Perception of the threat, mental health burden, and healthcare-seeking behavior change among psoriasis patients during the COVID-19 pandemic.

This study aimed to investigate the perceived threat, mental health outcomes, behavior changes, and associated predictors among psoriasis patients during the COVID-19 pandemic. The COVID-19 has been known to increase the health risks of patients with psoriasis owing to patients' immune dysregulation, comorbidities, and immunosuppressive drug use. A total of 423 psoriasis patients not infected with COVID-19 was recruited from the Department of Dermatology, National Taiwan University Hospital Hsin-Chu Branch, Chang Gung Memorial Hospital, and China Medical University Hospital from May 2020 to July 2020. A self-administered questionnaire was used to evaluate the perceived threat, mental health, and psychological impact on psoriasis patients using the Perceived COVID-19-Related Risk Scale score for Psoriasis (PCRSP), depression, anxiety, insomnia, and stress-associated symptoms (DAISS) scales, and Impact of Event Scale-Revised (IES-R), respectively. Over 94% of 423 patients with psoriasis perceived threat to be ≥ 1 due to COVID-19; 18% of the patients experienced psychological symptoms more frequently ≥ 1, and 22% perceived psychological impact during the pandemic to be ≥ 1. Multivariable linear regression showed that the higher psoriasis severity and comorbidities were significantly associated with higher PCRSP, DAISS, and IES-R scores. The requirement for a prolonged prescription and canceling or deferring clinic visits for psoriasis treatment among patients are the two most common healthcare-seeking behavior changes during the COVID-19 pandemic. Psoriasis patients who perceived a higher COVID-19 threat were more likely to require a prolonged prescription and have their clinic visits canceled or deferred. Surveillance of the psychological consequences in psoriasis patients due to COVID-19 must be implemented to avoid psychological consequences and inappropriate treatment delays or withdrawal.

Introduction

In December 2019, a novel outgoing coronavirus (COVID-19) emerged from Wuhan, Hubei Province, which caused unexplained pneumonia, rapidly spread to over 150 countries globally and became a global public health threat. On September 5, 2021, World Health Organization declared that the pandemic led to 218,946,836 confirmed cases and 4,539,723 deaths worldwide, with a case mortality rate of approximately 2% to 5% [1, 2].

In dermatology, treatment of inflammatory and autoimmune skin diseases commonly involves immunosuppressant use, which may alter the competence of the host immune-surveillance system to combat the virus and has the potential to increase susceptibility, persistence, and reactivation of viral infections [3-6]. It was estimated that 17% of patients with moderate to severe psoriasis required treatments with systemic immunomodulators (such as methotrexate and cyclosporine) or biologics agents (such as tumor necrosis factor (TNF)-α, and interleukin (IL)-17 inhibitors) [7]. Accumulating evidence shows that TNF-α and IL-17 play crucial roles in antiviral immune responses associated with COVID-19 [8, 9]. Patients with psoriasis face a higher risk of serious infections that can lead to hospitalization and increase significant morbidity and/or mortality [10]. The infections can also cause exacerbation of psoriasis [11]. Psoriasis is a T-cell-mediated and chronic disease, associated with risks of comorbidities [12]. An existing study also indicated that people with underlying chronic morbidities were at a greater risk of developing severe symptoms and having poorer clinical outcomes when contracting COVID-19 [13]. These underlying factors render patients with psoriasis vulnerable to the impact of COVID-19 [14, 15].

The uncertainty and consequences associated with morbidity inherent with pandemic outbreaks could induce profound psychosocial impacts on non-infected people, including general populations and patients with chronic health conditions, in addition to the physical illness directly caused by the infection [16-19]. Thus, COVID-19 poses several new concerns and challenges for healthcare professionals when caring for patients with pre-existing immune disorders [20, 21]. During the height COVID-19 pandemic, many psychiatric services were closed, and the lockdown further aggravated patients’ vulnerability to mental disorders [22]. A recent study observed that the COVID-19 pandemic had a moderate or worse psychological impact on 20% of patients with rheumatoid arthritis, systemic lupus erythematosus as well as those immunosuppressed and those taking immunosuppressant drugs [23]. A thorough search of academic databases reveals no existing study on the impact of COVID-19 pandemics on psoriasis patients who are free from COVID-19 infections. The present study aims to investigate the perception of the threat, mental health burden, and healthcare-seeking behavior changes among psoriasis patients not infected with the COVID-19 pandemic.

Methods

This study used a self-administered questionnaire to assess the impact and behavior changes of psoriasis patients during the COVID-19 pandemic. Psoriasis patients not infected with COVID-19 were recruited consecutively from the Department of Dermatology, National Taiwan University Hospital Hsin-Chu branch, Chang Gung Memorial Hospital, and China Medical University Hospital from May 2020 to July 2020. The anamnesis data provide information about the absence of COVID-19 infection in participants. The structured questionnaires are designed to collect patients’ demographic data, the perceived threat of COVID-19, the impact of the COVID-19 pandemic on mental health, sleep quality, and behavior changes. The study protocol was reviewed and approved by the institutional review board of National Taiwan University Hospital, Hsin-Chu branch (109-030-E), Chang Gung Medical Foundation, Taiwan (202000851B0), and China Medical University Hospital (CMUH109-REC3-066).

Patients’ perceptions of the COVID-19 threat were measured using 13 items (S1 Table) based on a five-point Likert rating scale ranging from 1 (not worried at all) to 5 (very worried). The responses on these items were summed to produce the Perceived COVID-19-Related Risk Scale score for Psoriasis (PCRSP), which ranged from 13 to 85. In addition, participants were asked to choose the top three items of their most concern. Regarding mental health, patients were asked whether they experienced more depression, anxiety, insomnia, and stress-associated symptoms (DAISS) after the COVID-19 than before the outbreak on a five-point scale (from “1 = strongly disagree” to “5 = strongly agree”) (S1 Table). Moreover, the psychological impact of COVID-19 was measured using the 22-item Impact of Event Scale-Revised (IES-R; range, 0–88), which was well-validated in the Chinese population to determine the extent of psychological distress after exposure to a public health crisis, such as COVID-19 [24, 25]. The changes in healthcare-seeking behavior and therapy adherence during the COVID-19 pandemic were assessed using seven questions. In S1 Table, these questions inquired whether patients had adopted the prespecified behaviors more frequently at the time of the survey using a five-point Likert rating scale ranging from 1 (strongly disagreed) to 5 (strongly agree) as compared with behaviors adopted in the pre-COVID-19 period. Items in these questionnaires except the IES-R were chosen and modified based on the following: a review of the published literature investigating the impact of COVID-19 [26], Severe Acute Respiratory Syndrome (SARS) [16], Middle East Respiratory Syndrome [27], avian influenza pandemics [28], and consultation with patients and clinical experts. Information about COVID-19-associated quarantined/isolation and psoriasis disease was collected using a questionnaire and/or chart review.

Statistical analysis

The content validity of PCRSP and DAISS was assessed by seven experts who rated the relevance of each question/item in the questionnaire on a scale of 1 to 4, and the results were presented as the Item Content Validity Index (I-CVI), as the average I-CVIs for all the items in the questionnaire (S-CVI/Ave), and total agreement [29, 30]. Internal consistency and the test-retest reliability of the PCRSP and DAISS were evaluated using Cronbach’s coefficient alpha (α > 0.70 is considered to be a good internal consistency) [31]. The intraclass correlation coefficients (ICC) are widely used for the reliability index. ICC ≥ 0.6 is considered good reliability [32]. We also evaluated the correlations between these scales using Spearman’s correlation coefficients (strong: rho ≥ 0.5, moderate: 0.30 < rho < 0.49, weak: 0.10 < rho < 0.29) [33] to ensure convergent validity. Comparisons between two or more groups were conducted using the Mann–Whitney U test and the Kruskal–Wallis test for continuous variables and the chi-squared test or Fisher’s exact test for discrete variables. In subgroup analysis, patients were groups using the baseline psoriasis area and severity index (PASI) score, as follows: < 12, 12 ≤ PASI < 20, or PASI ≥ 20 [34]. Multivariable linear regression models were used to determine potential risk factors for PCRSP, DAISS, and IES-R. Independent variables included age, sex, body weight, the severity of psoriasis, family history of psoriasis, disease duration, comorbidities (including cardiovascular disease, diabetes, hyperlipidemia, and psychiatric disorder), psoriatic arthritis, friends or family member with quarantine experience, and treatment categories (biologics for cutaneous psoriasis, biologics for psoriatic arthritis, traditional antipsoriatic drugs or phototherapy and/or topical drugs only). The R software was used to estimate the target sample size. Since little preliminary data were used in this issue, we determined the sample size based on a previous study [35] that reported gender differences using the IES-R scale during the COVID-19 pandemic. We assumed that the mean (± SD) of the IES-R score for men was 8.56 (±11.86) and that of women was 14.11 (±14.09). For a male-to-female ratio of 3:1, a sample size of 420 patients is required to achieve a 95% power and 5% type 1 error. Statistical analysis except the sample size estimation was performed using the SPSS 21 statistical package (IBM Corporation, Armonk, NY, USA). A p-value < 0.05 (two-tailed) was considered to be statistically significant.

Results

Validation of PCRSP and DAISS

The scores for S-CVI/Ave for PCRSP and DAISS were 0.98 and 1.00, respectively. The total agreement was 92.3% and 100%, respectively, which suggested the validity of the questionnaire content [36]. The construct validity of these scales was supported by a strong correlation between DAISS and IES-R (rho = 0.664, p < 0.001) and a moderate correlation between PCRCP and DAISS (rho = 0.416, p < 0.001) as well as PCRCP and IES-R (rho = 0.435, p < 0.001). For reliability, the internal consistency of the PCRCP and DAISS scale, measured by Cronbach’s alpha coefficient, was 0.938 and 0.908, respectively. Both PCRCP (ICC = 0.907) and DAISS (ICC = 0.944) showed a good test-retest reliability.

Perception of COVID-19-related risk

Four hundred twenty-three psoriatic patients not infected with COVID-19 completed the survey. Table 1 shows the demographic and background characteristics of participants. Three hundred ninety-nine (94.3%) patients with psoriasis perceived at least one threat from COVID-19 (item score ≥ 3). The top three items that concerned patients the most were the risk of COVID-19 transmission to family members if they contracted COVID-19 (44.9% of patients), drug shortages for psoriasis therapy during the COVID-19 pandemic (32.2%), and fear of contracting COVID-19 in hospitals when attending the dermatology clinic for psoriasis (30.9%) (S2 Table). Female patients with psoriasis, who had a comorbidity, had a psoriatic arthritis (PsA), had a psoriasis duration >15 years, had a higher PASI score at baseline (PASI ≥20), and whose friends or a family member had quarantine experience reported higher average PCRSP scores (aPCRSP) compared, respectively, with male patients (p = 0.004), had no comorbidity (p = 0.001), no PsA (p = 0.003), a duration ≤15 (p = 0.010), lower PASI score (PASI ≥20 vs. PASI <12, p = 0.001; PASI ≥20 vs. 12 ≤ PASI < 20, p = 0.011), and without quarantine experience (p = 0.001). Moreover, patients who were treated with biologics reported higher average of aPCRSP score compared with those who were treated with phototherapy and/or topical drugs only (biologics for cutaneous psoriasis vs. phototherapy/topical, p = 0.005; biologics for PsA vs. phototherapy/topical, p = 0.002) (Fig 1).

Table 1

Participant demographic and disease characteristics.

Cohort characteristic	N (%)
Number of cases	423
Age (years), median (IQR)	45.0 (21)
Sex (male/female)	306 (72.3%)/117 (27.7%)
Bodyweight (kg), median (IQR)	76.0 (22)
Smoking (Yes/No/Quit) (%)	126 (29.7%)/228 (53.9%)/69 (16.3%)
Alcohol consumption (%)	78 (18.4%)
Family history of psoriasis, %	27.9%
Duration of psoriasis (years), median (IQR)	13 (16)
Hypertension	27.7%
Diabetes	13.7%
Hyperlipidemia	10.9%
Cerebrovascular accident	0.9%
Psoriatic arthritis (%)	44.0%
Severity of psoriasis at baseline	15.8 ± 8.8
PASI ≥ 20	78 (18.4%)
12 ≤ PASI < 20	95 (22.5%)
PASI < 12	250 (59.1%)
Treatment
Biologics for cutaneous psoriasis	45.1%
Biologics for psoriatic arthritis	19.4%
Methotrexate	25.8%
Cyclosporine	4%
Acitretin	7.1%
Phototherapy	15.1%
Topical drugs	69.3%

IQR, interquartile range; PASI, Psoriasis Area and Severity Index; IQR, interquartile range.

Fig 1

Perceived COVID-19-Related Risk Scale score for Psoriasis.

Perceived COVID-19-Related Risk Scale score for Psoriasis stratified by demographic and psoriasis disease characteristics. PASI, Psoriasis Area and Severity Index, PsA, psoriatic arthritis, PsO, cutaneous psoriasis. Bars for each estimate indicate the standard error of the mean. #Friends or a family member with or without quarantine experience. *P < 0.05; ** P < 0.01, ***P < 0.001. Comparisons between groups were performed using the Mann–Whitney U test except for the subgroups that were stratified by PASI and treatment modalities, assessed using the Kruskal–Wallis test.

Impact of COVID-19 on mental health and healthcare-seeking behavior

A considerable number of participants with psoriasis (17.7%) experienced at least one psychological symptom, more frequently (item score ≥ 4) during the COVID-19 pandemic, which included depression (13.5%), stress (9.7%), insomnia (5.9%), and anxiety (5.4%) than before the outbreak. For IES-R, a total of 263 (21.7%) reported a psychological impact (IES-R ≥ 24) [37] of COVID-19. Psoriasis patients with higher PASI score at baseline of (PASI ≥ 20) and comorbidities scored higher in DAISS and IES-R than those with less severe disease and no comorbidities, respectively (PASI ≥ 20 vs. PASI < 12, p = 0.012 for DAISS and p = 0.002 for IES-R; PASI ≥ 20 vs. 12 ≤ PASI < 20, p = 0.009 for DAISS and p = 0.011 for IES-R) (Fig 2).

Fig 2

Psychological impact of the COVID-19 pandemic.

Comparison of scores from the IES-R and a scale measuring DAISS between psoriasis patients who were stratified by psoriasis severity and comorbidity. PASI, Psoriasis Area, and Severity Index. *P < 0.05; ** P < 0.01, ***P < 0.001. Comparisons between groups stratified by PASI and comorbidity were performed using the Kruskal–Wallis test and the Mann–Whitney U test, respectively.

Thirty-one percent of survey patients prefer switching to a long-term drug prescription for psoriasis or drugs that can decrease clinic visits for a long term during the COVID-19 pandemic (S3 Table). Compared with patients who had a PCRSP < 3 and disease duration >15 years, those with aPCRSP ≥ 3 (p = 0.045) and disease duration ≤ 15 years (p = 0.005) were more likely to require a prolonged prescription. Thirteen percent of patients postponed, canceled, or reduced scheduled clinic visits for psoriasis treatment, particularly those whose friends or family members had a quarantine experience (p = 0.001) and those with aPCRSP ≥ 3 (p = 0.044) (Fig 3). Fewer than 5 percent of patients interrupted or discontinued with phototherapy, oral drugs, or biologics for psoriasis treatment and did not take medications for psoriasis according to their doctor’s instructions or postponed healthcare-seeking behavior for other non-COVID-19 diseases owing to risks associated with COVID-19.

Fig 3

Healthcare-seeking behavior changes.

Changes in healthcare-seeking behaviors in psoriasis patients during the COVID-19 pandemic among psoriasis patients stratified by perceived COVID-19-related risk (average PCRSP score, aPCRSP), duration of psoriasis, and friends or a family member with and without quarantine experience. * Quarantine_Y, Friends or a family member with quarantine experience, Quarantine_N, Friends or a family member without quarantine experience.

Factors influencing the impact of COVID-19 on psoriasis patients

Multivariable linear regression showed that more severe psoriasis measured by PASI, comorbidities, female sex, duration of psoriasis >15 years, and friends or a family member with quarantine experience was significantly associated with a higher aPCRSP. Similarly, a higher PASI, comorbidity, and female sex were significantly associated with DAISS. A higher PASI and comorbidities were associated with a higher IES-R score (Table 2).

Table 2

Results of multiple linear regression on factors associated with PCRSP, DAISS, and IES-R.

	PCRSP†			DAISS			IES-R
Variables	β	p-value	95% CI	β	p-value	95% CI	β	P-value	95% CI
Sex	0.129	0.008**	0.06–0.40	0.101	0.046*	0.01–1.57	0.008	0.868	-2.48–2.94
Severity of psoriasis†	0.142	0.005**	0.04–0.25	0.105	0.045*	0.01–0.93	0.150	0.004**	0.77–3.97
Disease duration§	0.100	0.039*	0.01–0.32	-0.009	0.867	-0.76–0.64	0.002	0.975	-2.41–2.49
Comorbidity	0.172	<0.001***	0.13–0.44	0.125	0.014*	0.18–1.61	0.232	< 0.001***	3.40–8.34
Psoriatic arthritis	0.076	0.123	-0.03–0.28	0.085	0.099	-0.11–1.31	0.035	0.485	-1.60–3.36
Friends or a family member had quarantine experience	0.117	0.016*	0.10–0.95	0.006	0.910	-1.82–2.04	0.053	0.284	-3.05–10.4

DAISS, depression, anxiety, insomnia and stress-associated symptoms, IES-R, Impact of Event Scale-Revised, PCRSP, Perceived COVID-19-Related Risk Scale score for Psoriasis.

*p < 0.05

**p < 0.01

***p < 0.001.

† Average PCRCP score; † Divided into Psoriasis Area and Severity Index (PASI) ≥20, 12 ≤ PASI < 20, and PASI <12 groups

§ Divided into duration >15 and ≤15 years groups.

Discussion

The COVID-19 pandemic has brought the risks of physical illness or death from viral infection and unbearable psychological pressure [26]. The outcomes of a survey that evaluated the severity of the COVID-19 outbreak in China showed that approximately one-third of the participants reported moderate-to-severe anxiety, while more than half rated the psychological impact as moderate-to-severe [26]. Psoriasis is a systemic inflammatory disease characterized by immune dysregulation, and it is independently linked to a risk of serious infection [38]. Patients with psoriasis are more likely to face risks of comorbidities (such as hypertension, diabetes, and cardiovascular disease) [39], associated with high COVID-19 fatality [13]. A significant body of research also indicates that type I interferon, TNF-α, B-cell released antibodies, and other cytokines play a significant role in the viral immune response that combats infection against viral pathogens and promotes clearance [40]. Considering the medication’s mechanism, psoriatic patients, taking TNF-α inhibitors, abatacept (CTLA-4 inhibitor), and ustekinumab (IL-12/23 inhibitor), known to modulate and blunt Th1 responses [39], are concerned about the possibility of increased susceptibility to COVID-19 infection. Therefore, facing this large-scale infectious outbreak, patients with psoriasis are theoretically vulnerable to the psychological impact caused by COVID-19. To support this notion, our results showed that 94.3% of patients with psoriasis perceived at least one threat caused by COVID-19, and 88.6% of patients with psoriasis perceived at least two threats caused by COVID-19.

Moreover, psoriasis severity and duration, PsA, and comorbidities are vulnerability factors associated with patients’ perception of the COVID-19 threat, as shown by PCRSP. Patients with more severe psoriasis and comorbidity also reported more psychological symptoms caused by COVID-19 as revealed by DAISS and IES-R scales. The reasons for these associations are not fully understood. However, a recent meta-analysis shows that chronic or severe physical illness is associated with an increased risk of mental disorders, which include anxiety disorder, depression, bipolar disorders, and schizophrenia [41]. Thus, it is reasonable to argue that the accumulated stress or burden associated with a serious underlying physical illness or comorbidities may intensify the perception of danger and increase an individual’s lifetime vulnerability to mental disorder. A recent study found that higher levels of depression and anxiety are found in patients with severe psoriasis [42, 43]. Moreover, there is a significant correlation between psoriasis severity, perceived stress, and mood alterations [44, 45]. Patients with PsA also face a high risk of mental disorders, such as depression, which appears to be greater than patients with cutaneous psoriasis only [46].

Similar to the psychological burden caused by SARS [47, 48], our regression analysis indicated that the female sex was an independent factor associated with a higher likelihood of reporting depression, anxiety, insomnia, and distress from the threat of COVID-19, as shown by PCRSP [49]. A growing body of evidence indicates that women are more vulnerable to most traumatic and disaster events and they face an increased risk of developing psychopathological consequences, such as psychiatric disorders [50-52].

Compared with the percentage of patients who perceived a COVID-19 threat and psychological impact, the percentage of change in healthcare-seeking behaviors among psoriasis patients was less prominent in the present study. This was probably because our government initiated a rapid and effective strategy to combat the COVID-19 outbreak, using real-time surveillance for case identification, border control, and quarantine. The government also allocated anti-pandemic resources [53, 54] to mitigate the COVID-19 impact, prevent the breakdown of the medical care system, and maintain easy and safe access to health care. Our results revealed that a greater perception of a COVID-19-related threat was significantly associated with changes in healthcare-seeking behaviors. A higher proportion of canceling or deferring clinic visits by psoriasis patients was recorded by those who had friends or a family member with quarantine experience because of the fear of exposure to COVID-19. Previous studies also found that higher perceived risk, threat, or danger was related to protective or preventive behavior changes during the COVID-19 outbreak [55, 56]. The inverse association between the disease duration and a prolonged prescription was probable because patients with a longer disease duration were more likely to believe the benefits of regular assessment and treatment for psoriasis outweighed the potential risks caused by COVID-19.

This study has some limitations. First, the Taiwanese population is the selected patient for clinical research, and it might be difficult to generalize the results to other ethnic groups in other regions. Second, information was collected quickly over a relatively few weeks because of the uncertainty associated with the disease under investigation. Thus, the possibility of selection bias may be possible.

In conclusion, we identified a major perception of threat and mental health burden among psoriasis patients during the COVID-19 outbreak. Over 94% of patients perceived at least one threat caused by COVID-19, and 18% of patients experienced ≥ 1 psychological symptom more frequently, and 22% of patients experienced psychological impact during the pandemic. Patients with more severe psoriasis, comorbidity, and female sex face a higher risk of perceiving a greater threat and are more likely to experience psychological symptoms caused by COVID-19. The requirements for a prolonged prescription and reducing clinic visits for psoriasis treatment were the two most common healthcare-seeking behavior changes during the pandemic, significantly associated with patients’ awareness of a threat due to COVID-19. Continuous surveillance of the psychological consequences caused by the COVID-19 pandemic in patients with psoriasis must be immediately implemented along with the provision of mental health support, particularly for vulnerable groups to mitigate the impact of the COVID-19 pandemic.

(XLS)

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Questionnaire.

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Perception of the COVID-19 threat among patients with psoriasis.

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Psychological impact and behavioral changes caused by the COVID-19 pandemic on patients with psoriasis.

(DOCX)

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3 Sep 2021

PONE-D-21-15316

The perception of the threat, mental health burden and healthcare- seeking behavior changes amidst COVID-19 pandemic among psoriasis patients

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Reviewer #5: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

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Reviewer #2: Yes

Reviewer #3: Yes

Reviewer #4: No

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**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The study was well conducted and rather relevant to current issues of the pandemic. However, it seems that psoriasis and COVID did not really impact patients' behavior in a different way from other diseases or even the lay public. Patients still continue their treatments prescribed.

Reviewer #2: The manuscript entitled 'The perception of the threat, mental health burden and healthcare-seeking behaviour changes admist COVID-19 pandemic among psoriatic patients' addressed the question of whether perceived threat, mental health outcomes, behavior chenges, and associated predictors among patients admist COVID-19 pandemic. To do so, the 423 patients suffering from psoriasis were asked by using questionnaires such as PCRSP, DAISS and IES-R, showing the increase in perceived threat in most of the patients and association of a higher psoriatic severity and comorbidity with a higher PCRSP, DAISS and IER-S.

Since most of the patients presented here were Taiwanese, it might be difficult to generalize the conclusions drawn by the authors over the different social conditions. However alternatively , I would think that this kind of work should be done in different regions and/or ethnics, which may contribute to our understanding on mental influence of COVID-19 pandemics depending on the different social conditions. Conclusively, this paper should appear medical practitioners such as medical doctors, nurses and co-medics. In this context, I think that this paper may stand on the general readership.

Reviewer #3: The work is interesting and well prepared, but some information/changes need to be considered.

Methods

It is necessary to state whether the project was approved by a research ethics committee and the approval number

Results

"Four hundred and twenty-three psoriatic patients not infected with COVID-19 completed the survey."

Establish whether the criteria for including patients as "psoriatic patients not infected" were based on anamnesis data or if patients were tested to exclude infection.

References

Some references are not placed within the journal's norms

Reviewer #4: In this study the authors assess the perceived threat, mental health outcomes, behavior changes, and associated predictors among psoriasis patients amidst COVID-19 pandemic. The authors show that higher psoriasis severity and comorbidity of psoriasis is associated with higher PCRSP, DAISS and IES-R. I think it is important to address the effects of COVID 19 pandemic on mental and physical status of those affected with chronic diseases. The current study merely describes that the pandemic had led to an adverse psychological impact correlated with disease severity. I do not see this study to be adding new information specifically for psoriasis affected population.

The manuscript needs major English editing.

Abstract:

Line 102-104 is vague. It would be better to rephrase.

Introduction:

Mere general information was introduced in this section. The authors fail to convey their message on why they find psoriasis different from many other conditions in regards to COVID-19 induce adverse psychological impact. There are many chronic diseases that the concept of this study could be applied for them, the authors need to clarify what they find different about psoriasis.

Methods:

Please provide information on power and sample size calculation

Results/Discussion:

The authors claim that regression showed being female was an independent factor for COVID19 related adverse psychological effect. Psoriasis has a higher female to male ratio and some subtypes have more severity in males, however the current study’s cohort was 72.3% male and 27.3% female. What measures have the authors taken to avoid selection bios?

Discussion needs major English editing

Data is not available in supplementary files. The authors merely provided a questionnaire.

Reviewer #5: Considerations in Introduction

Line 132: “The pandemic, as declared by the World Health Organization on 06 May 2021,…"

The date of declaration of the COVID-19 pandemic by the WHO needs correction.

Lines 139, 140, and 141: Psoriasis, a T-cell mediated disease, it was estimated that 17% of patients with moderate to severe psoriasis required systemic immunomodulators or biologic agents, which keeps rising recently [7-9].

The references provided by the authors do not support this statement.

Lines 143, 144, and 145 “Psoriasis is not only a chronic disease itself but also associated with many comorbidities. These underlying factors render patients with psoriasis vulnerable to impact caused by COVID-19.”

The reference is missing.

Consideration in discussion:

Lines 344, 345 and 346 “These findings are consistent with previous studies showing having a higher perceived risk, threat and danger were related to behavior changes during the outbreak of SARS [49,50]”.

Reference 49 does not converge with the results obtained with this study, thus requiring a correction in this statement.

**********

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Reviewer #3: No

Reviewer #4: No

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8 Oct 2021

Reviewer #1:

Comment#1: The study was well conducted and rather relevant to current issues of the pandemic. However, it seems that psoriasis and COVID did not really impact patients' behavior in a different way from other diseases or even the lay public. Patients still continue their treatments prescribed.

Response 1: Thank you for the comments. Distinct from patients with other diseases, such as diabetes and hypertension, the immunosuppressive drugs for psoriasis therapy, immune dysregulation, and comorbidities associated with psoriasis all render patients with psoriasis more vulnerable to the impact of COVID-19 than patients with other chronic diseases [1, 2]. As described in the manuscript, our survey found that the COVID-19 pandemic has created substantial challenges to the healthcare-seeking behavior among psoriasis patients. Although only less than 5% of patients discontinued their treatment for psoriasis, a substantial portion (13%) of patients postponed, canceled, or decreased the scheduled clinic visits for their psoriasis. Previous studies have suggested that a delay or disruption of continuity of regular medical care can lead to nonadherence to treatment and increase the morbidity and mortality risk [3-5]. Our study reminds physicians who provide care for psoriasis patients to be aware of the changes in healthcare-seeking behavior and medication prescription patterns, which might mitigate the probability of inappropriate treatment delays, non-adherence, or withdrawal resulting in subsequent worsening of psoriasis.

Reviewer #2:

Comment #1: The manuscript entitled 'The perception of the threat, mental health burden and healthcare-seeking behaviour changes admist COVID-19 pandemic among psoriatic patients' addressed the question of whether perceived threat, mental health outcomes, behavior chenges, and associated predictors among patients admist COVID-19 pandemic. To do so, the 423 patients suffering from psoriasis were asked by using questionnaires such as PCRSP, DAISS and IES-R, showing the increase in perceived threat in most of the patients and association of a higher psoriatic severity and comorbidity with a higher PCRSP, DAISS and IER-S. Since most of the patients presented here were Taiwanese, it might be difficult to generalize the conclusions drawn by the authors over the different social conditions. However alternatively, I would think that this kind of work should be done in different regions and/or ethnics, which may contribute to our understanding on mental influence of COVID-19 pandemics depending on the different social conditions. Conclusively, this paper should appear medical practitioners such as medical doctors, nurses and co-medics. In this context, I think that this paper may stand on the general readership.

Response 1: Thank you for the comments. Our study only included the Taiwanese population. It might be difficult to generalize the conclusions over different regions and/or ethnics. The applicability to a broader population requires further research. We have reported this limitation in the revised Discussion section.

Reviewer #3:

The work is interesting and well prepared, but some information/changes need to be considered.

Comment #1: Methods

It is necessary to state whether the project was approved by a research ethics committee and the approval number

Response 1: Thank you for the constructive comment. We have stated the IRB approval and approval number in the revised manuscript.

Comment #2: Results

"Four hundred and twenty-three psoriatic patients not infected with COVID-19 completed the survey."

Establish whether the criteria for including patients as "psoriatic patients not infected" were based on anamnesis data or if patients were tested to exclude infection.

Response 2: Thank you for the suggestions. In the revised manuscript, we indicated that the absence of COVID-19 infection in participants was based on anamnesis data.

Comment #3:References

Some references are not placed within the journal's norms

Response 3: Thank you for the comment. We have rechecked and reformatted the reference lists according to the journal’s requirements.

Reviewer #4:

Comment #1: In this study the authors assess the perceived threat, mental health outcomes, behavior changes, and associated predictors among psoriasis patients amidst COVID-19 pandemic. The authors show that higher psoriasis severity and comorbidity of psoriasis is associated with higher PCRSP, DAISS and IES-R. I think it is important to address the effects of COVID 19 pandemic on mental and physical status of those affected with chronic diseases. The current study merely describes that the pandemic had led to an adverse psychological impact correlated with disease severity. I do not see this study to be adding new information specifically for psoriasis affected population.

Response 1: Thank you for the comments. The psychological and behavioral impact of the COVID-19 crisis is highly heterogeneous among different regions and specific populations [6, 7]. Distinct from the general population, patients with psoriasis are generally considered to be a vulnerable population during the COVID-19 pandemic because of their immune system dysfunction, immunosuppressive medication use, and associated comorbidities [1, 2]. However, to date, there is little information about the psychological impact and behavioral changes caused by COVID-19, especially for the psoriasis-affected population. In the present study, we used a questionnaire that was specially designed for patients with psoriasis, which was based on the distinct features of this population, to assess the perceived threat, mental health outcomes, and behavior changes among patients with psoriasis during the COVID-19 pandemic. We validated the questionnaire. Our results described accurate estimates of the mental health burden, degree of concern about the pandemic, and changes in healthcare-seeking behavior. A considerable proportion of participants with psoriasis (17.7%) had experienced at least one psychological symptom, suggesting that mental health interventions are critically required for patients with psoriasis during the COVID-19 pandemic. These findings can be used to plan for mitigating measures by the health authorities. Our study also found factors that were associated with a high perceived threat and psychological symptoms among patients with psoriasis. These findings can help to identify and target high-risk psoriatic patients with a high mental health burden who may need specific psychological intervention or counseling support to prevent adverse mental health outcomes.

Studies have found the COVID-19 pandemic and global efforts to contain its spread (such as lockdown measures and transportation shutdowns) have led to limited access to healthcare, resulting in decreased service delivery and utilization for the general population [8, 9]. However, the absolute magnitude of the COVID-19 impact on healthcare-seeking behavior specifically in patients with psoriasis remains mostly unclear. The present study revealed that health care utilization for psoriasis treatment has changed in a large proportion of psoriasis patents (31%) during the COVID-19 pandemic. Understanding healthcare-seeking behavior changes in people with psoriasis might help clinicians better address their patients’ needs and inform policies and health authorities to protect this potentially vulnerable population.

Comment #2:The manuscript needs major English editing.

Response 2 Thank you for the comment. We have had our manuscript reviewed and edited by a native English-speaking editor (UNIVERSAL LINK CO., LTD.). The certificate of English editing has been provided.

Comment #3:Abstract:

Line 102-104 is vague. It would be better to rephrase.

Response 3: Thank you for the comment. We have rephrased the abstract as follows:

“The requirement for a prolonged prescription and canceling or deferring clinic visits for psoriasis are the two most common healthcare-seeking behavior changes among patients with psoriasis during the COVID-19 pandemic. Psoriasis patients who perceived a higher COVID-19 threat were more likely to require a prolonged prescription and have their clinic visits cancelled or deferred.”

Comment #4:

Introduction:

Mere general information was introduced in this section. The authors fail to convey their message on why they find psoriasis different from many other conditions in regards to COVID-19 induce adverse psychological impact. There are many chronic diseases that the concept of this study could be applied for them, the authors need to clarify what they find different about psoriasis.

Response 4: Thank you for the suggestions. We have amended and added several sentences to point out the specific features of psoriasis that are distinct from other chronic diseases. The changes are as follows:

“It was estimated that 17% of patients with moderate to severe psoriasis required systemic immunomodulators (such as methotrexate and cyclosporine) or biologic agents (such as tumor necrosis factor (TNF)-α and interleukin (IL)-17) inhibitors to treat their psoriasis, which is a T cell-mediated disease [7]. Accumulating evidence has shown that both TNF-α and IL-17 play crucial roles in antiviral immune responses that are associated with COVID-19 [8, 9]. Compared with those without psoriasis, patients with psoriasis had a higher risk of serious infection, leading to hospitalization and significant morbidity and/or mortality [10]. Infections can also cause exacerbation of psoriasis [11]. Moreover, psoriasis is a chronic disease, and it is also associated with many comorbidities [12].”

Comment #5:Methods:

Please provide information on power and sample size calculation

Response 5:

Thank you for the comments. We had added the description of power and a sample size calculation into the statistical analysis section of the revised manuscript, which is as follows:

“The target sample size was calculated using R software. Because there were few preliminary data on this issue, we determined the sample size based on a previous study [35] that reported gender differences using the IES-R scale during the COVID-19 pandemic. We assumed that the mean (±SD) IES-R score for men and women was 8.56 (±11.86) and 14.11 (±14.09), respectively. For a male-to-female ratio of 3:1, we needed a sample size of 420 patients for 95% power and 5% type 1 error.”

Comment #6: Results/Discussion:

The authors claim that regression showed being female was an independent factor for COVID19 related adverse psychological effect. Psoriasis has a higher female to male ratio and some subtypes have more severity in males, however the current study’s cohort was 72.3% male and 27.3% female. What measures have the authors taken to avoid selection bios?

Response 6: Thank you for the comments. Although a slightly higher prevalence of psoriasis was observed in female subjects than male subjects in Germany (0.76% vs. 0.66%), United States (2.5% vs. 1.9%) and Norway (1.6% vs. 1.2%) [11], a nationwide epidemiologic study using Taiwan National Health Insurance (NHI) claims database showed that psoriasis was more frequent in men than in women in Taiwan (61.6% vs. 38.4%) [12]. Thus, in our study, the higher prevalence of psoriasis in men is less likely due to selection bias and suggests that the sex ratio for the prevalence of psoriasis varies between different ethnic groups.

Comment #7: Discussion needs major English editing

Response 7 Thank you for your comment. We have had our manuscript reviewed and edited by a native English-speaking editor. The certificate of English editing is has been provided.

Comment #8 Data is not available in supplementary files. The authors merely provided a questionnaire.

Response 8: Thank you for the comments. We have provided additional data in the revised supplementary files.

Reviewer #5: Considerations in Introduction

Comment #1:Line 132: “The pandemic, as declared by the World Health Organization on 06 May 2021,…"

The date of declaration of the COVID-19 pandemic by the WHO needs correction.

Response 1: Thank you for the constructive comments. We have updated the COVID-19 pandemic statistics and its date of declaration by the WHO.

Comment #2: Lines 139, 140, and 141: Psoriasis, a T-cell mediated disease, it was estimated that 17% of patients with moderate to severe psoriasis required systemic immunomodulators or biologic agents, which keeps rising recently [7-9].

The references provided by the authors do not support this statement.

Response 2: Thank you for the suggestions. We have revised the reference. According to a questionnaire study that was published by Mrowietz et al. in the British Journal of Dermatology (Br J Dermatol. 2006 Oct;155(4):729-36), 17% of patients with moderate to severe psoriasis required systemic immunomodulators or biologic agents. We have added this reference into the revised manuscript.

Comment #3: Lines 143, 144, and 145 “Psoriasis is not only a chronic disease itself but also associated with many comorbidities. These underlying factors render patients with psoriasis vulnerable to impact caused by COVID-19.”

The reference is missing.

Response 3: Thank you for the suggestions. We have revised the manuscript and cited the relevant references.

Comment #4: Consideration in discussion:

Lines 344, 345 and 346 “These findings are consistent with previous studies showing having a higher perceived risk, threat and danger were related to behavior changes during the outbreak of SARS [49,50]”. Reference 49 does not converge with the results obtained with this study, thus requiring a correction in this statement.

Response 4: Thank you for the constructive comments. We have rephrased the sentences and cited new relevant references, which are as follows:

“Similarly, previous studies also found that a higher perceived risk, threat, or danger was related to protective or preventive behavior changes during the COVID-19 outbreak.”

References

1. Strippoli D, Barbagallo T, Prestinari F, Russo G, Fantini F. Biologic agents in psoriasis: our experience during coronavirus infection. Int J Dermatol. 2020;59(8):e266-e7. doi: 10.1111/ijd.15002. PMID: 32516447.

2. J. Liu. Association between Biologic Therapy and COVID-19 Infection Risk in Patients with Psoriasis. Presented at the: American Academy of Dermatology Virtual Meeting Experience 2021 (AAD VMX); Virtual.

3. CDC, National Center for Health Statistics. Excess deaths associated with COVID-19. Atlanta, GA: US Department of Health and Human Services, CDC, National Center for Health Statistics; 2020. https://www.cdc.gov/nchs/nvss/vsrr/covid19/excess_deaths.htm

4. Osendarp S, Akuoku JK, Black RE, Headey D, Ruel M, Scott N, et al. The COVID-19 crisis will exacerbate maternal and child undernutrition and child mortality in low- and middle-income countries. Nature Food. 2021; 2(7):476-84. doi: 10.1038/s43016-021-00319-4.

5. Wang JJ, Levi JR, Edwards HA. Changes in Care Provision During COVID-19 Impact Patient Well-Being. J Patient Exp. 2021;8:23743735211034068. doi: 10.1177/23743735211034068. PMID: 34350341.

6. Ellwardt L, Prag P. Heterogeneous mental health development during the COVID-19 pandemic in the United Kingdom. Sci Rep. 2021; 11(1):15958. doi: 10.1038/s41598-021-95490-w. PMID: 34354201.

7. Glintborg B, Jensen DV, Engel S, Terslev L, Pfeiffer Jensen M, Hendricks O, et al. Self-protection strategies and health behaviour in patients with inflammatory rheumatic diseases during the COVID-19 pandemic: results and predictors in more than 12 000 patients with inflammatory rheumatic diseases followed in the Danish DANBIO registry. RMD Open. 2021; 7(1). doi: 10.1136/rmdopen-2020-001505. PMID: 33402443.

8. Roy CM, Bollman EB, Carson LM, Northrop AJ, Jackson EF, Moresky RT. Assessing the indirect effects of COVID-19 on healthcare delivery, utilization and health outcomes: a scoping review. Eur J Public Health. 2021; 31(3):634-40. doi: 10.1093/eurpub/ckab047. PMID: 33755130.

9. Blumenthal D, Fowler EJ, Abrams M, Collins SR. Covid-19 - Implications for the Health Care System. N Engl J Med. 2020; 383(15):1483-8. doi: 10.1056/NEJMsb2021088. PMID: 32706956.

10. Jo SH, Koo BH, Seo WS, Yun SH, Kim HG. The psychological impact of the coronavirus disease pandemic on hospital workers in Daegu, South Korea. Compr Psychiatry. 2020;103:152213. doi: 10.1016/j.comppsych.2020.152213. PMID: 33096399.

11. Parisi R, Symmons DP, Griffiths CE, Ashcroft DM, Identification, Management of P, et al., Global epidemiology of psoriasis: a systematic review of incidence and prevalence. J Invest Dermatol. 2013;133(2):377-85. doi: 10.1038/jid.2012.339. PMID: 23014338.

12. Tsai TF, Wang TS, Hung ST, Tsai PI, Schenkel B, Zhang M, et al., Epidemiology and comorbidities of psoriasis patients in a national database in Taiwan. J Dermatol Sci. 2011;63(1):40-6. doi: 10.1016/j.jdermsci.2011.03.002. PMID: 21543188.

Submitted filename: Reply letter.docx

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14 Oct 2021

PONE-D-21-15316R1Perception of the threat, mental health burden, and healthcare- seeking behavior changes among psoriasis patients during the COVID-19 pandemicPLOS ONE

Dear Dr. Huang,

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Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

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Reviewer #1: All comments have been addressed

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Reviewer #1: (No Response)

Reviewer #2: Yes

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Reviewer #1: Although much better, English editing in several places is still necessary.

Just one example in lines 294-5 is provided here: Psoriasis patients with are more prone to develop comorbidities....

Reviewer #2: (No Response)

**********

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Reviewer #2: No

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26 Oct 2021

Journal Requirements

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Response 1:

Thank you for the instructions. We have reviewed our reference list, and no cited papers have been retracted.

Reviewers’ comments

Reviewer #1:

Comment#1: Although much better, English editing in several places is still necessary. Just one example in lines 294-5 is provided here: Psoriasis patients with are more prone to develop comorbidities.....

Response 1: Thank you for the comments. We have rephrased this sentence as follows: Patients suffering from psoriasis are more likely to face the risks of comorbidities, such as hypertension, diabetes, and cardiovascular disease. The manuscript has been carefully reviewed by an experienced editor whose first language is English and who specializes in editing papers written by scientists whose native language is not English. The English editing certificate is provided below.

Submitted filename: REBUTTAL LETTER.docx

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28 Oct 2021

Perception of the threat, mental health burden, and healthcare-seeking behavior change among psoriasis patients during the COVID-19 pandemic

PONE-D-21-15316R2

Dear Dr. Huang,

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Reviewers' comments:

1 Dec 2021

PONE-D-21-15316R2

Perception of the threat, mental health burden, and healthcare-seeking behavior change among psoriasis patients during the COVID-19 pandemic

Dear Dr. Huang:

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