INTRODUCTION

The COVID-19 pandemic, caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), heralded an unprecedented era in healthcare[1]. There was global concern amongst both the clinical and scientific communities about the immediate and longer-term health implications of COVID-19 in the general population. Risk factors for poor COVID-19 outcomes were uncovered early in the pandemic using population-level studies, including male sex, increased age and comorbidities such as cardiovascular disease and obesity[2]. There was thus heightened concern regarding poor outcomes for people with immune-mediated inflammatory disease (IMID) and specifically psoriasis, given the prevalence of multimorbidity in this group. Indeed, prior to the COVID-19 pandemic, cohort studies found a greater risk of respiratory infection related hospitalization amongst people with psoriasis compared to the general population [3–5]. Additionally, there was uncertainty regarding the risk of severe COVID–19 associated with immune-modifying therapies, especially given pre-pandemic data on serious (including respiratory) infection risk in the psoriasis population [6,7]. These knowledge gaps prompted rapid mobilisation of the research community, resulting in the development and dissemination of multiple, partially synergistic, international patient registries to investigate the impact of the pandemic[8]. In psoriasis, an international collaborative effort led to the launch of two aligned sister registries which were developed in partnership with people with psoriasis and patient organisations. These were a clinician facing registry PsoProtect (Psoriasis Patient Registry for Outcomes, Therapy and Epidemiology of COVID-19 Infection) and a patient-facing registry, PsoProtectMe (Psoriasis Patient Registry for Outcomes, Therapy and Epidemiology of COVID-19 Infection Me)[9,10]. PsoProtect launched globally on March 27, 2020. Its initial assessment of 374 clinician-reported patients from 25 countries was the first global case series of COVID-19 in people with psoriasis. It found that older age, male sex, and non-white ethnicity were associated with greater risk of hospitalization for COVID-19 in people with psoriasis, in addition to comorbid chronic lung disease [11]. Furthermore, in individuals with moderate-to-severe psoriasis, biologic use was associated with lower risk of COVID-19–related hospitalization compared to non-biologic systemic therapies. However, limitations to this dataset included a limited number of patients reported, the absence of a control group and potential clinician reporting bias. Differences in confounding factors across treatment groups such as risk mitigating behaviours (social isolation) and drug non-adherence could not be assessed[11]. Importantly, information on the lived experience and mental health burden of people with psoriasis during the pandemic remained unknown.

study design

To address some of these limitations, PsoProtectMe was rapidly launched early in the pandemic in May 2020 shortly after its sister registry PsoProtect. It was designed to collect information directly from people with psoriasis, including information on medication adherence, mental health, and social isolation behaviour. It was aligned to clinician reported COVID-19 registries (e.g. PsoProtect) and patient reported registries in other IMIDs (e.g SECURE-IBD registry for inflammatory bowel disease, SECURE-AD Patient Survey for atopic dermatitis and HS COVID for hidradenitis suppurativa). PsoProtectMe partnered with CORE-UK (a patient-facing self-report survey for those with rheumatic disease) so that data could be pooled across IMIDs, enabling increased statistical power for analyses. This was a valuable opportunity given the shared immune-modifying therapies across dermatology and rheumatology. The data fields in PsoProtectMe were defined following multi-stakeholder input from a study group of patient representatives, clinicians, epidemiologists and health data researchers. Key variables included demographics (age, sex, ethnicity, and country), details of psoriasis (phenotype, severity and treatment), COVID-19 (symptoms, treatment, and outcome), medication adherence, social isolation behaviour, comorbidities and smoking status. Validated screening tools were embedded including the Dermatology Life Quality Index (DLQI) assessing health related quality of life, the Generalized Anxiety Disorder Scale -2 (GAD-2) and the Patient Health Questionnaire Depression Scale -2 (PHQ-2). These embedded screening tools allowed for improved quality and interpretability of the self-reported data collected. eConsent for future healthcare record linkage was collected from UK participants, to enrich and validate self-report data. PsoProtectMe was freely accessible online and took around 10 minutes to complete. The eligibility criterion was any person (all ages) with a clinician-confirmed diagnosis of psoriasis, irrespective of COVID-19 status. Data were collected and managed using REDCap electronic data capture tools licensed to King’s College London Division of Health and Social Care Research[12,13].

ENGAGEMENT AND RECRUITMENT

Patient-facing registries advocate citizen science, the act of involving members of the public to act as collaborators in scientific research. Citizen science can encourage support and advocacy for people with chronic diseases and empowers communities to act to support their health and wellbeing [14]. Citizen participation in data generation is likely to be crucial in pandemic management [15], and the uncertainty and urgent need for data may have contributed to the psoriasis patient community being highly motivated to submit their own data, resulting in robust recruitment in PsoProtectMe. People with psoriasis were involved in all aspects of PsoProtectMe research, including deciding the research questions, design of data fields, beta-testing prior to launch, supporting dissemination and data interpretation. PsoProtectMe partnered with global patient organisations [16] and had patient representatives on the research steering committee. Following its launch, it was promoted and disseminated globally by an international cohort of patient organisations, including the International Federation of Psoriasis Associations (IFPA), and professional clinical networks to enable uptake [16]. It was available in nine languages (English, Italian, Japanese, Portuguese, Polish, Spanish, French, Chinese and Vietnamese) to improve international uptake. Research inclusivity was also promoted by sharing direct quotes via social media from a wide diversity of participants from over the world detailing why they contributed to PsoProtectMe. Rapid data feedback throughout helped to keep the psoriasis community engaged as they could see the results of their participation efforts. Results were regularly published on the ‘current data’ page of the PsoProtectMe website and shared through the social media channels of PsoProtect (including Instagram, Facebook and Twitter) and partner patient organisations. Continued engagement with participants was led by a communications working group who met regularly to review the dissemination strategy. This group included representatives from IFPA, Psoriasis Association and Global Psoriasis Atlas. This resulted in robust recruitment throughout the early months of the pandemic. Successful patient-facing registry recruitment was echoed elsewhere, and a review of the seven dermatology registries initiated during the COVID–19 pandemic found that patient-facing registries reported greater recruitment than clinician facing registries[17]. However, the relative increased recruitment in the PsoProtectMe study could also be explained by the recruitment being independent of COVID-19 status, which differed from PsoProtect’s inclusion criteria.

STUDY POPULATION

The PsoProtectMe registry was far-reaching, with 5479 participants from more than 30 countries worldwide. Countries with more than 200 participants included the UK, USA, Chile, Argentina and Portugal. The mean age of participants was 45 years (range 3-91 years) and 67% were female. The mean BMI of participants was 26.8kg/m². 4408 respondents reported plaque psoriasis, 1122 guttate psoriasis, 289 pustular psoriasis and 120 self-reported erythroderma. 2320 (36%) respondents stated that they were receiving a systemic therapy for psoriasis, and 32% reported concurrent psoriatic arthritis.

PsoProtectMe findings on the burden of the COVID-19 pandemic

Analysis of PsoProtectMe data facilitated an international cross-sectional assessment of the impact and burden of the pandemic in people with psoriasis, along with assessing changes in behaviour during the pandemic.

Association between worsening psoriasis and mental health

People with psoriasis have a high prevalence of anxiety and depression: a pre-pandemic single centre UK cross-sectional study of 607 people with psoriasis (81.6% of whom were receiving systemic therapy) revealed that 10% screened positive for major depressive disorder (MDD) and 13% for generalized anxiety disorder (GAD)[18]. The risk of MDD or GAD was significantly higher in those with severe psoriasis. During the pandemic, there was an increased multifactorial mental health burden in the general population [19] and in people with psoriasis[20]. Public health efforts to reduce infection risk, such as shielding behavior and stay at home measures, were hypothesized to cause indirect morbidity including worsening psoriasis and mental health. An analysis of PsoProtectMe data from 4043 individuals highlighted that worsening psoriasis was common during the pandemic, and reinforced the association with poor mental health. The association between mental health and self-reported worsening psoriasis was assessed using a multivariable logistic regression model. A score of ≥3 in GAD-2 (anxiety) or PHQ-2 (depression) screens was defined as a positive mental health screen[21]. A total of 1728 (42.7%) PsoProtectMe respondents reported worsening psoriasis. The multivariable logistic regression model for worsening psoriasis estimated an odds ratio (OR) 2.01 (95% confidence interval (CI), 1.72–2.34) for those with a positive screen for anxiety or depression compared to those without a positive screen. Similar associations were observed for female sex (OR 1.82, 95% CI 1.56–2.13); obesity (OR 1.22, 95% CI, 1.09–1.36) and shielding behaviour (OR 1.18, 95%CI 1.03–1.35) [22]. These results highlight the burden of the COVID-19 pandemic in people with psoriasis. Access to holistic care and psychological support for people with psoriasis is imperative to address the increased mental health burden and PsoProtectMe findings highlighted the urgent need to provide this during the COVID-19 pandemic.

Risk mitigating behaviour

As part of the international recommendations from the World Health Organization (WHO), public health risk-mitigating measures such as social distancing were rapidly undertaken as a global measure to reduce the community spread of COVID-19[23]. High risk groups were advised to undertake strict social distancing measures defined as ‘shielding’. Those with IMIDs who were receiving immune-modifying therapies were initially thought to be at higher risk of severe COVID-19 due to pre-COVID 19 observational studies of drug related risk of serious infection [6,7]. However as detailed above, initial research from the PsoProtect registry and others indicated that use of biologic therapy was associated with a lower risk of COVID-19–related hospitalization than non-biologic systemic therapy. A possible explanation of this finding is a difference in behaviour such as risk mitigating behaviour across treatment groups. To explore this, an analysis of 2869 participants from the PsoProtectMe registry and 851 from the parallel CORE–UK registry was undertaken. Stringent risk mitigating behaviour (shielding) during the pandemic was associated with use of biologic therapies compared with non-biologic systemic therapies [OR 1.39, 95% CI 1.23–1.5] or no treatment [OR 1.63, 95% CI 1.35–1.97]. This difference in behaviour between treatment groups may have contributed to the reported lower risk of adverse COVID-19 outcomes associated with use of biologic therapies compared with standard (non-biologic) systemic therapies. Shielding was also associated with established risk factors for severe COVID-19 (male sex, obesity, and comorbidity burden) and a positive anxiety or depression screen[16].

Vaccine hesitancy

Vaccination against COVID-19 is crucial in reducing severe COVID-19 outcomes and hospitalisations, however vaccine hesitancy (delayed acceptance or refusal of vaccination despite service availability) threatened vaccination rates and public health COVID-19 risk mitigation strategies [24]. A UK cross-sectional study of 5,114 adults in the general population assessed vaccine hesitancy in the months prior to the COVID-19 vaccine rollout, reporting that 29% of respondents were vaccine hesitant. Vaccine hesitancy was higher in women, younger people and ethnic minority groups [25]. Individuals with psoriasis, particularly those treated with immune-modifying therapies, were prioritised for vaccination. However, there were limited data on vaccine hesitancy amongst people with psoriasis [26]. Therefore, PsoProtectMe was updated 1 year following its launch to include questions on COVID-19 vaccine hesitancy. Analysis of self-report data from 802 PsoProtectMe participants (data extracted 9 August 2021) indicated that 8.3% (n=63) participants were vaccine hesitant [27], consistent with other published data[26]. These individuals were younger, more likely to be of non-white ethnicity and live outside the UK, compared to those who were not hesitant. They were also less likely to be taking immune-modifying therapy. The most common reasons for vaccine hesitancy were concerns regarding vaccine side-effects, the vaccine being new and psoriasis worsening post vaccination.

Medication non-adherence

Prior to the pandemic, an association between mental health conditions and medication non-adherence was found in people with psoriasis[28]. The negative impact of the pandemic on the mental health of people with psoriasis[20]lead to concerns regarding medication adherence in this group. The PsoProtectMe data resource was leveraged to explore this, including the extent of and reasons underlying non-adherence. 1611 (40.5%) of 3980 PsoProtectMe participants were prescribed a systemic immune-modifying therapy. Of this group, 25.3% reported non-adherence during the pandemic, most commonly due to concerns about their immunity. In an unadjusted logistic regression model, a positive anxiety screen was associated with non-adherence to systemic immune-modifying therapy, however this association was not present following adjustment for potential confounders, although the direction of effect remained [29]. In an earlier assessment, non-adherence was also shown to be associated with worsening psoriasis[22]. This information highlights the need for clinicians to identify which groups are non-adherent to their treatment and therefore at risk of worsening psoriasis and a greater disease burden. Current guidelines (informed by reassuring data on immune-modifying therapy-related risks of severe COVID-19) recommend continuing immunosuppression in people without COVID-19 to maintain disease control [30]. Given the level of reported non-adherence in PsoProtectMe participants and the association with worsening psoriasis, close communication with patients to encourage medication adherence is important.

Limitation of findings

There are several limitations to these findings which are important to consider when interpreting the data. PsoProtectMe respondents were dominated by females of white ethnicity residing in the UK, therefore limiting the generalisability of the results. Data collection via online surveys may limit engagement from individuals who are less technology-literate or not connected to the media. Furthermore, self-report assessments may underestimate the true extent of medication non-adherence, and there may be ascertainment bias since those more concerned about COVID-19 risk may be more likely to participate. Data collection was also limited to people with psoriasis, so direct comparisons with the general population cannot be performed.

Communication of PsoProtectMe findings to the psoriasis community

The dissemination of the findings from the PsoProtectMe project was global and consistent. Multiple avenues of information transmission were utilised, including via partner organisations, social media and publications. Information was delivered in a variation of formats including infographics, lay summaries, newsletters and presentations. The content and presentation of the findings were optimised by PsoProtect’s partner organisations. Results were presented at the IFPA World Conference 2021, Psoriasis Association Conferences 2021 & 2022, International Psoriasis Council events, Skin Inflammation and Psoriasis International Network (SPIN) congress 2022 and at Patient and Public Involvement (PPI) webinars (delivered by St John’s DermAcademy in 2020 and 2021). The PsoProtectMe (and PsoProtect) website provided open access to ‘current data’ detailing the total number of participants and summary data in simple infographics. The websites also linked to lay summaries of the associated publications.

A summary of the findings

PsoProtectMe allowed for an international cross-sectional assessment of the impact of the COVID-19 pandemic in people with psoriasis. It found that worsening psoriasis was common in the pandemic and associated with a positive mental health screen, shielding behaviour, obesity and female sex. The results highlighted that stringent risk-mitigating behaviour, or shielding, during the pandemic was associated with the use of targeted biologic therapies compared with standard non-biologic systemic therapies or no treatment. Shielding was also associated with established risk factors for severe COVID-19 (male sex, obesity, and comorbidity burden) and a positive anxiety or depression screen. A quarter of patients on systemic immune-modifying therapy reported medication non-adherence, citing concerns about their immunity as the main reason for stopping treatment. Finally, PsoProtectMe data indicated low vaccine hesitancy amongst people with psoriasis.

What’s next?

The use of patient-facing registries such as PsoProtectMe allow for a novel and exciting means to further understanding of inflammatory skin diseases. PsoProtectMe has catalysed the creation of a novel patient self-report platform that aims to understand inflammatory skin disease onset, progression and treatment outcomes over time and to facilitate tools to improve disease outcomes. Co-designed using multi-stakeholder input, it will collect information about current treatments, physical health, mental wellbeing and everyday behaviours such as diet and physical activity. It also aligns with the Biomarkers and Stratification To Optimise outcomes in Psoriasis (BSTOP) UK observational study and population studies including Our Future Health[31]. Following participant eConsent, self-report data will be linked to healthcare records and existing research, thus enriching the data.

Conclusion

PsoProtectMe (and PsoProtect) provided valuable insight into the health impacts, behaviour changes and experiences of people with psoriasis during the COVID-19 pandemic, a unique period of unknowns and uncertainty. The findings informed clinical guidelines in psoriasis, including the National Psoriasis Foundation COVID-19 guidance and International Psoriasis Council COVID-19 statement [30,32]. It underscored the huge potential offered by online data collection from an engaged and motivated global patient community, enabling an accelerated translation of research to patient benefit. The regular, wide dissemination of results supported by partner organizations sustained patient community engagement and recruitment. This adaptive, time/resource efficient means of data collection, analysis and dissemination may enable future research efforts to rapidly address unmet health needs.

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Posted on 30 June 202322 November 2024