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Case series

COVID-19 outcomes in pemphigus patients: a single-center study

COVID-19 outcomes in pemphigus patients: a single-center study

Tsvetana Ivanova Abadjieva1,2,&, Zhaneta Hristova Zhelyazkova1, Kossara Venelinova Drenovska3,4, Snejina Georgieva Vassileva4

 

1Department of Dermatology and Venereology, Medical Faculty, Medical University of Plovdiv, Plovdiv, Bulgaria, 2Department of Dermatology and Venereology, St George University Hospital, Plovdiv, Bulgaria, 3Department of Dermatology and Venereology, Medical Faculty, Medical University Sofia, Sofia, Bulgaria, 4Department of Dermatology and Venereology, Alexandrovska University Hospital, Plovdiv, Bulgaria

 

 

&Corresponding author
Tsvetana Ivanova Abadjieva, Department of Dermatology and Venereology, Medical Faculty, Medical University of Plovdiv, Bulgaria

 

 

Abstract

Pemphigus patients undergoing treatment are immunosuppressed and susceptible to infections. With the outbreak of the COVID-19 pandemic, physicians and patients became concerned about the impact of pemphigus treatment on coronavirus infection. The aim of the study was to assess the incidence and course of coronavirus infection in patients with pemphigus, the impact of pemphigus treatment on coronavirus infection, and the impact of COVID-19 infection and vaccination against SARS-CoV-2 on pemphigus. Methods: sixty-five patients with pemphigus were followed up in person. The information was collected from the patients' case histories and through questions. Patients were asked about maintenance treatment of pemphigus, presence of skin or mucous membrane lesions, whether they had contracted COVID-19, the course of COVID-19, change in pemphigus therapy during coronavirus disease, impact of COVID-19 on the course of pemphigus, complications of COVID-19, vaccination for COVID-19, and compliance with the measures against COVID-19. Results: the mean age of the pemphigus patients was 55.74 (±14.228) years (30-87). Fifty-six patients were treated with corticosteroids and immunosuppressants, two patients were treated with rituximab, and seven patients had stopped therapy of their own volition. Nineteen patients (29.2%) had experienced COVID-19 infection. The course of coronavirus infection was mild to moderate. All patients recovered completely without complications. Seven patients were vaccinated. Conclusion: treatment of patients with pemphigus using corticosteroids and adjuvant immunosuppressants during the COVID-19 pandemic does not seem to increase their susceptibility to SARS-CoV-2 or worsen the outcome of the infection. Based on our limited experience, rituximab therapy in pemphigus patients does not appear to increase the risk of COVID-19 infection. The vaccination level is low.

 

 

Introduction    Down

Pemphigus is a group of life-threatening bullous diseases mediated by autoantibodies directed against desmosomal adhesion proteins, desmoglein 1 and desmoglein 3, which are expressed in the skin and mucous membranes. The mean age of onset of the disease is between 45 and 65 years. Pemphigus vulgaris and pemphigus foliaceus are the main clinical variants of the disease [1]. Pemphigus vulgaris is the prevalent subtype in Bulgaria [2]. The disease is controlled by corticosteroids with or without immunosuppressants, and in recent years rituximab has been used as first-line therapy [3-5]. With the outbreak of the COVID-19 pandemic, concerns arose among physicians and patients about the impact of pemphigus treatment on coronavirus infection. A logical question was whether pemphigus patients were more susceptible to SARS-CoV-2 and whether the course of the infection was more severe. Objectives: this retrospective study aimed to assess the incidence and course of coronavirus infection in patients with pemphigus, the impact of pemphigus treatment on coronavirus infection and vice versa, and the impact of COVID-19 infection and SARS-CoV-2 vaccination on pemphigus.

 

 

Methods Up    Down

Study design and settings: this study was conducted during the COVID-19 pandemic, in the period from March 2021 to September 2022. Patients with pemphigus were recruited in order of hospital admission from the archives of the Department of Dermatology and Venereology, where the patients were diagnosed, treated, and followed up. The diagnosis of pemphigus was established based on clinical manifestations, histopathologic findings of intraepidermal acantholytic bulla, and direct immunofluorescence examination indicating intercellular deposition of immunoglobulin G with or without complement C3 in the epidermis/epithelium.

Study patients: sixty-five patients with pemphigus were interviewed face-to-face and examined at the Department of Dermatology and Venereology.

Data collection: the information was collected from the patients' case histories and through questioning. Patients were questioned about maintenance treatment of pemphigus, including corticosteroids and adjuvant immunosuppressants; presence of skin and/or mucous membrane lesions; clinical remission of pemphigus; whether they had contracted COVID-19 or not; the course of coronavirus infection: mild, moderate, or severe; change in pemphigus therapy during coronavirus disease: no change, treatment discontinuation, reduction of corticosteroid dose, or discontinuation of adjuvant immunosuppressant treatment; impact of COVID-19 on the course of pemphigus: exacerbation of pemphigus; complications of COVID-19; vaccination for COVID-19: before or after the onset of pemphigus; post-vaccine exacerbation of pemphigus; and compliance with the measures against COVID-19. Patients were assessed clinically by the dermatologists who participated in the study. A COVID-19 infection was confirmed and documented by PCR or a SARS-CoV-2 antigen test. The severity of the coronavirus infection was determined based on detailed history and patients' medical records.

Statistical analysis: continuous variables are given as means and standard deviations (±SD), and categorical variables as percentages. Statistical analyses were performed with data analysis software IBM SPSS Statistics for Windows v. 26.0.

Ethical considerations: data were collected in accordance with the ethical principles of the Declaration of Helsinki. The Ethics Committee at the Medical University approved the study.

 

 

Results Up    Down

General characteristics of study patients: the mean age of the 65 patients followed up in this study was 55.74 (±14.228) years. Forty-six (70.8%) of the patients were women, and 19 (29.2%) were men. Thirty-one (47.7%) of the pemphigus patients were hospitalized during the pandemic, and 20 (30,8%) were newly diagnosed.

Disease variants: the following variants of pemphigus were diagnosed: pemphigus vulgaris in 52 (80.0%), pemphigus foliaceus in 13 (20%) patients.

Treatment results: twenty-four patients (36.9%) were treated with corticosteroids, 32 patients (49.2%) were treated with corticosteroids and immunosuppressants, two patients (3.1%) were treated with rituximab and corticosteroids, and seven patients (10.8%) had discontinued therapy prior to follow-up.

COVID-19 in study patients: nineteen patients (29.2%) had experienced COVID-19 infection confirmed by PCR or SARS-CoV-2 antigen test. The mean age of the COVID-19 patients was 58.89 (±14.948) years. The gender distribution was: 13 (68.4%) women and six (31.6%) men. The course of coronavirus infection was mild in 12 patients and moderate in seven patients. One patient in remission without therapy had a post-COVID-19 exacerbation. In one patient, a manifestation of pemphigus appeared six months post-COVID-19 infection.

Vaccination among study patients: seven patients (10.8%) had vaccination against SARS-CoV-2 infection: three patients before, and four after the onset of pemphigus without exacerbation of pemphigus. Twenty-four patients (36.9%) refused vaccination, and 34 (52.3%) were undecided.

COVID-19 prevention: all patients reported compliance with the measures against COVID-19. The patients' data are summarized in Table 1.

 

 

Discussion Up    Down

All but two pemphigus patients followed up in this study were treated with corticosteroids with or without adjuvant immunosuppressants like azathioprine, and two were treated with rituximab. The initial corticosteroid dose depended on the severity of the disease and was gradually reduced until metastasis was achieved. The maintenance dose of corticosteroids in COVID-19 patients was 5 to 20 mg prednisolone or equivalent as recommended [6,7]. There was an exception in only one patient, who developed a coronavirus infection before pemphigus was controlled. The patient was transferred to a COVID-19 ward. The course of COVID-19 infection in this patient was mild. Adjuvant immunosuppressants were discontinued for all patients with coronavirus disease, but corticosteroid treatment was continued. Seven patients had stopped treatment for pemphigus of their own volition for a period of time from seven to 72 months. Of these, a 72-year-old female, who had discontinued treatment for 18 months, reported oral erosions and a few bullae on the skin one week post-COVID-19. The disease was controlled with corticosteroid therapy. The other six pemphigus patients without treatment had no recurrences. Patients with pemphigus have been found to be at higher risk of respiratory, cutaneous, multiorgan, and systemic infections [8]. In the current study, treatment with systemic corticosteroids and immunosuppressive agents was not associated with increased susceptibility to COVID-19. Three of the pemphigus patients had stopped therapy before contracting COVID-19, and 16 contracted COVID-19 while under treatment for pemphigus. There were no severe cases of coronavirus disease among pemphigus patients. All patients recovered completely from COVID-19 without complications. As there were no severe cases or deaths among COVID-19 patients in our study, we did not differentiate patients based on the specific SARS-CoV-2 variants.

A 37-year-old woman with arterial hypertension and a 40-year-old man without comorbidities, both with extremely severe pemphigus and unvaccinated, were treated with rituximab during the pandemic for the study period. The woman received rituximab for more than one year; the man for more than six months. They had no COVID-19. The results of the current study are consistent with other reports. In the dermatologic clinic at Alexandrovska Hospital, Sofia, Bulgaria, one case of suspected COVID-19 was observed [9]. Publications by authors from Italy and Iran suggested that treatment of pemphigus patients with corticosteroids and immunosuppressants do not increase the risk of contracting COVID-19 or of poor outcome [10-13]. A higher risk of COVID-19 and hospitalization was found with prednisolone doses greater than 10 mg per day [14,15]. Authors from Alcona, Italy, reported no cases with febrile syndrome, respiratory failure, or death due to COVID-19 in 72 pemphigus patients. Of these, 50 received corticosteroid monotherapy, 20 combined therapies with corticosteroids and steroid sparing agent, and two were treated with rituximab [16]. A large population-based cohort study of 3,081 patients with bullous pemphigoid and pemphigus in Israel established that maintenance therapy with systemic corticosteroids and adjuvant immunosuppressants during the pandemic was not associated with worse outcomes. The risk of COVID-19 associated mortality was higher in patients with bullous pemphigoid than in controls. The risk of COVID-19-associated hospitalization and COVID-19-associated mortality was similar in patients with pemphigus and their controls [17]. Chinese authors concluded that treatment with immunosuppressants, especially glucocorticosteroids in low to medium doses, does not increase the risk of COVID-19 in pemphigus patients [18]. In this study, we found no increased risk of COVID-19 in pemphigus patients receiving rituximab.

The effect of rituximab on the course of coronavirus infection is not well established. Published data on the treatment with rituximab and COVID-19 outcomes in pemphigus patients are controversial. An Israeli study on the efficacy of repeated courses of rituximab did not establish a higher rate of infections and mortality among pemphigus vulgaris patients [19]. Authors from Italy and Iran did not report COVID-19 infection among pemphigus patients who received rituximab prior to the pandemic [12,13,20]. Other authors from Italy and Turkey reported isolated cases of COVID-19 infection in patients initiated on rituximab before the pandemic [21,22]. A retrospective analysis of 132 patients with autoimmune bullous diseases (AIBD) in the USA found no difference between the rates of SARS-CoV-2 positivity in patients with AIBD treated with rituximab compared to those without rituximab. Higher mortality from SARS-CoV-2 was found in patients with AIBD than the general population [23]. A multicenter study included 244 patients with pemphigus in Turkey. The authors found no difference between rituximab-treated and rituximab-untreated pemphigus patients regarding the number of cases diagnosed with COVID-19 and hospitalized. They concluded that rituximab treatment requires no additional safety precautions compared to other immunosuppressants [24]. Iranian authors found no increased risk of a severe form of COVID-19 in pemphigus patients receiving rituximab [25]. Authors from Iran presented a 40-year-old woman with aggressive course of pemphigus after administration of rituximab and COVID-19 infection. Intravenous immunoglobulin (IVIG) treatment resulted in rapid control of pemphigus. The general condition of the patient improved within a week [26].

Of 19 patients with AIBD and documented SARS-CoV-2 infection in the USA, one 74-year-old man with pemphigus vulgaris receiving rituximab two months prior coronavirus infection, and one 82-year-old patient with bullous pemphigoid treated with rituximab for four months, died of COVID-19. The authors concluded that recent rituximab therapy may increase the fatal outcomes of COVID-19 [27]. A retrospective cohort study on 704 patients with AIBD (620 with pemphigus) in dermatology referral hospital in Tehran, Iran, established 21 patients with confirmed COVID-19, 14 of which received rituximab within the last 12 months. The relative risk of COVID-19 infection and hospitalization decreased with each month since the last dose of rituximab [14]. The same conclusion was reached in another Iranian study [15]. A French nationwide study established more than a 5-fold higher risk of COVID-19 infection in patients with AIBD receiving rituximab compared with those who did not. Treatment of AIBD patients with rituximab during the first wave of COVID-19 was associated with increased risk of morbidity and higher mortality. Patients with lethal form of COVID-19 were older than those with a benign form [28]. Interpretation of COVID-19 outcomes among elderly pemphigus patients is complicated by comorbidities. Regarding COVID-19 outcome in AIBD patients, it is suggested that patients with bullous pemphigoid may be at higher risk of death of COVID-19 compared with pemphigus patients [17].

Post-COVID-19 exacerbation of pemphigus occurred in one (5.3%) of the patients followed up in this study. In one patient, pemphigus appeared six months after COVID-19 infection. The level of vaccination for COVID-19 among the pemphigus patients in this study is low. The major reasons for vaccine refusal among pemphigus patients were fear of exacerbation of the bullous disease and safety concerns. The vaccinated pemphigus patients had no exacerbation of pemphigus. Pemphigus occurred in three patients one, two and five months after application of the first dose of COVID-19 vaccine Moderna, Janssen, and second dose of Pfizer-BioNTech, respectively. It should not be concluded that pemphigus was induced by SARS-CoV-2 infection or vaccination, but it may be considered. COVID-19 infection or vaccination against SARS-CoV-2 may cause exacerbation of pemphigus or trigger the autoimmune bullous disease. Eleven (2.8%) of 383 patients with pemphigus and pemphigoid who were recruited from the database of the International Pemphigus and Pemphigoid Foundation, reported confirmed infection with SARS-CoV-2, and 35.2% of the patients reported a moderate to severe exacerbation of their autoimmune bullous disease [29]. Other authors reported AIBD flare-ups in 19.3% of the patients following COVID-19 infection [15].Cases of pemphigus having developed three days to four months after COVID-19 infection were reported [30-32].

A cross-sectional study established COVID-19 vaccine acceptance in 90.5% of 707 patients with pemphigus and pemphigoid, and exacerbation of the bullous disease in 12.3% (79) of the patients [33]. A Turkish study found that 18 (10.3%) patients experienced a post vaccination pemphigus flare [24]. Cases of new-onset pemphigus following all types of SARS-CoV-2 vaccination were described. The period from vaccination to the manifestation of pemphigus varies from two days to two months [34-41]. Cases of pemphigus following vaccination are rare and the association between pemphigus and vaccines remains doubtful [42]. Further studies are needed to clarify if there is an actual connection between vaccinations against COVID-19 and AIBD. Since the benefits of COVID-19 vaccination outweigh its risks, COVID-19 vaccination is recommended to pemphigus patient [43]. A study found that vaccination against COVID-19 reduces the severity of symptoms and duration of long COVID-19 [44]. It is preferable to vaccinate patients in the remission phase of pemphigus to increase vaccine efficacy and reduce the risk of exacerbation of the disease after vaccination [15,45]. It was recommended for all pemphigus patients to have a full course of vaccination prior to receiving rituximab [46,47]. It was recommended that the vaccination course should be completed four or more weeks before or 12-20 weeks after the rituximab infusions [45]. The pemphigus patients followed up in this study reported to have strictly adhered to measures against COVID-19. Similar findings have been reported by other authors [13]. An advantage of this study is that it was conducted by personal observation of pemphigus patients and SARS-CoV-2 infection was documented.

Limitations: the study are the insufficient number of included cases, lack of a control group, and the fact that experience of only one center is presented.

 

 

Conclusion Up    Down

The results of this study, as well as data published in the literature, suggest that treatment of patients with pemphigus with corticosteroids and adjuvant immunosuppressants does not seem to increase their susceptibility to SARS-CoV-2 or worsen the outcomes of the infection. Based on our limited experience, rituximab therapy in pemphigus patients during COVID-19 pandemic does not appear to be associated with an increased risk of COVID-19 infection. Data about rituximab in pemphigus patients and the course of COVID-19 are limited and controversial, and more studies are needed. Vaccination level is low because of patients' safety concerns. Nevertheless, it should be considered that vaccination benefits far outweigh the risks.

What is known about this topic

  • Patients with pemphigus have been found to be at higher risk of respiratory, cutaneous, multiorgan, and systemic infections;
  • Steroid-sparing agents like azathioprine, mycophenolate mofetil should be discontinued for pemphigus patients with coronavirus disease, but corticosteroids should be continued;
  • Low-dose pandemic corticosteroids were recommended for pemphigus patients during the COVID-19.

What this study adds

  • Treatment with low and moderate doses of corticosteroids and adjuvant immunosuppressants patients does not increase susceptibility to COVID-19 in pemphigus patients;
  • Treatment with corticosteroids and adjuvant immunosuppressants does not worsen the outcomes of SARS-CoV-2 infection in pemphigus patients;
  • Based on our limited experience, rituximab therapy in pemphigus patients during COVID-19 pandemic does not appear to be associated with an increased risk of COVID-19 infection.

 

 

Competing interests Up    Down

The authors declare no competing interests.

 

 

Authors' contributions Up    Down

Conceptualization: Tsvetana Ivanova Abadjieva. Data collection: Zhaneta Hristova Zhelyazkova, Tsvetana Ivanova Abadjieva. Data curation, data analysis, investigation: Tsvetana Ivanova Abadjieva, Zhaneta Hristova Zhelyazkova. Methodology: Tsvetana Ivanova Abadjieva, Zhaneta Hristova Zhelyazkova, Kossara Venelinova Drenovska, Snejina Georgieva Vassileva, project administration, resources. Tsvetana Ivanova Abadjieva, Zhaneta Hristova Zhelyazkova: software, validation, visualization, writing original draft. Tsvetana Ivanova Abadjieva: review and editing manuscript. All authors have read and approved the final version of this manuscript.

 

 

Acknowledgments Up    Down

We thank the patients for their responsiveness.

 

 

Table Up    Down

Table 1: patients with pemphigus during COVID-19 pandemic: age, treatment, COVID-19, SARS-CoV-2 vaccination, at department of dermatology and venereology (2021-2022)

 

 

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COVID-19 outcomes in pemphigus patients: a single-center study

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