key: cord-1019653-mmcoqtb5 authors: Seirafianpour, Farnoosh; Sodagar, Sogand; Mohammad, Arash Pour; Panahi, Parsa; Mozafarpoor, Samaneh; Almasi, Simin; Goodarzi, Azadeh title: Cutaneous manifestations and considerations in COVID‐19 pandemic: A systematic review date: 2020-07-08 journal: Dermatol Ther DOI: 10.1111/dth.13986 sha: 6322198e7146d8ec21d4f13a53487892959c2e33 doc_id: 1019653 cord_uid: mmcoqtb5 BACKGROUND: COVID‐19 had a great impact on medical approaches among dermatologist OBJECTIVE: This systematic review focuses on all skin problems related to COVID‐19, including primary and secondary COVID‐related cutaneous presentations and the experts recommendations about dermatological managements especially immunomodulators usage issues METHOD: Search was performed on PubMed, Scopus, Embase and ScienceDirect. Other additional resources were searched included Cochrane, WHO, Medscape and coronavirus dermatology resource of Nottingham university. The search completed on May/03/2020. 377 articles assigned to the inclusion and exclusion groups RESULT: Eighty‐nine articles entered the review. Primary mucocutaneous and appendageal presentations could be the initial or evolving signs of COVID‐19. It could be manifest most commonly as a maculopapular exanthamatous or morbiliform eruption, generalized urticaria or pseudo chilblains recognized as “COVID toes” (pernio‐like acral lesions or vasculopathic rashes). Conclusion: During pandemic, Non‐infected non‐at risk patients with immune‐medicated dermatologic disorders under treatment with immunosuppressive immunomodulators are not needed to alter their regimen or discontinue the therapies. At‐risk and infection‐suspected patients needed to dose reduction, interval increase or temporary drug discontinuation (at least 2 weeks). Patients with an active COVID‐19 infection should hold the biologic or non‐biologic immunosuppressives until the complete recovery occur (at least 4 weeks). This article is protected by copyright. All rights reserved. Totally there were 453 articles with 76 duplicate data that were deleted. 377 articles were screening by the authors. From 377 articles, 240 article were met exclusion criteria in the first step. And, 39 article met exclusion criteria in the second step. 89 articles were met inclusion criteria. 27 articles were about cutaneous manifestation of covid-19; from them, 19 articles were case-reports and 8 articles were case-series. You can see the details in Figure 1 (in the supplement file). In Table 1 and 2, we summarized case reports and case series of primary cutaneous COVID-19-related reactions, respectively. In Table 3 , you can see cutaneous drug reactions related to COVID-19 treatment, till to our systematic search. Since there are wide categories of proposed drugs for treatment of COVID-19, In Table 8 (in the supplement file) the most prevalent and important cutaneous adverse reactions of these drugs is visible according to Tursen, u et al. review had done on all COVID-19 drugs skin reaction (8) . Totally 5 article were about skin drug reactions of COVID-19 treatments; two of them were original studies as case reports that were summarized in Table 7 (in the supplement file). Also, in Sharma, Ajay N et al. and Jakhar, D et al. Studies, adverse effect of hydroxychloroquine were reviewed (2, 9) . 11 articles were about skin injuries among medical staff fightingCOVID-19 & general population and usable recommendation about skin care in this global crisis that summarized in Table 3 . And in Table 4 , prevalence of areas affected by secondary skin complications were recorded. Also, 46 articles were about concerns in management of immune-based dermatologic disorders and autoimmune rheumatologic disorder and collagen vascular disease, and immunomodulator treatments in this pandemic. 26 of them don't have certain usable recommendation and 20 of them had specific advice that reported in Table 5 .Table 6 (in the supplement file) shows our exact search strategy. Eczema Not reported *frequent use of emollients/ *use soap-free cleanser; synthetic detergents have a neutral or slightly acidic pH and have relatively high free fatty acid content/ *Use alcohol-based cleansers or other antibacterial hand rub/ *Use lukewarm water (45°C-50°C)/ *use paper towels drying of hands after washing instead electric air dryers/ *Apply an ointment-based emollient during work time after hand washing and after work, at home/ *Avoid a water-based moisturizer/ *Avoid coming into direct contact with chemicals that are used for surface disinfection/ *Use anti-inflammatory topical medication under the supervision of a specialist (59) Dermatologic patients postpone initiation of biologic treatments in icular period this part The lack of sufficient data concerning the interaction of SARS-CoV-2 and biologics is also an important factor that should be taken into consideration when examining the option of initiating therapy with the latter. Another logistic parameter that should not be underestimated is the need of frequent careful monitoring under such treatments that includes both regular laboratory examinations as well as routine dermatologic follow-up visits, which could constitute a problem under the emerging societal circulatory restrictions that are posed in order to control the pandemic Unnecessary biologic discontinuation would lead to a worsening of psoriasis and psoriatic arthritis in a high percentage of the cases. As a consequence, there may be higher disease n, destructive impact on quality of life, burde as well as increased health care costs due to the augmented number of consultations and recovery. Furthermore, the unavoidable subsequent return to biologic therapy could be cost associated with switching toward higher known lower efficacy of -drugs, due to the well biologics in the same patient after their interruption Coronavirus widespread quickly across the world and in the March 2020,WHO announced the pandemic condition (11) . There is necessity to paying more attention to skin and its appendix (hair, nail) and the mucosal manifestation of COVID 19 also being more aware of them and updates our knowledge according to the latest reports. These manifestations could be the presenting signs of COVID19 which may help for early disease diagnosis. In addition, we had many concerns about patient who are suffering from chronic dermatologic disorders which needed to have repeated follow ups or who are on immunomodulator agents specifically immunosuppressives that are needed to be controlled without any more risk to getting infected with COVID19 or getting involved with its consequences. This article is protected by copyright. All rights reserved. According to the study which has done among 88 positive patients with covid19, in Italy, 20.4 % of patient had skin manifestation that the most common manifestation was erythematous rash or patchy exanthematous red rash. Also, there was urticarial eruption that could be localized or widespread, and 1 case of chickenpox-like blisters. The most involved area was trunk and all of the lesions were pruritic. There was not no any relation between disease severity and skin manifestations (29) . In a study carried out in France between 103 patients, skin manifestations were seen in 5(4.9 %), which were red rashes or urticarial rashes, mostly in the face and upper trunk. And there was a case of HSV-1 in an intubated patient (33) . There were reports of COVID19 patients with mottling or livedo-reticularis (LR) that could be because of disseminated intravascular coagulation (DIC) (18) . Transient LR have been also seen in 2 COVID19 patients who weren't in bad general condition (18) . Petechial skin rash (Dengue-like) could be considered as a presenting sign of COVID19, like acute hemorrhagic edema of infancy (10) . Symmetrical pruritic papules on both heels which were confluent yellowish-erythematous in color appeared 13 days after symptoms onset of COVID19 in a 28-year-old previously healthy woman,that gradually became erythematous hardened pruritic plaques (10) . Acroischemic lesions (pseudo-chilblain or Pernio-like lesion) or "COVID toe" which are micro thrombotic presentations of COVID occur in both children and adolescents when they are in good health condition, and the main affected parts were the feet and hands. The color of lesions were red and purple or blue and they could become blistering or having a black crust (68) . In a study of 63 patients who complained about chilblain like lesions in Italy, the range of patient's age was 12-16 years old, and the most affected area was the feet (85.7 %), then the both hands plus feet in the second place (7%), and next the only hands (6%). Most This article is protected by copyright. All rights reserved. lesions were erythematous edematous, and in blistering form. Most of the cases were in good general conditions, some of the patients were sympotomatic as, gastrointestinal (11.1%) , respiratory (7.9%) or febrile (4.8%) before showing skin manifestations. It was not possible to perform confirmatory tests for SARS-CoV-2 in all patients, but in those who did (18 cases), 4 of them turned positive. A study stated the hypothesis of chilblain-like lesions could be occur because of delayed immune reaction to COVID-19 in genetically prone ones (32) . A similar study with these finding performed in Spain (14) . In a case series of 14patients, 11 children with average age of 14.4 years and 3 adult patients with average age of 29 years were reported, they did not have any systemic symptoms except cough and fever in 3 cases from 3 weeks before skin eruption onset. The morphology of rash was a red-purple maculopapular eruption on the feet, hand of both sides and in 2 children papular targetoid lesions appeared on the hands and the elbow after few days. The rash diminished without any treatment during 2-4 weeks. The tests of 4 of them showed a negative result for COVID19 (35) . Acral ischemic lesions, 2 healthy young females who complained of bilateral papules on the dorsum of their fingers in a red-purple color reported, a 35-year-old patient had another complaint about diffuse redness under the nail of her right thumb. They both confirmed for having SARS-CoV-2 (13) . Digit ischemia may happen due to transient increase in antiphospholipid antibodies in severe illnesses or in viral disorders (69) . Another assumption was that this digit ischemia could be related to immunological mechanism or prothrombotic activation states (14) . Pruritic lesions in severe COVID-19related respiratory failures revealed an inflammatory thrombogenic vasculopathy with trace amount of C5b_9 and C4d depositions (22) . Maculopapular lesions which were fixed erythematous blanching on the trunk and limbs presented 2 days after onset of COVID infection symptoms in a 57 years old woman with not any significant past medical history (12) . This article is protected by copyright. All rights reserved. In another case who was a 48 years old man with HTN, 3 days after onset of fever, the macules, papules and petechial lesions appeared in a symmetric pattern in buttocks, popliteal fossae, proximal anterior thighs, and the lower abdomen. The petechial lesions were similar to parvovirus B19 infection (70) . In a 6 years old boy after 14-16 days' work-up for fever and elevated liver enzymes, erythematous, nonpruritic maculopapular rashes appeared first in the trunk and neck and then gradually spread to the other areas. The lesions diminished with no specific therapies after 5 days (28) . A 32 years old healthy female, 6 days after symptomatic current corona virus infection presented with generalized progressive maculopapular and petechial lesions in a reddish base that by the time became scaly, more itchy and less erythematous (71) . In the most cases of maculopapular lesions palmoplantar region and the mucosa were spare. A 60-year old man with a history of flulike symptoms and positive COVID19 infection experienced sudden disseminated red macular lesions which turned into papules on bilateral flank, groin ,back and proximal lower extremities (17) . In a 71-year old Caucasian woman scattered maculopapular eruption (morbilliform) with cervical lymphadenopathy ,fever and cough was seen in addition to hemorrhagic macular exanthem on the legs (16) . Pruritic Papulovesicular lesions was seen in a 72 years old woman who had a history of flu-like symptoms 4 days before skin rash appearance and the rash was on sub-mammary folds, hips and trunk (16) . Petechial lesions have been seen in above case and another one in Thailand who misdiagnosed as dengue fever (70, 72) . Digitate papulosquamous lesions occurred in a hospitalized old man who infected with COVID 19. The initiate periumbilical scaly patches widespread rapidly toward flank and thigh and the other areas, some of them were only papular. The lesions resembled pityriasis rosea and diminished suddenly in 7 days (73) . A 34 months old child with conjunctivitis and eyelid dermatitis confirmed SARS-CoV-2 in China (15) . Acute urticaria and low-grade fever was noticed in 2 months girl lasted 4 days, and spread in few hours from face and upper extremities toward lowers limbs and trunk (28) . A 27 years old previously healthy women who complained of diffuse arthralgia, odynophagia and pruritic reddish plaque in the acral area and the face proceed by fever ,chills and chest pain (11) . urticaria have been seen in a female patient who just had dry cough in the past days and her CT scan confirmed the COVID19 infection (20) . Also in a 61 years old Spanish MD male patient, progressive pruritic urticarial lesions manifested which lasted about 10 days without no other symptoms (27). A 60-year old woman with a history of flu-like and gastrointestinal symptoms 9 days ago, presented to dermatology department with complaint of diffuse urticarial plaques on the trunk, head and limbs (17) . About Febrile rash it could be say that in a 39 years old male patient with 39 °C fever and rashes which appeared at the same time of the fever onset presented, the lesions morphology were red, annular, stable plaques in neck, chest, abdomen, upper limbs and palms without involvement of face and the mucosa. The rash were edematous and erythematous and non-pruritic. He had no medication use in recent days and weeks before initiation of rash (74) . Varicella-like exanthema was foun in a 8 years old girl who had only mild cough 6 days before papulovesicular skin rash starts which had a symmetrical and bilateral pattern on the trunk. The test of she and her family confirmed for SARSCoV-2.The lesions diminished after a week (75) . Morbilliform exanthema presented in a 58 years old man who complained about cough and pain in limbs, the physician prescribed Azithromycin and Benzonatate for him and after a few days, pruritic progressive erythematous macule appeared in upper and lower limbs, neck and shoulders and trunk which had morbilliform pattern and through the time, lesions expanded and confluent as patches more than 10 cm on the trunk (24). This article is protected by copyright. All rights reserved. A 20 years old healthy male who complained of 6-day lasting fever and rash presented to emergency department and admitted in ICU. He had spreading nonpruritic maculopapular morbilliform rash on her trunk and limbs, respecting face, mucosa and the eyes. His COVID19 confirmed in day 2 (21). Skin rash in infants of positive COVID-19 mother, none of infant had positive test result among those who have been tested (3 of 4), 2 of the infant had two different patterned rashes, one of them diffuse red maculopapules and the other had ulceration on the forehead. Their rash diminished without any treatment (20) . Erythematous rash appeared 4 days after fever and asthenia in a 64 years old woman used oral paracetamol, the erythematous rash extended to the both antecubital fossa, axillary area and the trunk. The rash disappeared in 5 days with no specific treatment while continuing paracetamol intake .The patient's COVID19 infection confirmed with positive RT-PCR (19) . Malar eruption, a 26 years old man, a known case of Crohn disease, who had a history of close contact to a COVID19 patient, developed sore throat, anosmia, ageusia, mild dry cough, malaise and chest congestion in the past 2-3 week , who presented with asymptomatic red and edematous malar eruption on his face with a low grade fever and mildly tender large cervical lymph node (25) . C. Galván Casas summarized prevalence of different skin lesions of COVID19 based on a study among 375 patients in Spain: maculopapular lesions 47%, urticarial eruption 19%, acral erythematous lesions with pustule or vesicle (chilblain like lesion) 19%, other vesicular lesions 9%, and livedo reticularis 6% (1). There were several drug regimens used for treatment of COVID-19 patients, some of which could result in cutaneous side effects like presence of a new dermatoses or flare/aggravation of a previous dermatologic disorder. Till to the last update of this systematic review, generalized pustular reaction and exacerbation of psoriasis due to Hydroxychloroquine were the reported cases of cutaneous adverse reaction of COVID-19 treatment (35, 36) (supplementary Table 7 ). The following is the most common adverse reactions found in the publications irrespective of this pandemic, yhat could be in mind for better dermatologic disease approaching (supplementary Table 8 ). Hydroxychloroquine; Despite the inconclusive result over the implication of Anti-Malarial drugs; it is used widely for treating COVID-19 patients. In a study by Sharma et al., A total of 21 unique dermatologic reactions were reported in 3578 patients had Hydroxychloroquine cutaneous adverse drug reactions. The most common was drug eruptions as in maculopapular, erythematous, and urticarial dermatosis. Hyperpigmentation came second followed by pruritis, SJS/TEN and AGEP(Acute generalized exanthematous pustulosis) (2) . Dermatologists should consider the COVID-19 cutaneous manifestations such as erythematous rash, petechia, urticaria as differential diagnosis while assessing the possible Hydroxychloroquine drug reactions (29) . Azithromycin; Azithromycin is another drug used in combination with Hydroxychloroquine in COVID-19 treatment regimens. Skin adverse events of it may include cutaneous severe skin reaction associated fever, generalized red or purple skin rashes, angioedema, blisters, skin peeling, burning sensation in eyes or painful skin (76) . Antiviral Drugs; Several Antiviral drugs are used for its treatment as well; including Oseltamivir which could result in SJS/TEN, angioedema and idiosyncratic cutaneous drug reactions. Ribavirin also may cause alopecia, acneiform eruptions, maculopapular and eczematous lesions, localized scleroderma, skin dryness and rash. Other anitiviral drugs such as antiretrovirals are also used in some patient including Lopinavir and Ritanavir. Their adverse effects my presented as maculopapular drug eruptions, exfoliative erythroderma, SJS/TEN, severe cutaneous drug reactions, injection site reactions (8, 77) . In overall, non-infected non-at risk patients with immune-medicated dermatologic disorders under usage of immunosuppressive immunomodulator drugs like biologic agents are not needed to be alter regimen or discontine the therapies during pandemic, even these drugs may control the deteriorating cytokine storms also prevented disease flare-ups which both were associated with poorer outcomes and more complications in COVID-19 course, although strict adherence to quarantine and personal-social preventive hygiene performances are highly recommended especially in these groups of patients. But in patients who are living in highly prevalent disease area, showing flu like or COVID-19 specific symptoms (anosmia or asthenia) or who are highly suspected to having had any positive exposures, based on the consult with their physician and considering all circumstances, it is better to have changing in their therapeutic regimens as dose reduction, dose interval increase or temporary discontinuation. Patients with an active COVID-19 infection should hold the biologic or non-biologic immunosuppressants until the complete recovery (at least 4 weeks). In patients who were symptomatic but were no definite cases, therapies should stop for at least 2 weeks. Most of skin diseases which were treated with systemic immunomodolators were usually associated with more severe COVID-19 morbidity. Dermatologic disorders which were associated with metabolic syndrome, older age or vital organ comorbidities in particular respiratory disorders like patients with psoriasis, hidradenitis suppurativa and atopic tendencies may have poorer prognosis if become infected. Patients with more severe skin disorders (e.g. severe psoriasis) were in higher risk for developing pneumonias by any cause that is of great importance in this pandemic. In overall these group of patients may benefit more from future SARS-Cov-2 vaccination. Since the chronic nature of this pandemic, specialists should decide based on recent evidence with regard to case-by case variations considering cost-benefit ratio and also disease psychological burden (48, 56, 65, 78, 79) . Biologic immunomodulators especially TNF-a inhibitors, janus kinase (JAK) inhibitors, anti-IL 6 (Tocilizumab) may capable to control cytokine storms and it was systemic consequences like ARDS and etc in COVID-19 course and some trials were conducted to evaluate their efficacy in disease management, so patients who are using these drugs do not be needed to disrupt (80) . 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The authors declare there is no conflict of interest in this study.Funding: This study had no funding.