Allergic patients during the COVID‐19 pandemic—Clinical practical considerations: An European Academy of Allergy and Clinical Immunology survey

Abstract Background The COVID‐19 pandemic has affected health care systems unexpectedly. However, data focusing on practical considerations experienced by health care professionals (HCPs) providing care to allergic patients is scarce. Methods Under the framework of the European Academy of Allergy and Clinical Immunology (EAACI), a panel of experts in the field of immunotherapy developed a 42‐question online survey, to evaluate real‐life consequences of the COVID‐19 pandemic in allergy practice. Results The respondents in the survey were 618. About 80% of HCPs indicated being significantly affected in their allergy practice. A face‐to‐face visit reduction was reported by 93% of HCPs and about a quarter completely interrupted diagnostic challenges. Patients with severe uncontrolled asthma (59%) and anaphylaxis (47%) were prioritized for in‐person care. About 81% maintained an unaltered prescription of inhaled corticosteroids (ICS) in asthmatics. About 90% did not modify intranasal corticosteroids (INCS) in patients with allergic rhinitis. Nearly half of respondents kept biological prescriptions unmodified for asthma. About 50% of respondents kept their allergen immunotherapy (AIT) prescription patterns unchanged for respiratory allergies; 60% for insect venom allergies. Oral immunotherapy (OIT) for food allergies was initiated by 27%. About 20% kept carrying out up‐dosing without modifications and 14% changed to more prolonged intervals. Telemedicine practice was increased. Conclusions HCPs providing care to allergic patients were affected during the pandemic in diagnostic, management, and therapeutic approaches, including AIT for respiratory, insect‐venom, and food allergies. Most HCPs maintained controller treatments for both asthma, and allergic rhinitis consistent with international recommendations, as well as biological agents in asthma. Remote tools are valuable in delivering allergy care.


Funding information
European Academy of Allergy and Clinical Immunology Methods: Under the framework of the European Academy of Allergy and Clinical Immunology (EAACI), a panel of experts in the field of immunotherapy developed a 42-question online survey, to evaluate real-life consequences of the COVID-19 pandemic in allergy practice.

Results:
The respondents in the survey were 618. About 80% of HCPs indicated being significantly affected in their allergy practice. A face-to-face visit reduction was reported by 93% of HCPs and about a quarter completely interrupted diagnostic challenges. Patients with severe uncontrolled asthma (59%) and anaphylaxis (47%) were prioritized for in-person care. About 81% maintained an unaltered prescription of inhaled corticosteroids (ICS) in asthmatics. About 90% did not modify intranasal corticosteroids (INCS) in patients with allergic rhinitis. Nearly half of respondents kept biological prescriptions unmodified for asthma. About 50% of respondents kept their allergen immunotherapy (AIT) prescription patterns unchanged for respiratory allergies; 60% for insect venom allergies. Oral immunotherapy (OIT) for food allergies was initiated by 27%. About 20% kept carrying out up-dosing without modifications and 14% changed to more prolonged intervals.
Telemedicine practice was increased.
Conclusions: HCPs providing care to allergic patients were affected during the pandemic in diagnostic, management, and therapeutic approaches, including AIT for respiratory, insect-venom, and food allergies. Most HCPs maintained controller treatments for both asthma, and allergic rhinitis consistent with international recommendations, as well as biological agents in asthma. Remote tools are valuable in delivering allergy care. The pandemic has resulted in the irreparable loss of millions of lives and an increased burden on health systems. Moreover, it has negatively impacted the economy, education, society, and other sectors. A series of adjustments were formulated rapidly to prevent virus spread, including using masks, improvement of hygiene, and physical distancing measures. 6 Furthermore, staying at home, changes in transport, and travel patterns have impacted the environment, social interaction, and routine medical practice.  [17][18][19][20][21][22][23][24] Implementing remote care was one of the most relevant recommendations proposed by international societies 14,20,25 to assess disease control, promote patients' compliance, oversee selfadministration of biologics, and provide patient education. 26 However, these remote tools are not exempt from limitations since there may be regional disparities in implementation and access. Furthermore, its effectiveness in severe conditions is limited.
As a general rule, medical consensus and guidelines are developed based on quality evidence, but given the nature of the pandemic, issuing recommendations supported by prior evidence was not feasible.
Considering the urgent need to assess the impact of the COVID-19 pandemic on the care of allergic patients, EAACI developed an international survey to generate real-life experience data.
Focusing on practical considerations, the aim was to provide information that could give rise to future management, and recommendations, even out of the pandemic.

| Domain III-SARS-CoV-2 screening methods (Q11-Q12, Q24)
Most HCPs performed a triage questionnaire prior to face-to-face visits, 19.0% required a negative SARS-CoV-2 test exclusively for patients who needed spirometry and in procedures with aerosolization high risk (Table 1). About the latter, spirometry, exercise tests, and using peak flow meter devices were considered high-risk procedures by 92.0%, 67.6%, and 66.0% of the surveyed physicians, respectively (Q24). Finally, 6.8% responded having as a mandatory requirement for in-person care a negative SARS-CoV-2 test. SARS-CoV-2 testing time before face-to-face visits is displayed in Table 1.
Frequencies of phone and online platforms used for patients' consultations are presented in Figure 2, Q30-Q31.
Interestingly, 42.2% had used telemedicine before the pandemic.
In those who had previously used it, 61.1% augmented diversely the number of teleconsultations, whereas 24% did not make modifications in this regard. Concerning participants who had not used telemedicine prior to the COVID-19 pandemic, 30.5% did not implement new teleconsultation methodologies, while 63.1% increased in a portion of their visits (Table S4).
Half of the respondents pointed out that telemedicine tools had limited efficacy not applicable to all diagnostic scenarios, and the same rate highlighted usefulness in a portion of patients, although consider them not helpful for proper management of severe conditions. Solely, about 9% were satisfied since it allowed them to provide patient care from diagnosis to therapy prescription ( Figure S2, Q35).
Data concerning the age range of patients satisfied with telemedicine care are displayed in Table S4. In general, patients under 50 years appeared to be more satisfied.

| Domain V-Planned care of allergic patients after pandemic (Q37)
Focusing on future care once the pandemic is over; 55.8% plan to wear protective masks; 40.8% will increase telemedicine use; 33.7% will require maintaining social distancing during visits and use of face masks. Remarkably, 24.1% will carry out their practice in the same manner as before the pandemic.  Figure 3).

| DISCUSSION
A few months after the pandemic declaration, a series of recommendations were issued by leading international scientific societies in the allergy field to provide guidance. 13,14,16,20,24 However, given the American experience, during the first 3 weeks of COVID-19 restrictions, all food and drug challenges were canceled as well as half of the scheduled visits, while the remaining appointments were more commonly conducted by telephone. Only 2% of face-to-face consultations were kept. 31 It is important to remark that diverse findings may reflect practice disparities influenced by regional differences in imposed restrictions and the constantly changing dynamics of the pandemic over time. 27 The present pandemic has also impacted diagnostic practice Domain III investigated SARS-CoV-2 screening methods. Respiratory diagnostic challenges, spirometry, and other airway procedures result in aerosol production. Given its inherent spreading risk, a suspension of procedures has been issued. Nonetheless, it is advised to prioritize their performance on a case-by-case basis. 20 Consistently, nine out of 10 HCPs considered spirometry as a high infectious risk procedure, while exercise tests and using peak flow meter devices were outlined as high-risk but to a lesser extent. However, although these methods were considered high risk, only 19% reported as a prerequisite a negative SARS-CoV-2 test to carry them out. Regarding screening practices before face consultations, nearly F I G U R E 2 Domain IV, Telemedicine (Q29-Q31)  Although some have reported asthma as a relatively frequent comorbidity among patients with COVID-19, 32 to date, asthma has not been robustly considered a significant risk factor for developing severe COVID-19, 33 increased risk of hospitalization 34 and mortality. 35 Furthermore, data from a multinational cohort revealed an improvement in control and outlined that asthmatic children were not disproportionately affected by SARS-CoV-2 infection. Such findings were also consistent with the results of an online survey. 36 infection, more than half continued the prescribed dose unchanged.
There has been a concern about corticosteroid effects on the out- AIT is one of the most important treatments for Immunoglobulin E (IgE)-mediated allergies as it is the only disease-modifying therapy. 19,44 An early statement advised not to initiate AIT during the pandemic for patients with allergic rhinitis unless there is an "unavoidable exposure that has resulted in anaphylaxis or asthmarelated hospitalization." 14 Moreover, the continuation of both subcutaneous and sublingual immunotherapy was suggested in noninfected patients. 19 Our findings revealed that just a few HCPs completely stopped prescribing AIT for respiratory allergies (4%) during the pandemic and a minority changed the route of administration. About one-third reduced AIT prescription. However, this query did not allow discrimination between treatment initiation and maintenance. Furthermore, interruption of AIT was discouraged, especially in potentially life-threatening allergies, such as venom allergy, 19 and in our survey, more than half did not make any VIT prescription changes. In a recent EAACI survey, almost 60% of respondents indicated not initiating AIT for respiratory allergies, while 16% switched the route from SCIT to SLIT. Moreover, VIT initiation was postponed by 40% of surveyed HCPs. 45 Other reports in the UK, Portugal, Germany, Austria, and Switzerland have described a significant reduction in VIT initiation during the COVID-19 pandemic. 28,46,47 Early recommendations advised postponing OIT treatment initiation and up-dosing until normal practice restoration. 14,16 Our findings outline that oral immunotherapy (OIT) treatment initiation and dose escalation were continued in some cases. One quarter continued initiating treatment and one-fifth continued up-dosing.
However, a high number of participants indicated not performing OIT before the pandemic.
Telehealth was encouraged considering its potential to provide remote care while assisting in physical distancing. Allergy and immunology clinicians have needed to adopt telemedicine expeditiously. 26,30 In a systematic review and meta-analysis before the pandemic, combined-telemedicine was outlined as an effective intervention for assessing and improving asthma control and patients' quality of life. 48 Also, it has been a valuable tool for providing asthma education. 49 High patient satisfaction with telemedicine encounters in allergy/immunology practice has been reported during the COVID-19 pandemic 50 and in previous reports. 51,52 Although there seems to be an apparent increase in telemedicine use worldwide since the onset of the COVID-19 pandemic, almost half of the practitioners selected direct clinical evaluation at the hospital/clinic as the preferred communication method. Half of the respondents pointed out that telemedicine tools did not apply to all diagnostic scenarios and the same rate noted that these tools worked for some of the patients but were not helpful for patients with severe conditions. Only a minority of HCPs were satisfied with telemedicine tools.
Regarding controller treatment modifications for the COVID-19 vaccination, the majority did not make any change in the ICS prescription. Also, most clinicians did not make any changes in biological agent prescriptions for planned COVID-19 vaccination (domain VI).
Concerning this matter, a recent consensus report of the German learned societies recommended the treatment and continuation of biologics (allergies and type-2 inflammation indication) during current COVID-19 vaccinations, but also emphasized a timely interval between COVID-19 vaccination and the application of the biologicals. 53 Indeed, immunosuppressive or immunomodulatory therapies, including biologics, are not contraindicated for COVID-19 vaccination. 53

| CONCLUSIONS
The

ACKNOWLEDGMENTS
The authors thank all staff members of the EAACI headquarters and specially Anna Gandaglia as well as all health care professionals who kindly supported the survey and took the time to share their valuable experience during the pandemic. This research received funding support from the EAACI. This research did not receive any specific grant from other funding agencies in the public, commercial, or notfor-profit sectors.

CONFLICT OF INTEREST
The authors declare that they have no competing interests.