Chilblains is a common cutaneous finding during the COVID-19 pandemic: A retrospective nationwide study from France
Authors: Adèle de Masson, Jean-David Bouaziz, Luc Sulimovic, Charles Cassius, Marie Jachiet, Marius-Anton Ionescu, Michel Rybojad, Martine Bagot, Tu-Anh Duong, Dominique Denjean, Marie-Pierre Labarthe, Maud Bézier, Marie Risbourg, Geneviève Payan, Sabrina Alain, Frédéric Mathivon, Anny Cohen-Letessier, Delphine Kerob, Jean-Philippe Hellier, Christelle Comte, Fabielle Keller, Caroline Brue, Paul Lestang, Laurence Allanore, Eliane Pierkarski-Carp, Anne Amoric, Hervé Serpier, Philippe Pruvost, Fabien Guibal, Damien Giacchero, Elisa Funck-Brentano, Sandrine Sierra Fortuny, Isabelle Gallay, Agnès Zavarro, Caroline Bider-Valle, Sylvie Lagrange, Etty Grynberg, Florence Weill, Dominique Penso, Marie Gomel, Jean Schneider, Anne Larabelle, Philippe Bonhomme, Marie-Sophie Gautier, Jean Hatchuel, Imane Mourtada, Charlotte Fite, Catherine Oliveres-Ghouti, Elisabeth Domergue, Sabrina Fourcade-Roch, Sylvie Lecanu, Nathalie Sebban, Bruno Halioua, Anne Bellut, Fabienne Keller, Isabelle Baratte, Françoise Lejoyeux, Laurence Ollivaud, Georges Abirached, Marielle Burnouf, Beatrix Reynayd-Mendel, Jean-Noël Dauendorffer, Joëlle Sebaoun, Anne Larabelle, Hervé Garrat, Marie-Martine Pomper, Anne-Marie Heudes, Isabelle Beaulieu, Hugues Cartier, Amélie Arsouze, Dominique Lons-Danic, Michèle Pelletier, Geneviève Payan, Valérie Gallais, Valérie Piantade, Marlène Risbourg, Georges Reuter, Serge Dahan, Murielle Creusot, Abdallah Kolli, Isabelle Egasse-Broca, Jean-Luc Rigon, Pascale Sabban, Hélène Flacher, Benoît Jaillard, Pierre André, Dominique Debjoux, Elodie Poirier, Bénédicte Solyga, Marc Perrussel, Sabrina Makhloufi, Bertrand Margnier, Clotilde Huzar, Laetitia Vandame, Hortense Thelu, Anne-Claire Chollet, Frédérique Marchal, Michael Naouri, Marion Nadaud, Elodie Boissy, Abdelhamid Lameche, Charles Berdougo, Audrey Rolland, Marie-Laure Fléchet, Gabriel Colonna, Delphine Jouannet, Isabelle Berdah, Françoise Truchot, Isabelle Lavallée
Journal: Journal of the American Academy of Dermatology (2020)

To the Editor: Coronavirus disease 19 (COVID-19), a pneumonia associated with severe acute respiratory syndrome coronavirus 2 (SARS-Cov2), was first identified in Wuhan, China, in December 2019, and was characterized as a pandemic by the World Health Organization on March 11, 2020. Fever, dry cough, dyspnea, fatigue, anorexia, ageusia, and anosmia are common symptoms of COVID-19. Reported skin manifestations of COVID-19 include erythematous lesions, sometimes with dengue-like petechiae,1Joob B. Wiwanitkit V. COVID-19 can present with a rash and be mistaken for dengue.J Am Acad Dermatol. 2020; 82: e177Abstract Full Text Full Text PDF PubMed Scopus (337) Google Scholar and urticaria and chickenpox-like vesicles.2Recalcati S. Cutaneous manifestations in COVID-19: a first perspective.J Eur Acad Dermatol Venereol. 2020; ([e-pub ahead of print])https://doi.org/10.1111/jdv.16387Date accessed: May 20, 2020Crossref Scopus (928) Google Scholar We performed a retrospective observational nationwide study of skin lesions encountered during the COVID-19 pandemic in France from March 18 to April 9, 2020, in an outpatient setting of French private practices. Patients gave informed consent for the publication of their photographs. The study enrolled 277 patients, half were male, and the median age was 27 years (range, 2-98 years). The lesions were classified into 6 categories: urticarial in 26 (9%; Fig 1, A), vesicular in 41 (15%; Fig 1, B), acral in 142 (51%; Fig 1, C), morbilliform in 25 (9%; Fig 1, D and E), petechial in 7 (3%), livedo reticularis in 4 (1%), and other types in 41 (15%). Some patients presented with cutaneous signs fitting in multiple categories (detailed in Table I). Acral lesions were unexpectedly common (n = 142). Chilblain-like lesions were the most frequent of the acral lesions (106 of 142 [75%]; Fig 1, C; Supplemental Fig 1, available via Mendeley at https://doi.org/10.17632/2f9rpvh9vd.1). Vesicular acral (dyshidrosis-like) lesions were reported in 20 patients (14%). Acrodynia was present in 18 patients (6%), sometimes isolated.Table ICharacteristics of the patientsCharacteristic∗Some patients presented with cutaneous signs fitting in multiple categories.No. (%) or median (range)All patients277Male sex129/259 (50)Age, y27 (2-98)SARS-Cov2 PCR test34/277 (12) Positive PCR test25/34 (74)Contact with a patient with COVID-1931/277 (11)Suggestive extracutaneous symptoms†There were 19 patients who reported suggestive extracutaneous symptoms and contact with a patient with COVID-19.103/277 (37) Fever48/277 (17) Respiratory symptoms44/277 (16) Anosmia/ageusia18/277 (6) Digestive symptoms16/277 (6)Acrodynia18/277 (6)Morbilliform lesions25/277 (9) Male sex10/21 (48) Age, y29 (2-70) Location of lesionsTrunk or limbs25/25 (100)Face2/25 (8)Acral lesions142/277 (51) Male sex67/132 (51) Age, y27 (6-73) Type of lesionsChilblains106 (75)Dyshidrosis-like lesions20 (14)Other16 (11) Location of lesionsHands23/34 (68)Feet18/34 (53)Vesicular lesion41 (15) Male sex22/38 (58) Age, y43 (8-74) Type and location of lesionsVesicles/varicella-like lesions of the trunk and limbs21 (51)Acral dyshidrosis-like lesions20 (49)Livedo reticularis4 (1) Male sex1/2 (50) Age, y15Urticarial lesions26 (9) Male sex13/23 (57) Median age (range)3 (2-23) Location of lesionsTrunk and limbs24 (92)Face2 (8)Petechial lesions7 (3) Male sex5/7 (71) Age, y21 (5-70) Location of lesionsDiffuse3/7 (43)Acral2/7 (29)Limbs2/7 (29)Other types of lesions‡Including eczema-like, angiomatous, and annular lesions.41 (15) Male sex11/36 (31) Median age (range)40 (1-98) Location of lesions, n (%)Trunk and limbs33/41 (80)Face8/41 (20)PCR, Polymerase chain reaction; SARS-Cov2, severe acute respiratory syndrome coronavirus 2.∗ Some patients presented with cutaneous signs fitting in multiple categories.† There were 19 patients who reported suggestive extracutaneous symptoms and contact with a patient with COVID-19.‡ Including eczema-like, angiomatous, and annular lesions. Open table in a new tab PCR, Polymerase chain reaction; SARS-Cov2, severe acute respiratory syndrome coronavirus 2. Among the 277 patients, 34 had a SARS-Cov2 polymerase chain reaction (PCR) test, of which 25 (74%) were positive, and 7 of these 25 (28%) had acral lesions. Among the patients without a positive PCR test, 115 patients had suggestive extracutaneous symptoms (detailed in Table I) or reported a close contact with a patient with COVID-19, or both. In addition, 59 patients had isolated chilblains (without any past history of chilblains and in the absence of cold exposure), without associated extracutaneous symptoms; this may suggest cutaneous symptoms of COVID-19, because this finding has been documented in some patients with a positive SARS-Cov2 PCR test in our case series and in 2 recently published case reports.3Alramthan A. Aldaraji W. A case of COVID-19 presenting in clinical picture resembling chilblains disease. First report from the Middle East.Clin Exp Dermatol. 2020; ([e-pub ahead of print])https://doi.org/10.1111/ced.14243Date accessed: May 20, 2020Crossref PubMed Scopus (109) Google Scholar,4Kolivras A. Dehavay F. Delplace D. et al.Coronavirus (COVID-19) infection-induced chilblains: a case report with histopathological findings.JAAD Case Rep. 2020; ([e-pub ahead of print])https://doi.org/10.1016/j.jdcr.2020.04.011Date accessed: May 20, 2020Abstract Full Text Full Text PDF PubMed Scopus (210) Google Scholar Histologic examination of 3 chilblain-like lesions showed a lichenoid dermatitis with a perivascular and eccrine mononuclear infiltrate and vascular microthrombi in 2 cases. Owing to the retrospective, outpatient setting and the limited number of available SARS-Cov2 PCR tests in France to date, most patients were not tested. However, the number of observed chilblain-like lesions in patients without significant past medical history is extremely unusual during the spring season in France, especially because people are staying inside, and may suggest a link with COVID-19. Finally, the presence of microthrombi in patients with chilblains is consistent with the altered coagulation status observed in patients with severe COVID-19.5Tang N. Bai H. Chen X. Gong J. Li D. Sun Z. Anticoagulant treatment is associated with decreased mortality in severe coronavirus disease 2019 patients with coagulopathy.J Thromb Haemost. 2020; 18: 1094-1099Crossref PubMed Scopus (2443) Google Scholar Although the number of tested patients does not allow us to draw firm conclusions regarding a direct link between SARS-Cov2 and these skin lesions, the unexpected outbreak of acral skin lesions in this epidemic context requires further investigation. The authors thank all of the dermatologists of the French National Union of Dermatologists-Venereologists (SNDV), general practitioners, and pediatricians, who provided data and pictures, and the patients involved in this study.