The impact of the COVID-19 pandemic on pediatric rheumatology practice: an international, cross-sectional survey study

Abstract

Objective:

The COVID-19 pandemic has affected patient care in general. We aimed to analyze the impact of the pandemic on pediatric rheumatology practice.

Methods:

An online survey including 22 questions was created by the representatives of the Emerging RheumatoloGists and rEsearchers (EMERGE) group of the Pediatric Rheumatology European Society (PReS) on SurveyMonkey. The descriptive analysis of the responses was performed on SurveyMonkey.

Results:

Overall, 469 pediatric rheumatologists (F/M: 2.9) from 70 countries completed the survey. The practice of drug prescription is not affected by the pandemic, according to 65.3 % of the respondents, while 24.3 % and 16.5 % are prescribing biologic drugs and corticosteroids less often, respectively. Over 40 % of the respondents have seen an increased number of patients with vasculitis or chilblains during the pandemic. One-third of the respondents stated no adjustments in their clinical practice after 2.5 years of COVID-19 pandemic. The rest indicated implementing various changes, with an emphasis on incorporating telemedicine. Telemedicine constitutes ≥10 % of the clinical practice for one-third of the participants. Nonetheless, 35.5 % agree that there are still delays in patient care due to the pandemic. However, most (~90 %) think our practice is returning to the pre-pandemic routine.

Conclusion:

The findings of our study indicate a significant alteration in pediatric rheumatology practice due to the pandemic. This includes increased caution when prescribing anti-rheumatic drugs, a transition towards telemedicine utilization, delays in routine care, and a rise in COVID-19-related inflammatory conditions. It is imperative to address these aspects in order to improve patient care in pediatric rheumatology.

Introduction

The COVID-19 pandemic transformed our daily life and routine patient care. Although we are recovering from the severe restrictions introduced during the early stages of the pandemic, healthcare still encounters challenges. Since the onset of the pandemic, children with rheumatic diseases have comprised a distinct group requiring specialized attention. The primary concerns in pediatric rheumatology patients during the pandemic are the underlying immune dysregulation and anti-rheumatic medications that are often immunosuppressive. Pediatric rheumatologists have also contributed to the management of multisystem inflammatory syndrome in children (MIS-C), which is a hyperinflammatory complication of COVID-19 [1]. Additionally, the frequency of several inflammatory conditions, such as vasculitis and chilblains, increased during the pandemic [2–4]. All of these changes have affected routine clinical practice in pediatric rheumatology.

Pediatric rheumatology patients are generally children with chronic conditions requiring therefore regular and longitudinal care. The restrictions introduced by the pandemic, such as lockdowns and social distancing, and the fear of contracting COVID-19 have disrupted patient care and led to missed appointments [5,6]. The use of telemedicine tools has expanded to avoid irregularities in routine care [5]. However, this shift towards telemedicine use has brought some challenges, such as technical limitations and inequity of access [7].

Analyzing the pandemic-induced changes in the care of pediatric rheumatology patients is crucial for identifying areas that can be improved. We analyzed the impact of the pandemic on pediatric rheumatology practice at the beginning of the pandemic [8]. In the present study, we aimed to define the long-term impacts of the COVID-19 pandemic on pediatric rheumatology practice.

Methods

This study was a cross-sectional, global, online survey study. The survey was created by the representatives of the Emerging Rheumatolo-Gists and rEsearchers (EMERGE) group of Pediatric Rheumatology European Society (PReS) on SurveyMonkey. The survey was announced on the PReS website and in the EMERGE newsletter. It was also distributed via e-mail and Whatsapp to all members of EMERGE, PReS, the Childhood Arthritis and Rheumatology Research Alliance (CARRA), and Paediatric Society of the African League Against Rheumatism (PAFLAR). The survey remained accessible from January to April 2023. A respondent could fill out the survey only once.

There were 22 questions in the survey (Supplementary File 1). Q1-Q5 were questions regarding the respondents’ demographic features and pediatric rheumatology experience. Q6-Q8 were on drug prescription practices during pandemic, while Q9-Q11 inquired about the adjustments made when a pediatric rheumatology patient has COVID-19. Q12-Q15 addressed the changes and adjustments introduced in pediatric rheumatology practice as a result of the pandemic. Vaccination against COVID-19, MIS-C, and inflammatory conditions associated with COVID-19 were the addressed topics in Q16-Q17, Q18-Q21, and Q22, respectively.

This study was exempted from review by the institutional review board of Istanbul University, Istanbul School of Medicine. The respondents completed the survey voluntarily and anonymously.

Statistical analysis

The descriptive analysis of the responses was performed on Survey-Monkey. Categorical variables were presented with ratios and percentages. Categorical variables were compared by using the Chi-square test or Fisher’s exact test as appropriate.

Results

A total of 469 pediatric rheumatologists (F/M = 2.9) from 70 countries completed the survey. The highest number of respondents were from Turkey (n = 73; 15.6 %) and the USA (n = 68; 14.5 %), followed by Italy (n = 37; 7.9 %) and Brazil (n = 33; 7 %). The complete list of the countries with the number of respondents is presented in Supplementary Table 1. Most respondents are ≥35 years old (84 %), are practicing in a university hospital (73.9 %), and have ≥5 years of experience in pediatric rheumatology (71.4 %) (Table 1).

Table 1.

The demographic features of the 469 pediatric rheumatologists who responded to the COVID-19 Pediatric Rheumatology Survey.

Characteristics	Number of respondents, n (%)
Sex, female	346 (73.8)
Age  • < 35 years	• 75 (16)
• 35–44 years	• 189 (40.3)
• 45–65 years	• 184 (39.2)
• >65 years	• 21 (4.5)
Place of practice  • University hospital	• 347 (73.9)
• State hospital	• 78 (16.7)
• Private hospital	• 20 (4.2)
• Private practice	• 16 (3.4)
• University and private hospital	• 4 (0.9)
• Other	• 4 (0.9)
Years in pediatric rheumatology practice  • <5	• 134 (28.6)
• 5–9	• 95 (20.3)
• 10–19	• 129 (27.5)
• >20	• 111 (23.6)

Supplementary Table 2 summarizes the survey results. Of all respondents, 65.3 % has indicated that the pandemic does not affect their current practice of anti-rheumatic drug prescription (Fig. 1). Among the rest, 24.3 % and 16.5 % have mentioned prescribing biologic disease modifying anti-rheumatic drugs (DMARDs) and corticosteroids less often, respectively, in their current practice due to the pandemic. Regarding biologic and conventional synthetic DMARDs, 53.7 % and 39.5 % of the respondents indicated that during the pandemic they hesitated most in initiating rituximab and cyclophosphamide therapies respectively (Fig. 1). Rheumatic disease remains unaffected when pediatric rheumatology patients have COVID-19 according to 60 % of the respondents. In contrast, 33.4 % has mentioned that the rheumatic disease can be activated during or following SARS-CoV-2 infection. Around 60 % of the respondents modify anti-rheumatic treatment only when the patient has symptomatic SARS-CoV-2 infection, while one-fifth modify treatment in all patients with COVID-19. Around two-thirds skip the doses of biologic DMARDs during symptomatic SARS-CoV-2 infection. It is noteworthy that 16 % skip the doses of biologics even until the patient has a negative SARS-CoV-2 PCR test.

Fig. 1.

The strategy of prescribing anti-rheumatic drugs during the pandemic, according to the survey respondents. DMARD, disease-modifying anti-rheumatic drug; JAK, Janus kinase; NSAID, nonsteroidal anti-inflammatory drug; TNF, tumor necrosis factor.

Around one-third of the respondents mention that there are no adjustments in their clinical practice after 2.5 years of the pandemic. On the contrary, remaining respondents reported a decrease in the number of routine daily appointments (24.6 %), a shift towards using video consultations (34.6 %) smartphone communication apps (29.1 %), and e-mail consultations (13.1 %) to deliver care. One-fifth of the respondents do not use telemedicine tools at all; 45.2 % report that only <10 % of their clinical practice is based on telemedicine tools. A few respondents mentioned that the shift towards the use of telemedicine tools was especially prominent during lock-downs or surges of infections with different SARS-CoV-2 variants, and it has gradually decreased apart from these periods. They have also indicated that the telemedicine tools are now mainly used for non-C0VID-19 related reasons such as travel issues.

More than one-third of the participants (35.5 %) agree that there are still delays in the care of pediatric rheumatology patients due to the pandemic. The majority (~90 %) state that the clinical practice is returning to the pre-pandemic routine. More than two-thirds of the respondents think that vaccination policies have decreased the impact of COVID-19 on pediatric rheumatology practice (66.5 %) and that vaccines against COVID-19 will reduce the prevalence of MIS-C (72.9 %) (Fig. 2). Moreover, 86.6 % contribute to the care of MIS-C patients, and 72.1 % of these respondents mention that this has informed their perspective on managing macrophage activation syndrome (MAS) given overlapping features of these conditions. Regarding MIS-C, intravenous immunoglobulin (IVIG) combined with corticosteroids is the primary treatment reported by almost 60 % of the respondents who contribute to MIS-C care (Fig. 3). Notably, ~20 % combine IVIG and corticosteroid with anakinra or tocilizumab in the primary treatment of MIS-C.

Fig. 2.

Opinions of pediatric rheumatologists about vaccination against COVID-19. MIS-C, multisystem inflammatory syndrome in children; PIMS, pediatric inflammatory multisystem syndrome.

Fig. 3.

The primary treatment strategy in multisystem inflammatory syndrome in children (MIS-C) according to the survey respondents. ANA, anakinra; CS, corticosteroid; IVIG, intravenous immunoglobulin; MIS-C, multisystem inflammatory syndrome in children; PIMS, pediatric inflammatory multisystem syndrome; TOC, tocilizumab.

Around 60 % think that a history of MIS-C is not a contraindication for the COVID-19 vaccine. An increase in the number of patients with chilblains (42.1 %), non-MIS-C vasculitis (41.2 %), systemic autoimmune diseases (31.4 %), myositis (18.8 %), systemic autoinflammatory diseases (17.5 %), thrombosis (16.6 %), systemic juvenile idiopathic arthritis (13.3 %), and stroke (8 %) during the pandemic has been indicated by respondents (Fig. 4).

Fig. 4.

The percentages of pediatric rheumatologists who have seen an increased number of patients with several inflammatory conditions during the pandemic. sJIA, systemic juvenile idiopathic arthritis.

We compared the responses of the participants with an experience of <5 years (n = 134) with those who had a pediatric rheumatology experience of ≥5 years (n = 335). There was not a major difference between the two groups except that a shift towards video consultations was mentioned by a higher ratio of respondents with an experience of <5 years than the rest (30.5 % vs. 22.3 %, respectively; p = 0.04).

We have separated the respondents into two groups according to the income classification of the countries as low-to-middle income and high income countries (Supplementary Table 3). Then, we have compared the responses regarding demographics, drug prescription pattern, and adjustments and changes in clinical practice between the two groups (Supplementary Table 4). There were only slight differences regarding the demographics and experience in pediatric rheumatology. It is noteworthy that respondents with >5-year experience in pediatric rheumatology were more prevalent in the low-to-middle income country group (34.4 % vs. 23.5 %; p = 0.009). In response to the question querying the drugs that ware prescribed less often currently due to the pandemic, more respondents from high-income countries picked the option “none” than those from low-to-middle income countries (79.3 % vs. 49.5 %; p<0.001). More respondents from low-to-middle income countries mentioned a decrease in the number of daily appointments (33.9 % vs. 16.7 %) and a shift towards the smartphone communication applications (43.1 % vs. 17.1 %), while a shift towards video consultation was more frequently mentioned by the respondents from high income countries (47.4 % vs. 20.2 %) (p<0.001 for all). Notably, a higher number of respondents from low-to-middle income countries than those from high income countries has indicated that they do not use telemedicine at all in their current practice (24.8 % vs. 16.7 %; p = 0.03). More respondents agree that there are still delays in pediatric rheumatology care due to the pandemic in the low-to-middle income than high-income country groups (45.9 % vs. 26.7 %; p<0.001).

We have also compared our results with the results of our previous survey study analyzing the impact of the pandemic on pediatric rheumatology practice at the beginning of the pandemic [8] (Table 2). Interestingly, the trend of reduced prescribing of conventional synthetic and biologic DMARDs during the pandemic has slightly risen. The respondents hesitated most while initiating cyclophosphamide and rituximab in both studies (Table 2). These drugs were followed by tumor necrosis factor (TNF) inhibitors and Janus kinase (JAK) inhibitors in the previous [8] and current studies, respectively.

Table 2.

The comparison of findings in the present survey study with those of our previous survey study analyzing the impacts of pandemic on pediatric rheumatology practice.

n (%)	Previous survey study (n = 493) (ref. no: 8)	Current survey study (n = 469)
-Prescribing drugs less often due to pandemic
NSAIDs	67 (13.6 %)	55 (11.7 %)
csDMARDs	45 (9.1 %)	50 (10.6 %)
Biologic DMARDs	78 (15.8 %)	114 (24.3 %)
-Hesitating most in initi ating drugs during pandemic (top 4 of both surveys)
Cyclophosphamide	179 (36.3 %)	186 (39.5 %)
Rituximab	114 (23.1 %)	252 (53.7 %)
Janus kinase inhibitors	22 (4.5 %)	72 (15.3 %)
Mycophenolate mofetil	4 (0.8 %)	58 (12.3 %)
TNF inhibitors	25 (5.1 %)	45 (9.5 %)
-Shift towards telemedicine tools
Phone calls/applications	260 (52.7 %)	137 (29.1 %)
E-mail consultations	138 (28 %)	62 (13.1 %)
Video consultations	234 (47.5 %)	163 (34.6 %)

DMARD, disease modifying anti-rheumatic drug; NSAID, nonsteroidal anti-inflammatory drug; TNF, tumor necrosis factor.

Discussion

The present study highlights the changes and adjustments in pediatric rheumatology practice during the pandemic. Although some respondents think that there are no more delays in patient care and most agree that their practice is returning to its pre-pandemic routine, a considerable portion mentions that there are still challenges and modifications associated with the pandemic, such as hesitancy while prescribing some anti-rheumatic drugs, delays in diagnosis and management of patients, increase in several inflammatory conditions related to COVID-19, and a shift towards telemedicine use.

Most adult studies demonstrated a worse COVID-19 outcome in patients with rheumatic diseases compared to those without [9–14]. Many factors contribute to this difference, such as the type of rheumatic disease, disease activity, anti-rheumatic treatment, and other comorbidities. Since anti-rheumatic treatment often constitutes immunosuppressive drugs, a certain degree of hesitancy while prescribing these drugs is understandable during the COVID-19 pandemic, especially during the peak period. In a survey study analyzing the impact of the pandemic on rheumatology practice across Africa in the early pandemic period, ~14 % of rheumatologists indicated that they avoided initiating new biologic treatment with the fear of SARS-CoV-2 infection [15]. In our study, more than one-fifth of the respondents mentioned prescribing biologics less often due to the pandemic. In addition, 10–15 % of our respondents were reluctant to prescribe nonsteroidal anti-inflammatory drugs, corticosteroids, and conventional synthetic DMARDs (especially cyclophosphamide and mycophenolate mofetil). Notably, a higher percentage of respondents from high income than those from low-to-middle income countries has mentioned that they do not prescribe any anti-rheumatic drugs less often currently due to the pandemic, in our study. There might have been more problems regarding the access to several anti-rheumatic drugs such as biologics in the low-to-middle income countries during the pandemic compared to the high-income countries. When we compared our results with the results of our previous survey study performed at the peak of the pandemic [8] (Table 2), the most striking finding was the increase in the trend of a reduced prescription of DMARDs. This pattern may indicate that clinicians continue to harbor concerns regarding the potential for severe and complicated COVID-19 in their patients when utilizing anti-rheumatic drugs during the pandemic. Addressing these concerns is of utmost importance, as they have the potential to impede effective disease management. An increase in relapse rate was observed in children with rheumatic diseases, especially during the lockdown period of the pandemic [16,17]. This was primarily because of the changes in the anti-inflammatory treatment due to fear of SARS-CoV-2 infection [16, 17]. There are conflicting results regarding the effects of the anti-rheumatic treatment on the COVID-19 course. In a previous study analyzing COVID-19 course in pediatric rheumatology patients, use of biologic DMARDs was not associated with negative COVID-19 outcomes [18]. On the other hand, corticosteroid use was more frequent among the pediatric rheumatology patients hospitalized with COVID-19 [18]. It is important to note that the number of patients treated with rituximab or JAK inhibitors was very limited in this study. Similarly, another pediatric study did not demonstrate a more severe or complicated COVID-19 infection in children with juvenile idiopathic arthritis who received DMARDs [19]. In contrast, corticosteroids (at doses ≥10 mg/day prednisone equivalent), biologic drugs such as rituximab and belimumab, conventional synthetic DMARDs such as sulfasalazine, mycophenolate mofetil or tacrolimus and small molecules such as JAK inhibitors have been associated with worse COVID-19 outcomes in adult patients [9,20–24]. However, it is crucial to note that adults are more prone to having severe COVID-19 and it was found that high rheumatic disease activity is strongly associated with negative COVID-19 outcomes [21,24]. Thus, escalating anti-rheumatic treatment timely and efficiently is critical to control the rheumatic disease on the one hand and prevent severe COVID-19 on the other hand.

As the pandemic has progressed, the prevalence of severe COVID-19 in patients with rheumatic diseases has markedly diminished, aligning with trends observed in the general population [22,25]. Vaccination policies and changing virus variants are probably the main reasons for this change [22,25]. Most of our respondents also agree that vaccination policies have decreased the impact of the pandemic on pediatric rheumatology practice.

Restrictions introduced by the pandemic, such as lockdowns, have caused discontinuation or fragmentation of routine care for pediatric rheumatology patients. Thus, telemedicine tools have been progressively integrated into regular patient care. The rapidly accumulated experience has shown that virtual visits are not as effective as in-person visits [4], which provide the great advantage of performing a comprehensive physical examination and building a solid and robust patient-physician relationship. However, the option of telehealth might be critical to maintain the continuity of patient care [5]. Thus, telemedicine tools are not here to replace in-person patient care but to support and improve the quality of this care. In our previous study performed at the peak period of the pandemic [8], the shift towards telemedicine tools was more prominent than in the present study (Table 2). This finding is to be expected, given that the restrictions on in-person visits were more stringent during the peak period of the pandemic. In another recent survey, almost one-third of the parents indicated that they missed at least one follow-up visit in pediatric rheumatology clinic during the pandemic, most frequently because of the fear of COVID-19 exposure [6]. Another striking finding was that 70 % of parents preferred telemedicine visits, especially for routine check-ups [6]. However, only one-third of the parents believed they would receive the same quality of care as in-person visits [6]. In our survey, a considerable portion of respondents have indicated a shift towards telemedicine use. Although people have become more fluent in using internet-based virtual tools with the progress of the pandemic, there are still technical limitations and inequities while accessing these tools in the population. This may partially explain why one-fifth of the respondents do not use telemedicine tools in their current practice. In our study, a higher number of respondents from low-to-middle income countries has mentioned that they do not use telemedicine tools at all compared to the respondents from high income countries. This may be due to the decreased availability of telemedicine tools in low-to-middle income countries. Also, a higher percentage of respondents from low-to-middle income countries agreed that there were still delays in pediatric rheumatology care than those from high-income countries. Considering these delays still experienced in the diagnosis and management of patients, it would be beneficial to increase the use, availability, and accessibility of telemedicine tools to improve the continuity of patient care in pediatric rheumatology. Even after the pandemic, telemedicine tools will probably complement patient care by preventing missed appointments due to travel challenges or issues regarding school absenteeism.

Since MIS-C, a cytokine storm syndrome associated with COVID-19, has features similar to Kawasaki disease, pediatric rheumatologists have been involved in the management of MIS-C patients. In our study, close to 90 % of respondents indicate that they have a role in MIS-C management. A large majority of these respondents agree that managing MIS-C has boosted their perspective on managing MAS. As pediatric rheumatologists, we are constantly challenged by cases of MAS. The large number of MIS-C patients during the pandemic has increased our experience in fighting against cytokine storm syndromes considerably. The primary treatment option for around two-thirds of our respondents (who contributed to the care of MIS-C patients) was the combination of IVIG with corticosteroids, consistent with the most recent treatment recommendations for MIS-C [26]. One-fifth also used anakinra or tocilizumab in the primary treatment of MIS-C. In our recent study, we have compared propensity-score-matched (according to age, sex, comorbidities, fever duration, and the COVID-19 PCR results) groups of MIS-C patients treated with IVIG+corticosteroids and patients treated with IVIG+corticosteroids+biologics [27]. The disease was more severe, laboratory features suggested a more inflammatory phenotype, and the disease outcome was worse in the biologic group [27].

With the progress of the pandemic, the incidence of MIS-C has been decreasing [28] and outcomes have improved over time as well [29,30]. Changes in the virus strains and effective vaccination campaigns are probably the main contributors to these changes. Also, the majority of the population have developed antibodies against SARS-CoV-2 as the time passes. More than two-thirds of our respondents also agreed that vaccination policies will reduce MIS-C incidence. It is noteworthy that the clinicians have gained experience in MIS-C in the meantime, and an earlier diagnosis and an effective, timely treatment are also important contributors to the decreased severity of MIS-C.

There are some limitations in the present study. Although there were a high number of respondents from 70 countries, some parts of the world were still underrepresented. This might have introduced some non-responder bias. Also, our survey did not address the challenges regarding the access to biologic drugs due to the pandemic, the differences of the impact on the care of new and follow-up patients, or the experience of managing multidisciplinary care during the pandemic. Lastly, around 30 % of the respondents have <5 years of experience in pediatric rheumatology. Considering the presence of a subgroup who started practicing in pediatric rheumatology during the pandemic, abilities of these respondents to make a fair comparison between the pre-pandemic and pandemic periods would be limited. However, we did not identify a significant difference between less (<5 years) and more (≥5 years) experienced rheumatologists regarding the responses of the questions comparing pandemic and pre-pandemic periods.

Conclusion

Our study highlights the dynamic changes experienced in pediatric rheumatology practice during the COVID-19 pandemic. It underscores the aspects that demand improvement, including hesitancy surrounding the prescription of certain anti-rheumatic drugs, delays in routine patient care, and barriers to the use of telemedicine tools. Despite several unique challenges, patient care in pediatric rheumatology is recovering from the negative impacts of the pandemic. This survey study also provides insights about planning ahead in a future pandemic. The increased experience of using telemedicine tools during this pandemic will probably enable pediatric rheumatologists to take action more promptly during another pandemic. Our results also suggest that hesitancy regarding the use of anti-rheumatic drugs should be addressed more effectively during the early phases of a pandemic.

Abbreviations:

ACR

American college of rheumatology

CARRA

Childhood arthritis and rheumatology research alliance

COVID-19

Coronavirus disease 2019

DMARDs

Disease-modifying antirheumatic drugs

EMERGE

Emerging rheumatologists and researchers

EULAR

European league against rheumatism

IVIG

Intravenous immunoglobulin

JAK

Janus kinase

MAS

Macrophage activation syndrome

MIS-C

Multisystem inflammatory syndrome in children

NSAIDs

nonsteroidal anti-inflammatory drugs

PAFLAR

Paediatric Society of the African League Against Rheumatism

PReS

Pediatric Rheumatology European Society

SARS-CoV-2

severe acute respiratory syndrome coronavirus 2

TNF

tumor necrosis factor