experienced mild disease&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Magro et al&#46;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">38</span></a> reported on patients with COVID-19 who developed cutaneous manifestations consistent with a procoagulant or microangiopathic state&#46; A skin biopsy was performed in 3 patients who developed retiform purpura or livedo racemosa &#40;<a class="elsevierStyleCrossRef" href="#fig0030">Fig&#46; 6</a>A&#41; associated with elevated D-dimer levels during the course of their respiratory illness&#44; with findings showing pauci-inflammatory thrombogenic vasculopathy and C5b-9 and C4d deposition &#40;<a class="elsevierStyleCrossRef" href="#fig0030">Fig&#46; 6</a>B and C&#41;&#46; This observation sparked the hypothesis of a link between mechanisms dependent on the alternative or lectin complement pathways and thrombotic events in patients with SARS-CoV-2 infection&#44; and subsequently provided an explanation for the existence of procoagulant states in other organs&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">39</span></a></p><elsevierMultimedia ident="fig0030"></elsevierMultimedia></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Spanish Consensus on the Classification of Cutaneous Manifestations of COVID-19</span><p id="par0085" class="elsevierStylePara elsevierViewall">The <span class="elsevierStyleItalic">British Journal of Dermatology</span> published the results of a Spanish consensus study of 375 patients with confirmed or suspected SARS-CoV-2 infection who developed cutaneous manifestations without a clear explanation&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">40</span></a> Numerous factors were evaluated over a period of 2 weeks&#44; including clinical manifestations&#44; time of onset in relation to other symptoms&#44; demographics&#44; and associations with disease course and outcomes&#46; The group&#44; led by Galv&#225;n Casa&#44; divided the manifestations into 5 clinical patterns&#58; <span class="elsevierStyleItalic">1</span>&#41; pseudo-chilblains &#40;19&#37;&#41;&#44; <span class="elsevierStyleItalic">2</span>&#41; vesicular eruptions &#40;9&#37;&#41;&#44; <span class="elsevierStyleItalic">3</span>&#41; urticarial lesions &#40;19&#37;&#41;&#44; <span class="elsevierStyleItalic">4</span>&#41; maculopapular eruptions &#40;47&#37;&#41;&#44; and <span class="elsevierStyleItalic">5</span>&#41; livedoid or necrotic lesions &#40;6&#37;&#41;&#46; They found that livedoid and necrotic lesions affected older patients &#40;mean age&#44; 63 years&#41; with severe disease &#40;mortality rate&#44; 10&#37;&#41;&#44; while pseudo-chilblain lesions &#40;acral areas of erythema and edema with vesicles or pustules&#41; were more common after the onset of respiratory symptoms &#40;59&#37; of cases&#41; and occurred in young patients &#40;mean age&#44; 21&#46;8 years&#41; with mild COVID-19&#46; The survival rate of patients with maculopapular eruptions was 98&#37;&#46; The Spanish findings were consistent with reports from other authors&#44; especially in terms of the mild nature of these chilblain-like lesions&#46;<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">30&#8211;33</span></a></p></span></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Pathophysiological Findings</span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Pathophysiology of SARS-CoV-2 Infection and Possible Association With Cutaneous Manifestations</span><p id="par0090" class="elsevierStylePara elsevierViewall">Laboratory findings in patients with severe SARS-CoV-2 infection include leukocytosis&#44; neutrophilia&#44; lymphopenia&#44; thrombocytopenia&#44; increased lactate dehydrogenase and procalcitonin levels&#44; and D-dimer and fibrinogen degradation product alterations&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">41</span></a> In some cases&#44; these findings overlap with those observed in disseminated intravascular coagulation syndrome&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">42</span></a> Lippi and Favoro<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">43</span></a> reported a directly proportional association between D-dimer levels and severe respiratory illness in patients with SARS-CoV-2 infection&#44; supporting previous reports showing a link between elevated D-dimer levels and mortality in COVID-19&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">42</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">In humans&#44; ferritin exerts a protective function during infection by limiting the amount of iron available to numerous pathogens&#44;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">44</span></a> explaining also why ferritin levels increase during inflammatory states&#46;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">45</span></a> Very high ferritin levels have been observed in patients with severe COVID-19 and linked to high morbidity and mortality&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">46</span></a></p><p id="par0100" class="elsevierStylePara elsevierViewall">As mentioned&#44; COVID-19 is characterized by a diverse range of biochemical changes&#46; These changes&#44; however&#44; are reminiscent of findings observed in macrophage activation syndrome<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">47</span></a> and highlight the important role of white blood cells&#44; in particular T cells and macrophages&#44; in the exaggerated cytokine and thrombotic immune response associated with COVID-19&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Macrophages and T Cells at the Root of Acro-Ischemic Lesions in COVID-19</span><p id="par0105" class="elsevierStylePara elsevierViewall">Preliminary studies characterizing the novel coronavirus identified the angiotensin converting enzyme 2 &#40;ACE<span class="elsevierStyleInf">2</span>&#41; receptor as the main receptor in SARS-CoV-2 infection&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> SARS-CoV-2 uses the ACE<span class="elsevierStyleInf">2</span> receptor to enter human cells and has no affinity for receptors used by other coronavirus families&#44; such as the dipeptidyl peptidase 4 receptor&#46;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">48</span></a></p><p id="par0110" class="elsevierStylePara elsevierViewall">The ACE<span class="elsevierStyleInf">2</span> receptor is found on the surface of pulmonary epithelial cells&#44; in enterocytes of the small intestine&#44; in arterial and venous endothelial cells&#44; and in arterial smooth muscle cells in numerous organs&#44; including the skin&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">49</span></a> Viral replication within cells causes direct cell injury&#44; triggering the release of proinflammatory alarmins &#40;direct viral effect&#41;&#46; Viral particles can also trigger innate immune responses&#44; including the activation of alveolar macrophages and the complement cascade through the lectin pathway&#46;<a class="elsevierStyleCrossRefs" href="#bib0190"><span class="elsevierStyleSup">38&#44;50</span></a></p><p id="par0115" class="elsevierStylePara elsevierViewall">Complement activation and diverse immune responses promote the recruitment of leukocytes and an exaggerated proliferation of lymphocytes and massive release of proinflammatory cytokines &#40;interleukin &#91;IL&#93; 1B&#44; IL-6&#44; IL-8&#41;&#44; interferon-gamma &#40;IFN-&#947;&#41;&#44; and tumor necrosis factor alpha &#40;TNF-&#945;&#41;&#44; among others&#46; IFN-&#947;&#44; in large quantities&#44; drives macrophage activation and ferritin production&#44;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">45</span></a> IL-6 causes fever&#44;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">51</span></a> and hemophagocytosis causes pancytopenia&#46;<a class="elsevierStyleCrossRefs" href="#bib0235"><span class="elsevierStyleSup">47&#44;52</span></a> Macrophages also release plasminogen activator&#44; and this is possibly one of the many mechanisms that would explain the thrombotic events and elevated D-dimer levels observed in severe COVID-19&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">53</span></a> It could also explain other findings such as the presence of antiphospholipid antibodies in patients with severe disease in the absence of comorbidities&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">54</span></a> Bowles et al&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">55</span></a> in the United Kingdom and Connel et al&#46;<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">56</span></a> in the United States confirmed the presence of antiphospholipid antibodies &#40;especially lupus anticoagulant&#41; in patients with SARS-CoV-2 infection&#46; This might be linked to the observation of acro-ischemic presentations &#40;other than chilblain-like lesions&#41;&#44; necrosis&#44; and even livedo reticularis and racemosa in certain patients with COVID-19 and concomitant multisystemic thrombotic responses&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">Viral sepsis has also been proposed to explain the systemic and cutaneous changes associated with COVID-19&#46;<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">57</span></a> This hypothesis&#44; which came about following multiple reports of multiorgan damage in autopsy studies of patients who had died of severe COVID-19&#44;<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">58</span></a> holds that the massive release of cytokines&#44; in particular TNF-&#945;&#44; would promote the death of infected cells via apoptosis-dependent pathways&#46; In addition&#44; SARS-CoV-2 may also be capable of infecting T cells&#44; leading to lymphopenia&#46;</p><p id="par0125" class="elsevierStylePara elsevierViewall">There is sufficient evidence to support direct viral injury to endothelial cells followed by diffuse endothelial inflammation and consequently vascular endothelial apoptosis&#44;<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">59</span></a> raising the question of whether COVID-19 may actually be an endothelial disease&#46;<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">60</span></a> This theory is supported by reports of death in patients with COVID-19 who had a history of diabetes mellitus or chronic cardiovascular disease and the observation of ischemic cutaneous manifestations&#44; particularly at acral sites&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Association Between IFN and Chilblain-like Lesions</span><p id="par0130" class="elsevierStylePara elsevierViewall">Patients with chilblain-like lesions&#44;<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">30&#8211;32</span></a> apart from being apparently younger&#44; experience mild COVID-19&#44; while those with severe acro-ischemic manifestations&#44; such as gangrene<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a> and retiform purpura&#44;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">38</span></a> develop more severe disease&#46; The milder forms of disease associated with chilblain-like lesions may be linked to type I IFN&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">Kolivras et al&#46;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">33</span></a> highlighted the robust activation of type I IFN in SARS-CoV-2 infection&#44; stating that a similar response was induced in many other acute viral infections&#46;<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">61</span></a> Type I IFN levels are elevated in lupus erythematosus and interferonopathies such as Aicardi-Gouti&#232;res syndrome&#44; which is also characterized by microangiopathic changes at acral sites&#46;<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">62</span></a> The authors hypothesized that these changes are the result of early type I IFN responses&#44; which would also explain the mild disease course&#44; as IFN exerts an antiviral effect&#46; In addition&#44; because early type I IFN responses are capable of suppressing the uncontrolled release of diverse proinflammatory cytokines&#44; they would reduce the risk of a cytokine storm&#46; Elderly patients&#44; however&#44; or patients with comorbidities that alter the functioning of the immune system&#44; would generate a delayed type I IFN response&#44; leading to the release of cytokines&#44; macrophage activation syndrome&#44; elevated ferritin and D-dimer levels&#44; true acro-ischemic lesions&#44; and a much worse prognosis&#46;</p></span></span></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Discussion</span><p id="par0140" class="elsevierStylePara elsevierViewall">The COVID-19 pandemic has created enormous challenges for health care professionals&#44; including the need to keep abreast with the vast spectrum of clinical manifestations associated with this disease&#46; COVID-19 is a multisystemic disease that affects multiple organs&#44; including the skin&#46; The occurrence of cutaneous manifestations&#44; however&#44; represents an advantage&#44; as their recognition can lead to early suspicion of disease in some cases and provide clues about individual immune responses or complications in others&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">Based on the pathophysiological mechanisms hypothesized&#44; we propose classifying the various cutaneous manifestations of COVID-19 into 2 groups&#58; <span class="elsevierStyleItalic">1</span>&#41; manifestations primarily linked to a direct cytopathogenic effect on cells such as keratinocytes&#44; which are involved in many known viral infections &#40;morbilliform or urticarial rashes&#44; reactions similar to drug eruptions&#44; varicella-like lesions&#41; and <span class="elsevierStyleItalic">2</span>&#41; manifestations linked to an uncontrolled release of cytokines due to alterations in specific white blood cells&#44; such as T cells and macrophages&#46; This second group could be divided into a further 2 groups&#58; <span class="elsevierStyleItalic">1</span>&#41; manifestations characterized by features similar to those seen in macrophage activation syndrome &#40;acral ischemia&#44; gangrene&#44; retiform purple&#44; livedo racemosa&#41; and associated with poor outcomes in terms of morbidity and mortality and <span class="elsevierStyleItalic">2</span>&#41; cutaneous manifestations with a mild&#44; self-limiting disease course&#44; observed in young patients and linked to the activation of an early type I IFN response &#40;chilblain-like lesions&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0035">Fig&#46; 7</a>&#41;&#46; This hypothesis is one of the first in the literature to provide a possible explanation of the pathophysiological mechanisms underlying the main cutaneous manifestations of COVID-19&#59; it also provides a means of classifying these manifestations and establishing their possible prognostic value&#46;</p><elsevierMultimedia ident="fig0035"></elsevierMultimedia><p id="par0150" class="elsevierStylePara elsevierViewall">We believe that it is paramount for physicians&#44; nurses&#44; respiratory therapists&#44; health care professionals still in training&#44; and even members of the general population to be aware of the relationship between SARS-CoV-2 infection and the skin and its various manifestations&#46; Heightened awareness will promote an active search for manifestations and a detailed study of cases&#44; adding to the scientific knowledge and our understanding of the pathophysiology of COVID-19 and ultimately contributing to the development of effective treatments and protocols that will mitigate the complications of this infection&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Funding</span><p id="par0155" class="elsevierStylePara elsevierViewall">This study did not receive any specific funding from public sector bodies or commercial or nonprofit entities&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Conflicts of Interest</span><p id="par0160" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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              "titulo" => "Cutaneous Manifestations in COVID-19"
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                  "titulo" => "SARS-CoV-2 Infection and Onset of Nonspecific Rashes"
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                  "titulo" => "Pathophysiology of SARS-CoV-2 Infection and Possible Association With Cutaneous Manifestations"
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                1 => array:2 [
                  "identificador" => "sec0045"
                  "titulo" => "Macrophages and T Cells at the Root of Acro-Ischemic Lesions in COVID-19"
                ]
                2 => array:2 [
                  "identificador" => "sec0050"
                  "titulo" => "Association Between IFN and Chilblain-like Lesions"
                ]
              ]
            ]
          ]
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          "identificador" => "sec0055"
          "titulo" => "Discussion"
        ]
        8 => array:2 [
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          "titulo" => "Funding"
        ]
        9 => array:2 [
          "identificador" => "sec0065"
          "titulo" => "Conflicts of Interest"
        ]
        10 => array:2 [
          "identificador" => "xack522220"
          "titulo" => "Acknowledgments"
        ]
        11 => array:1 [
          "titulo" => "References"
        ]
      ]
    ]
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    "tienePdf" => true
    "fechaRecibido" => "2020-05-06"
    "fechaAceptado" => "2020-11-15"
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          "clase" => "keyword"
          "titulo" => "Keywords"
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          "palabras" => array:4 [
            0 => "Coronavirus"
            1 => "COVID-19"
            2 => "Severe acute respiratory syndrome-related coronavirus"
            3 => "Skin"
          ]
        ]
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        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Palabras claves"
          "identificador" => "xpalclavsec1354284"
          "palabras" => array:4 [
            0 => "Coronavirus"
            1 => "infecciones por coronavirus COVID-19"
            2 => "virus del S&#237;ndrome Respiratorio Agudo Severo"
            3 => "piel"
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        ]
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      "en" => array:2 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">The rapid spread of severe acute respiratory syndrome coronavirus 2 &#40;SARS-CoV-2&#41; infections soon led to a pandemic with serious health&#44; economic&#44; political&#44; and cultural repercussions across the globe&#46; The disease caused by SARS-CoV-2&#44; coronavirus disease 2019 &#40;COVID-19&#41;&#44; is a multisystemic disease that requires a multidisciplinary approach involving specialists from all fields and levels of care&#46; In this article&#44; we review the literature on the diverse cutaneous manifestations associated with COVID-19&#46; We also describe the pathophysiologic mechanisms proposed to date and their possible association with these manifestations&#46; Finally&#44; we propose a system for classifying the cutaneous manifestations of COVID-19 according to their underlying pathophysiologic mechanisms and prognosis&#46;</p></span>"
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        "titulo" => "Resumen"
        "resumen" => "<span id="abst0015" class="elsevierStyleSection elsevierViewall"><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">La infecci&#243;n por SARS-CoV-2 se ha convertido r&#225;pidamente en una pandemia con importantes implicaciones en &#225;mbitos sanitarios&#44; econ&#243;micos&#44; pol&#237;ticos y culturales en todo el planeta&#46; La enfermedad que produce&#44; llamada COVID-19&#44; es considerada actualmente una patolog&#237;a florida y de obligatorio manejo multidisciplinario por todas las especialidades m&#233;dicas y de servicios de salud&#46;</p><p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Este art&#237;culo presenta una revisi&#243;n bibliogr&#225;fica de las variadas manifestaciones cut&#225;neas a causa de la COVID-19&#46; Posteriormente&#44; se mencionan los diversos engranajes fisiopatol&#243;gicos que se han postulado hasta el momento y su posible relaci&#243;n con los hallazgos de la enfermedad en la piel&#46; Por &#250;ltimo&#44; se propone una clasificaci&#243;n de las manifestaciones cut&#225;neas seg&#250;n mecanismos fisiopatol&#243;gicos de base y pron&#243;stico de la enfermedad&#46;</p></span>"
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      0 => array:2 [
        "etiqueta" => "&#9734;"
        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Gonz&#225;lez Gonz&#225;lez F&#44; Cort&#233;s Correa C&#44; Pe&#241;aranda Contreras E&#46; Manifestaciones cut&#225;neas en pacientes con COVID-19&#58; caracter&#237;sticas cl&#237;nicas y mecanismos fisiopatol&#243;gicos postulados&#46; Actas Dermosifiliogr&#46; 2021&#59;112&#58;314&#8211;323&#46;</p>"
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">A&#44; Hardened erythematous-yellowish plaques on the heels&#46; Source&#58; Est&#233;banez et al&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> B&#44; 67-year-old man with unilateral livedo reticularis on the right thigh&#46; The patient also had gross hematuria&#46; The hematuria and livedo both resolved within 24&#8239;hours&#46; Source&#58; Manalo et al&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a></p>"
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                      "titulo" => "A novel coronavirus from patients with pneumonia in China&#44; 2019"
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                          "autores" => array:6 [
                            0 => "N&#46; Zhu"
                            1 => "D&#46; Zhang"
                            2 => "W&#46; Wang"
                            3 => "X&#46; Li"
                            4 => "B&#46; Yang"
                            5 => "J&#46; Song"
                          ]
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                      "doi" => "10.1056/NEJMoa2001017"
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                            0 => "P&#46; Zhou"
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                            2 => "X&#46; Wang"
                            3 => "B&#46; Hu"
                            4 => "L&#46; Zhang"
                            5 => "W&#46; Zhang"
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                          "autores" => array:5 [
                            0 => "N&#46; Petrosillo"
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                            2 => "O&#46; Ergonul"
                            3 => "G&#46; Ippolito"
                            4 => "E&#46; Petersen"
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                      "titulo" => "The incubation period of coronavirus disease 2019 &#40;COVID-19&#41; from publicly reported confirmed cases&#58; Estimation and application"
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