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Allergy clinics in times of the SARS-CoV-2 pandemic: an integrated model

Allergy clinics in times of the SARS-CoV-2 pandemic: an integrated model Background: Almost the entire World is experiencing the Coronavirus-Disease-2019 (COVID-19) pandemic, respon- sible, at the end of May 2020, of more than five million people infected worldwide and about 350,000 deaths. In this context, a deep reorganization of allergy clinics, in order to ensure proper diagnosis and care despite of social distanc- ing measures expose, is needed. Main text: The reorganization of allergy clinics should include programmed checks for severe and poorly controlled patients, application of digital medicine service for mild-to-moderate disease in well-controlled ones, postponement of non urgent diagnostic work-ups and domiciliation of therapies, whenever possible. As far as therapies, allergen immunotherapy (AIT ) should not be stopped and sublingual immunotherapy (SLIT ) fits perfectly for this purpose, since a drug home-delivery service can be activated for the entire pandemic duration. Moreover, biologic agents for severe asthma, chronic spontaneous urticaria and atopic dermatitis should be particularly encouraged to achieve best control possible of severe disease in times of COVID-19 and, whenever possible, home-delivery and self-administra- tion should be the preferred choice. Conclusion: During COVID-19 pandemic, allergists have the responsibility of balancing individual patients’ needs with public health issues, and innovative tools, such as telemedicine and digital medicine services, can be helpful to reduce the risk of viral spreading while delivering up-to-date personalized care. Keywords: Allergy, Asthma, COVID-19, SARS-CoV-2, Pandemic, Immunotherapy, Biologicals, Telemedicine, Digital medicine service, Home delivery Introduction systems in order to ensure diagnosis and care for patients The recent Coronavirus-Disease-2019 (COVID-19) pan - and contemporaneously trying to expose them to the demic has radically changed health priorities and the minimum risk of contracting the infection in hospi- management of non Covid-19 diseases. At the time of tal or outpatient clinics. In addition, there is continu- writing (end of May 2020), more than five million peo - ous new scientific knowledge about the novel virus that ple in the world have been infected and about three hun- changes the indications on how to treat and prevent it. dred and fifty thousand have died from COVID 19 [1]. In this perspective, allergists have to adapt to the change This has resulted in a deep reorganization of health-care by managing their patients keeping in mind that some allergic diseases of the upper and lower airways, such as allergic rhinitis, chronic rhinosinusitis with nasal polyps *Correspondence: enrico.heffler@hunimed.eu (CRSwNP) and asthma have symptoms in common with Personalized Medicine, Asthma and Allergy, Humanitas Clinical COVID-19. and Research Center IRCCS, Via Alessandro Manzoni 56, Rozzano, MI, Italy Full list of author information is available at the end of the article © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. 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Clin Transl Allergy (2020) 10:23 Page 2 of 9 Anxiety is associated to both chronic airways diseases Clinical features of COVID‑19 and differential and COVID-19 pandemic, acting as a confounding fac- diagnosis with allergic diseases tor that should be carefully factored in when interpret- The susceptibility to and severity of Severe Acute Res - ing subjective symptoms. From a different perspective, it piratory Syndrome-Coronavirus-2 (SARS-Cov-2) infec- has been reported that COVID-19 patients might present tion positively correlate with age and comorbidities like with skin signs and symptoms of urticaria and eczema hypertension, diabetes and cardiovascular disease [2]. resembling those acute urticaria or drug reactions, thus The spectrum of clinical presentations is variable, from posing a diagnostic challenge to dermatologists and aller- asymptomatic and mild clinical symptoms to acute res- gists [4]. Therefore, in this kind of patients, it is important piratory-distress syndrome (ARDS) [3]. Adults with mild to focus attention on symptoms typical for COVID-19, COVID-19 most commonly manifest fever, cough, con- manly fever but also excessive fatigue and impaired sense junctivitis, fatigue and anosmia, which in some patients of smell or taste, to obtain a correct diagnosis (Fig.  1). can be accompanied by runny nose and headache. In Two apps have been developed to assess both COVID-19 the more severe clinical presentations, the patient feels (MASK-COVID) and asthma/rhinitis (MASK-air, availa- worsening dyspnoea and general exhaustion. Additional ble in 18 languages). A combined MASK-air-COVID app symptoms such as diarrhea are less common. When the will be launched and will differentiate rhinitis/asthma virus affects the lung, it can cause interstitial pneumonia symptoms from those of COVID-19 (personal communi- [2]. The most severe manifestations appear to be related cation form Prof. Bousquet). to an excessive immune system response (“cytokine storm”) that leads to development of ARDS and respira- The need for mitigation efforts tory failure requiring invasive ventilation. Healthcare systems have been implemented to ensure Some allergic diseases, like allergic rhinitis, CRSwNP citizens’ right of receiving appropriate and prompt care, and asthma, can simulate symptoms of COVID-19: as declared by the bill of right of many European Coun- cough and dyspnoea are shared with asthma, while runny tries. In pandemics, unanticipated stresses challenge nose and headache are frequent symptoms in allergic rhi- healthcare systems efficiency and performance, given the nitis and CRSwNP. In addition, this pandemic started in acute extraordinary shifts in patients’ needs and alloca- the spring season when the majority of patients with sea- tion of resources. Of course, a number of measures can sonal allergies suffers from partially similar symptoms. Fig. 1 Differential diagnosis of allergic airway diseases and SARS-CoV-2 infection M alipiero et al. Clin Transl Allergy (2020) 10:23 Page 3 of 9 be enacted to slow the pace of epidemic spread and keep this aim, a risk-stratified approach can be applied by con - health-care systems accessible to everyone. That would sidering patients’ clinical needs and in accordance to local translate into a more favorable distribution of resources, and institutional policies. Therefore, acute service reduc - meantime allowing for serological tests, results of rand- tion can be arranged through combinations of measures omized double-blind placebo-controlled trials and mass that could change form nation to nation according to vaccination to become available. local epidemiology and socio-political trends. In such a The first and obvious measure is quarantining of highly dynamic setting, it is difficult to forecast how long infected individuals, which is nonetheless limited by the pandemic will last and whether subsequent “waves” the challenge of identifying and isolating asymptomatic of COVID-19 will require additional lockdowns before individuals and the high false negative rate of microbio- herd immunity is reached or a vaccine becomes available. logical screening tests [5]. Next, use of protective equip- u Th s integrated planning is essential to keep allergy clin - ment, especially by health-care providers, is a mainstay ics and allergists operative in the long-term. of mitigation strategy but might be limited by shortage In general, acute access to allergic emergency or life- of material or misuse due to lack of operative skills. In threatening acute events is mandatory even during pan- the context of uncontrollable spreading of communica- demics. As to outpatients, scheduled in-person visits ble diseases, social limitations and home confinement for severe and poorly controlled allergic diseases should are extreme measures, even though made more bearable be regularly provided, by instructing patients to enter by the availability of social digital technologies. To make the clinic in a precise time-range and respect social dis- social distancing more feasible, a number of issues should tancing. To reduce the risk of in-hospital spread of the be addressed and, in the context of care delivering, infection, COVID-19 and COVID-19 free-zones can be reducing unnecessary direct patients’ interaction with created by predisposing check-points at COVID-19 free- health-care providers is a priority requiring maximum zone entrance to detect patients with fever (> 37.5  °C), efforts to adapt to and may be prolonged to the post- screen for symptoms of active infection and/or con- pandemic period, according to transmission dynamics tact with COVID-19 positive individuals. Conversely, of SARS-CoV-2 [6]. There is particular concern for aging accesses for mild-to-moderate disease in well-controlled individuals, where coexisting comorbidities and con- patients can be transitioned to a digital medicine service sequent polypharmacy carry the risk of adverse events (DMS), including phone, video and email consults [10]. in terms of loss of control of chronic diseases, lack of Telehealth has the advantage of respecting social distanc- therapeutic adherence, drug-related adverse events and ing, thus reducing the risk of viral transmission. When need for urgent care, which would put both the patient patients experience worsening symptoms requiring and health care providers at risk of infection. In addi- timely evaluation, digital tele-triaging should be arranged tion, uncontrolled chronic airway diseases could con- in order to segregate patients suitable for remote moni- tribute to SARS-CoV-2 dissemination through coughing toring and therapeutic adjustment (for example, by pro- or sneezing, especially during periods of increased pol- viding them with an up-to-date action plan) from those len exposure. Delivering targeted educational programs requiring in-person visits and access to health-care facili- and action plans to enact in case of disease exacerbation ties. Psychological and physical barriers to treatment is essential. Patients should be routinely checked about adherence and comorbidities causing loss of control their technical skills (e.g. inhaler use) and treatment might be safely addressed and resolved by teleconsulta- adherence and remotely monitored for initial signs of tions. Moreover, digital teletriaging of patients experi- physical or psychological decompensation, possibly by encing worsening respiratory symptoms can provide using mobile health technology [7]. an invaluable aid at suspecting COVID-19 and activat- ing general practitioners to monitor and/or investigate Allergy clinic at COVID‑19 times: the dawn of a new suspected patients [11]. Patients waiting for diagnostic era for telemedicine and digital medicine work-up or experiencing troublesome lack of comfort Since allergic diseases are highly heterogeneous in sever- with therapeutic recommendations can access to digi- ity and risk of exacerbation, both at inter- and intra- tal platforms in order to contact their caring specialist. patient levels, in the event of acute outpatients’ service Objective questionnaires administered on-line may help rationing aimed at mitigating virus spread, patients’ deal with patients who poorly perceive their symptoms. access to allergy services has to be rationalized [8, 9]. A We specify that some of these clinical interventions and gradual escalation in acute service reduction would be ascertainments may be provided by health providers col- preferable but might not be applicable in case of tumul- laborating with allergists in multidisciplinary teams, such tuous spread of the virus. Similarly, “phase 2” re-opening as specialized nurses, dietitians, ENT physicians and policies should be based on gradualism and prudence. To psychologists. Malipiero et al. Clin Transl Allergy (2020) 10:23 Page 4 of 9 It should be noted that virtual care has to be delivered by the local Pharmacy [9]. This can prove a fruitful according to national laws and by licensed providers. This advantage of SLIT over subcutaneous immunotherapy could represent a problem where laws governing virtual (SCIT), in keeping patients adherent to AIT; transition care are not available or not up-to-date to ever modern- from SCIT to SLIT might be considered as a possible izing tools. Standardized digital platforms should be pro- management strategy during COVID-19 pandemic. SCIT vided to patients and health-care providers, accessible for hymenoptera venom allergy should be continued through a digital identity, in order to avoid misconducts although increasing administration interval can be con- and retain information in case of legal allegations [12]. sidered during long-term maintenance. In confirmed or Meantime, other more common and widespread tools suspected COVID-19 patients, AIT should not be started might be used, provided a properly informed consent to and should be temporarily interrupted if already pre- being treated via telemedicine has been obtained from scribed. AIT-specific recommendations are summarized the patient, when admitted by national laws on general in Table 1 [15]. data protection. First line anti-allergy agents, such as anti-histamines Diagnostic work-up can be postponed in the great and low-dose steroids, are not likely to affect immu - majority of allergic diseases, provided affected patients nocompetence and should not be discontinued during are well instructed about avoidance of potential environ- the pandemic (for disease specific recommendations, mental triggers and treatment of acute events, also based see  “Disease-specific management ” section), provided on written action plans [13, 14]. Anyway, diagnostic pro- systemic corticosteroid posology remains under the cedures should be reconsidered as soon as pandemic immunosuppressive threshold [16–18] and that all strat- becomes more controlled and confinement de-escalation egies to reduce systemic corticosteroid use should be begins. applied independently from the pandemic [19]. Notably, Therapeutic management deserves particular attention. regular steroid-based regimens, including inhaled and Whenever possible, therapeutic maneuvers not requiring oral corticosteroids, should not be stopped, since abrupt hospital access should be domiciled. interruption would bring along an increased risk of adre- In SARS-Cov-2 negative, low-risk individuals, allergen nal insufficiency in case of acute stressing events, as immunotherapy (AIT) should not be stopped and actu- COVID-19 is [20]. Conversely, a pulsed dose of steroids ally can be started in naive patients provided the required could result in a protective effect in such a circumstance infrastructure is in place during the pandemic [15]. We [21]. underline that sublingual immunotherapy (SLIT) for air- Second-line steroid sparing immunomodulat- borne allergens allows not suspending AIT and can be a ing agents are potentially detrimental on immunity valid and safe alternative for patients about to undergo although clear-cut distinctions exist between nonspe- SCIT, as far as a drug home-delivering service is activated cific immunosuppressive drugs, like cyclosporine and Table 1 AIT recommendations (adapted from Klimek et al. 2020), [19] Recommendations in non COVID-19 individuals Interrupting subcutaneous immunotherapy is not advised. Especially in potentially life-threatening allergies, such as venom allergy, SCIT should be regularly continued. The possibility of expanding injection intervals in the continuation phase should be checked and may be beneficial Interrupting sublingual immunotherapy is not advised. Supply the patient with sufficient medication for a minimum of 14 days isolation Sublingual immunotherapy can be taken at home. The intake of SLIT by the patient at home or any place is advantageous in avoiding contact with potentially infected persons Both subcutaneous and sublingual immunotherapy can be continued in the current COVID-19 pandemics, in any asymptomatic patient without suspi- cion for SARS-CoV-2 infection and/or contact with SARS-CoV-2 positive individuals, in any patient with negative test result (RT-PCR) or in any patient after an adequate quarantine or with detection of serum IgG to SARS-CoV-2 without virus-specific IgM Preparedness of your Allergy clinic is imperative to cope with COVID-19. Follow World Health Organization ( WHO) guidelines and advice staff accord- ingly These recommendations are conditional since there is paucity of data and they should be revised regularly with incoming new information on COVID- Recommendations in COVID-19 diagnosed cases or suspicion for SARS-CoV-2 infection Interrupting subcutaneous immunotherapy is advised Interrupting sublingual immunotherapy is advised Both subcutaneous and sublingual immunotherapy should be discontinued in symptomatic patients with exposure or contact with SARS-CoV-2 posi- tive individuals, or patients with positive test results (RT-PCR) M alipiero et al. Clin Transl Allergy (2020) 10:23 Page 5 of 9 azathioprine, and biological agents targeting discrete questionnaires and monitor domiciliary drug self- molecular pathways associated with type 2 allergic administration [9]. inflammation. In fact, besides inducing nonspecific Disease-specific measures and therapeutic recommen - suppression of anti-infective immunity, nonbiological dations are rapidly provided in the following sections agents are strong inducers of hepatic cytochromes, thus and graphically resumed in Fig.  2. In the case of atopic requiring plasma level monitoring when used in com- multimorbidity, priority should be given to uncontrolled/ bination with antimicrobial agents [22]. According to severe components over well-controlled/mild ones. a WAO paper [23], no definitive evidence is presently available to obligate clinical decision making. As anti- Disease‑specific management IgE, ant-IL5/IL5R and anti IL4/IL3R biologics are not Asthma likely to induce immunosuppression or interfere with Asthma-specific recommendations from Global Initiative virus clearance (actually the contrary seems to hold for Asthma (GINA) are reported in Table 2 [30]. Data are true, at least for omalizumab [24] and dupilumab [25], controversial regarding the interaction between asthma while mepolizumab treatment was not associated with and COVID-19 as European and Chinese data suggest a worse immunological response to viruses [26, 27]), lower risk for asthmatic patients to contract the infection they can be safely continued. Anyway, until evidence- [31] while U.S. data suggest the opposite [32]. Probably based data are available, some countries, like the UK, this association is modulated by the severity of asthma, have advised home confinement for at least 12  weeks age class, and levels of indoor and outdoor, allergen and to patients with severe asthma on systemic immuno- pollution exposures. With knowledge evolving, GINA suppressants or biological therapy. Steroid-sparing and the British National Institute for Health and Care effect of biologics is a potential advantage over steroid Excellence (NICE) guidelines recommend not stopping therapy since patients on chronic steroid therapy can the regular treatment regimen, including inhaled and oral be affected by subclinical adrenal insufficiency [20]. corticosteroids [30, 33], since abrupt interruption would Depending on the specific monoclonal antibody, in-site bring along an increased risk of acute/severe exacerba- administration or home-delivery and self-administra- tions or adrenal insufficiency [21]. Every patient should tion can be the preferred choice. When patients live be provided with a detailed and convenient action plan to far away from the Centre, National Networks can be deal with potential loss of control [13], and invited to reg- activated in order to identify a local near-home Centre ularly use mobile health technology apps to self-monitor for in-site administration (in Italy the Severe Asthma symptoms of their asthma [7]. Aerosol generating proce- Network in Italy (SANI) [28, 29]). In case of infection, dures are discouraged unless essential and lung function discontinuation should be discussed on a case-by-case testing should be postponed whenever possible [30]. basis. We should also consider the complexity of allergic Allergic rhino-conjunctivitis patients and the synchronous atopic involvement of Allergic rhino-conjunctivitis-specific recommendations multiple organs that interface with the environment’. from allergic rhinitis and its impact on asthma (ARIA) Therefore, as far as precision medicines targeting nodal and European Academy of Allergy and Clinical Immu- pathogenic pathways allow to treat “atopy” as a whole, nology (EAACI) are reported in Table 3 [15, 34]. Allergic we claim priority and lower prescription threshold rhinitis visits should not be prioritized and can be safely could be assigned to biologicals, given the good safety postponed unless exceptional circumstances supervene. profile, the lack of interference with drug metabolism Intranasal steroids do not induce immunosuppression and the favorable effect on treatment adherence. The and are not to discontinue [34]. As stated above, optimal regulatory agencies should address these new needs in disease control is mandatory as sneezing in asympto- pandemic times and coordinate with health care pur- matically infected patients can contribute to viral spread; chasers to make biological more accessible. mobile applications can contribute in improving optimal Clinical research has been seriously threatened by self-management of rhinitis [7]. For AIT-specific recom - COVID-19 epidemics. New recruitments in ongoing mendations, see Table 1 [15]. clinical trials have been temporarily suspended. Inves- tigators can consult with sponsors in order to reas- Chronic rhinosinusitis sess follow-up visit schedules and amend protocol We are unaware of specific recommendations from requirements to facilitate online visits. When accorded medical societies about this topic. For reasons analo- with the Sponsor and local Pharmacy, investigational gous to those specified for allergic rhino-conjunctivitis, product home-delivery service and a digital medi- it is commonsense to keep patients on regular treat- cine service can be activated to administer scheduled ments. Patients with uncontrolled disease or waiting for Malipiero et al. Clin Transl Allergy (2020) 10:23 Page 6 of 9 Fig. 2 An integrated model of tele- and digital-allergy clinic during COVID-19 pandemic. Suggested actions to be implemented in order to re-organize an allergy clinic are reported in boxes for asthma, rhino-conjunctivitis, atopic dermatitis and food allergy, anaphylaxis, drug and venom hypersensitivity and CSU. The truck represents the home-delivery service that should be activated for biologicals, AIT and self-injectable adrenaline Table 2 Asthma‑specific recommendations from Global Initiative for Asthma (GINA) as reported on GINA website [34] People with asthma should continue all of their inhaled medication, including inhaled corticosteroids, as prescribed by their doctor In acute asthma attacks patients should take a short course of oral corticosteroids if instructed in their asthma action plan or by their healthcare pro- vider, to prevent serious consequences In rare cases, patients with severe asthma might require long-term treatment with oral corticosteroids (OCS) on top of their inhaled medication(s). This treatment should be continued at the lowest possible dose in these patients at risk of severe attacks/exacerbations. Biologic therapies should be used in severe asthma patients who qualify for them, in order to limit the need for OCS as much as possible Nebulizers should, where possible, be avoided for acute attacks due to the increased risk of disseminating COVID-19 (to other patients AND to physi- cians, nurses and other personnel) Pressurized metered dose inhaler (pMDI) via a spacer is the preferred treatment during severe attacks. (Spacers must not be shared at home) While a patient is being treated for a severe attack, their maintenance inhaled asthma treatment should be continued (at home AND in the hospital) Patients with allergic rhinitis should continue to take their nasal corticosteroids, as prescribed by their clinician Routine spirometry testing should be suspended to reduce the risk of viral transmission, and if absolutely necessary, adequate infection control meas- ures should be taken Table 3 Allergic rhino‑ conjunctivitis‑specific recommendations from ARIA/EAACI (from: Bousquet et al. 2020) [37] With the current knowledge, in patients with COVID-19 infection, intra-nasal corticosteroid (including spray) can be continued in allergic rhinitis at the recommended dose Stopping local intra-nasal corticosteroid is not advised. Suppression of the immune system has not been proven and more sneezing after stopping means more spreading of the Coronavirus These recommendations are conditional since there is a paucity of data and they should be revised regularly with new knowledge M alipiero et al. Clin Transl Allergy (2020) 10:23 Page 7 of 9 Ear-Nose-Throat (ENT) surgery could be transitioned to chronic spontaneous urticaria), in whom shift to a bio- biological treatment whenever possible. logical agent with a more favorable safety profile might be considered on a case-by-case basis (e.g. close contact with infected individuals, active infection) [40]. For new Atopic dermatitis and food allergy evaluations, diagnostic procedures should be postponed Disseminated skin viral infections are a major compli- during the epidemics peak and reconsidered on a sec- cation of severe/uncontrolled atopic dermatitis. It is ond time, unless urgently needed (e.g. severe reactions unknown whether increased risk of SARS-Cov-2 infec- to Hymenoptera venom). We highlight that urticaria can tion or disease severity is associated with atopic der- be a presenting sign of COVID-19 and allergy to drugs matitis due to impaired cutaneous barrier. Patients on used to treat COVID-19 can present with rashes that may immunosuppressive therapy for severe atopic dermati- involve the allergist’s evaluation [4]. tis should be strictly monitored or transitioned to safer anti-IL4/IL13 immune-modulatory agents, as advocated by the European Task Force on atopic dermatitis [35, 36]. Conclusion Safe use of Dupilumab in severe AD patients affected We are now in the middle of the storm and we do not by COVID-19 has been recently reported [37]. Food know how long it will last or whether additional con- allergy and allergic gastrointestinal diseases are preva- sequences are on the horizon. In these times of sus- lent comorbidities in atopic dermatitis, especially in chil- pense, we have the responsibility of balancing individual dren; careful evaluation is needed and food challenge patients’ needs with public health issues. To our mind, a should be performed to prevent unnecessary food avoid- black-and-white thinking does not suit a scientific way ance interfering with growth and micronutrients bal- of addressing theoretical and practical problems. We ance [38]. Food allergy in asthma is of particular concern therefore advocate for a risk-stratified approach aimed since it has been associated with fatal asthma. Asthmatic at conjugating COVID-19 and non-COVID-19 health patients with food allergies may need to be provided with care needs of allergic patients. We have to reshape our epinephrine auto injectors (see the following section on practice and optimize those innovative tools that help anaphylaxis management) and should avoid introducing us reduce the risk of viral spreading while delivering up- new foods in their diets during the pandemic as long as to-date personalized care. A new era of integrated preci- the risk of contagion is high [38]. sion-digital medicine is knocking at the door. Anaphylaxis A modified anaphylaxis management algorithm dur - Abbreviations ing COVID-19 pandemic has been proposed by Casale ACE-2: Angiotensin-converting enzyme-2; AIT: Allergen immunotherapy; ARDS: Acute respiratory distress syndrome; ARIA: Allergic rhinitis and its et  al. [39]. Patients are invited to carry two epinephrine impact on asthma; COVID-19: Coronavirus-Disease 2019; CRSwNP: Chronic injectors and to activate emergency services only when rhinosinusitis with nasal polyps; DMS: Digital medicine service; EAACI: Euro- a second administration of epinephrine fails to control pean Academy of Allergy and Clinical Immunology; ENT: Ear-Nose-Throat; GINA: Global initiative for asthma; NICE: National Institute for Health and Care symptoms. It might be prudent to proactively discuss Excellence; OCS: Oral corticosteroids; pMDI: Pressurized metered dose inhaler; the modified management of anaphylaxis, if feasible, e.g., SANI: Severe Asthma Network in Italy; SARS-CoV-2: Severe Acute Respiratory via telemedicine. Home delivery service of self-injectable Syndrome-Coronavirus-2; SCIT: Subcutaneous immunotherapy; SLIT: Sublin- gual immunotherapy; TLR: Toll-like receptor; WHO: World Health Organization. adrenaline should be implemented, provided the patient has been instructed on the underlying disease, triggers Acknowledgements avoidance measures and proper use. Not applicable. Author’s contributions Drug allergy, hymenoptera venom allergy and urticaria/ GM, GP, EH and GWC contributed in conception and drafting the review article; CP, FP, FR, SF, LS, DL, GC, MM, MS: contributed in critically interpret and angioedema revise the article. All authors read and approved the final manuscript. Expert recommendations and consensus on these top- ics during COVID-19 epidemics are missing at the time Funding No funds for this review article. of this manuscript being written. As a general princi- ple, we maintain that ongoing treatment for these con- Availability of data and materials ditions should not to be discontinued in order to keep Not applicable. disease under control as far as these treatments are not Ethics approval and consent to participate likely to increase the risk of SARS-Cov-2 infection or Not applicable. complicate COVID-19 course in case of infection. A Consent for publication possible exception might be represented by patients Requested (pending) (for reproducing Tables 1 and 3). on immunosuppressive regimens (e.g. cyclosporine for Malipiero et al. Clin Transl Allergy (2020) 10:23 Page 8 of 9 Competing interests 12. Portnoy J, Waller M, Elliott T. Telemedicine in the Era of COVID- Enrico Heffler reports personal fees from AstraZeneca, Sanofi, Novartis, Teva, 19. J Allergy Clin Immunol Pract. 2020. https ://doi.org/10.1016/j. GSK, Circassia, Boehringer Ingelheim, Valeas, Nestlè Purina, outside the submit- jaip.2020.03.008. ted work. Giorgio Walter Canonica reports grants and personal fees from 13. Rank MA, Volcheck GW, Li JT, Patel AM, Lim KG. Formulating an Menarini, Alk Abello’, Anallergo Boehringer Ingelheim, Chiesi, Circassia, Genen- effective and efficient written asthma action plan. Mayo Clin Proc. tech, Guidotti Malesci, GSK, Hal Allergy, Meda, Merck, Merck Sharp & Dome 2008;83(11):1263–70. https ://doi.org/10.4065/83.11.1263. Novartis Recordati-InnuvaPharma, Roche, Sanofi Stallergenes, UCB Pharma, 14. Wang J, Sicherer SH. Section on allergy and immunology. Guidance on Uriach Pharma, Teva Astrazeneca, Thermo Fisher, Valeas, Vibor Pharma, outside completing a written allergy and anaphylaxis emergency plan. Pediat- the submitted work. Francesca Puggioni reports personal fees from Astra- rics. 2017;139(3):e20164005. https ://doi.org/10.1542/peds.2016-4005. zeneca, Chiesi, GSK, Guidotti, Menarini, Mundipharma Novartis, Sanofi, Valeas, 15. Klimek L, Jutel M, Akdis C, Bousquet J, Akdis M, Bachert C, Agache I, Allergy Therapeutics, Almirall outside the submitted work. Giovanni Paoletti Ansotegui I, Bedbrook A, Bosnic-Anticevich S, Canonica GW, Chivato T, reports personal fees from Novartis and Lusofarma, outside the submitted Cruz AA, Czarlewski W, Giacco SD, Du H, Fonseca JA, Gao Y, Haahtela T, work. Giacomo Malipiero reports personal fees from Allergy Therapeutics, Hoffmann-Sommergruber K, Ivancevich JC, Khaltaev N, Knol EF, Kuna P, outside the submitted work. Francesca Racca, Corrado Pelaia, Sebastian Ferri, Larenas-Linnemann D, Melen E, Mullol J, Naclerio R, Ohta K, Okamoto Donatella Lamacchia, Giuseppe Cataldo, Lina Spinello, Melissa Sansonna, and Y, O’Mahony L, Onorato GL, Papadopoulos NG, Pawankar R, Pfaar O, Morena Merigo do not have potential conflict of interest to declare. 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Wang C, Rademaker M, Baker C, Foley P. COVID-19 and the use of immu- AA, Czarlewski W, DelGiacco S, Du H, Fonseca JA, Gao Y, Haahtela T, nomodulatory and biologic agents for severe cutaneous disease: an Hoffmann-Sommergruber K, Ivancevich JC, Khaltaev N, Knol EF, Kuna P, Australia/New Zealand consensus statement. Australas J Dermatol. 2020. Larenas-Linnemann D, Mullol J, Naclerio R, Ohta K, Okamoto Y, O’Mahony https ://doi.org/10.1111/ajd.13313 (Epub ahead of print). L, Onorato GL, Papadopoulos NG, Pfaar O, Samolinski B, Schwarze J, Toppila-Salmi S, Teresa Ventura M, Valiulis A, Yorgancioglu A, Zuberbier T. Publisher’s Note Intranasal corticosteroids in allergic rhinitis in COVID-19 infected patients: Springer Nature remains neutral with regard to jurisdictional claims in pub- an ARIA-EAACI statement. Allergy. 2020. https ://doi.org/10.1111/all.14302 lished maps and institutional affiliations. (Epub ahead of print). Ready to submit your research ? 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Allergy clinics in times of the SARS-CoV-2 pandemic: an integrated model

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Abstract

Background: Almost the entire World is experiencing the Coronavirus-Disease-2019 (COVID-19) pandemic, respon- sible, at the end of May 2020, of more than five million people infected worldwide and about 350,000 deaths. In this context, a deep reorganization of allergy clinics, in order to ensure proper diagnosis and care despite of social distanc- ing measures expose, is needed. Main text: The reorganization of allergy clinics should include programmed checks for severe and poorly controlled patients, application of digital medicine service for mild-to-moderate disease in well-controlled ones, postponement of non urgent diagnostic work-ups and domiciliation of therapies, whenever possible. As far as therapies, allergen immunotherapy (AIT ) should not be stopped and sublingual immunotherapy (SLIT ) fits perfectly for this purpose, since a drug home-delivery service can be activated for the entire pandemic duration. Moreover, biologic agents for severe asthma, chronic spontaneous urticaria and atopic dermatitis should be particularly encouraged to achieve best control possible of severe disease in times of COVID-19 and, whenever possible, home-delivery and self-administra- tion should be the preferred choice. Conclusion: During COVID-19 pandemic, allergists have the responsibility of balancing individual patients’ needs with public health issues, and innovative tools, such as telemedicine and digital medicine services, can be helpful to reduce the risk of viral spreading while delivering up-to-date personalized care. Keywords: Allergy, Asthma, COVID-19, SARS-CoV-2, Pandemic, Immunotherapy, Biologicals, Telemedicine, Digital medicine service, Home delivery Introduction systems in order to ensure diagnosis and care for patients The recent Coronavirus-Disease-2019 (COVID-19) pan - and contemporaneously trying to expose them to the demic has radically changed health priorities and the minimum risk of contracting the infection in hospi- management of non Covid-19 diseases. At the time of tal or outpatient clinics. In addition, there is continu- writing (end of May 2020), more than five million peo - ous new scientific knowledge about the novel virus that ple in the world have been infected and about three hun- changes the indications on how to treat and prevent it. dred and fifty thousand have died from COVID 19 [1]. In this perspective, allergists have to adapt to the change This has resulted in a deep reorganization of health-care by managing their patients keeping in mind that some allergic diseases of the upper and lower airways, such as allergic rhinitis, chronic rhinosinusitis with nasal polyps *Correspondence: enrico.heffler@hunimed.eu (CRSwNP) and asthma have symptoms in common with Personalized Medicine, Asthma and Allergy, Humanitas Clinical COVID-19. and Research Center IRCCS, Via Alessandro Manzoni 56, Rozzano, MI, Italy Full list of author information is available at the end of the article © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Malipiero et al. Clin Transl Allergy (2020) 10:23 Page 2 of 9 Anxiety is associated to both chronic airways diseases Clinical features of COVID‑19 and differential and COVID-19 pandemic, acting as a confounding fac- diagnosis with allergic diseases tor that should be carefully factored in when interpret- The susceptibility to and severity of Severe Acute Res - ing subjective symptoms. From a different perspective, it piratory Syndrome-Coronavirus-2 (SARS-Cov-2) infec- has been reported that COVID-19 patients might present tion positively correlate with age and comorbidities like with skin signs and symptoms of urticaria and eczema hypertension, diabetes and cardiovascular disease [2]. resembling those acute urticaria or drug reactions, thus The spectrum of clinical presentations is variable, from posing a diagnostic challenge to dermatologists and aller- asymptomatic and mild clinical symptoms to acute res- gists [4]. Therefore, in this kind of patients, it is important piratory-distress syndrome (ARDS) [3]. Adults with mild to focus attention on symptoms typical for COVID-19, COVID-19 most commonly manifest fever, cough, con- manly fever but also excessive fatigue and impaired sense junctivitis, fatigue and anosmia, which in some patients of smell or taste, to obtain a correct diagnosis (Fig.  1). can be accompanied by runny nose and headache. In Two apps have been developed to assess both COVID-19 the more severe clinical presentations, the patient feels (MASK-COVID) and asthma/rhinitis (MASK-air, availa- worsening dyspnoea and general exhaustion. Additional ble in 18 languages). A combined MASK-air-COVID app symptoms such as diarrhea are less common. When the will be launched and will differentiate rhinitis/asthma virus affects the lung, it can cause interstitial pneumonia symptoms from those of COVID-19 (personal communi- [2]. The most severe manifestations appear to be related cation form Prof. Bousquet). to an excessive immune system response (“cytokine storm”) that leads to development of ARDS and respira- The need for mitigation efforts tory failure requiring invasive ventilation. Healthcare systems have been implemented to ensure Some allergic diseases, like allergic rhinitis, CRSwNP citizens’ right of receiving appropriate and prompt care, and asthma, can simulate symptoms of COVID-19: as declared by the bill of right of many European Coun- cough and dyspnoea are shared with asthma, while runny tries. In pandemics, unanticipated stresses challenge nose and headache are frequent symptoms in allergic rhi- healthcare systems efficiency and performance, given the nitis and CRSwNP. In addition, this pandemic started in acute extraordinary shifts in patients’ needs and alloca- the spring season when the majority of patients with sea- tion of resources. Of course, a number of measures can sonal allergies suffers from partially similar symptoms. Fig. 1 Differential diagnosis of allergic airway diseases and SARS-CoV-2 infection M alipiero et al. Clin Transl Allergy (2020) 10:23 Page 3 of 9 be enacted to slow the pace of epidemic spread and keep this aim, a risk-stratified approach can be applied by con - health-care systems accessible to everyone. That would sidering patients’ clinical needs and in accordance to local translate into a more favorable distribution of resources, and institutional policies. Therefore, acute service reduc - meantime allowing for serological tests, results of rand- tion can be arranged through combinations of measures omized double-blind placebo-controlled trials and mass that could change form nation to nation according to vaccination to become available. local epidemiology and socio-political trends. In such a The first and obvious measure is quarantining of highly dynamic setting, it is difficult to forecast how long infected individuals, which is nonetheless limited by the pandemic will last and whether subsequent “waves” the challenge of identifying and isolating asymptomatic of COVID-19 will require additional lockdowns before individuals and the high false negative rate of microbio- herd immunity is reached or a vaccine becomes available. logical screening tests [5]. Next, use of protective equip- u Th s integrated planning is essential to keep allergy clin - ment, especially by health-care providers, is a mainstay ics and allergists operative in the long-term. of mitigation strategy but might be limited by shortage In general, acute access to allergic emergency or life- of material or misuse due to lack of operative skills. In threatening acute events is mandatory even during pan- the context of uncontrollable spreading of communica- demics. As to outpatients, scheduled in-person visits ble diseases, social limitations and home confinement for severe and poorly controlled allergic diseases should are extreme measures, even though made more bearable be regularly provided, by instructing patients to enter by the availability of social digital technologies. To make the clinic in a precise time-range and respect social dis- social distancing more feasible, a number of issues should tancing. To reduce the risk of in-hospital spread of the be addressed and, in the context of care delivering, infection, COVID-19 and COVID-19 free-zones can be reducing unnecessary direct patients’ interaction with created by predisposing check-points at COVID-19 free- health-care providers is a priority requiring maximum zone entrance to detect patients with fever (> 37.5  °C), efforts to adapt to and may be prolonged to the post- screen for symptoms of active infection and/or con- pandemic period, according to transmission dynamics tact with COVID-19 positive individuals. Conversely, of SARS-CoV-2 [6]. There is particular concern for aging accesses for mild-to-moderate disease in well-controlled individuals, where coexisting comorbidities and con- patients can be transitioned to a digital medicine service sequent polypharmacy carry the risk of adverse events (DMS), including phone, video and email consults [10]. in terms of loss of control of chronic diseases, lack of Telehealth has the advantage of respecting social distanc- therapeutic adherence, drug-related adverse events and ing, thus reducing the risk of viral transmission. When need for urgent care, which would put both the patient patients experience worsening symptoms requiring and health care providers at risk of infection. In addi- timely evaluation, digital tele-triaging should be arranged tion, uncontrolled chronic airway diseases could con- in order to segregate patients suitable for remote moni- tribute to SARS-CoV-2 dissemination through coughing toring and therapeutic adjustment (for example, by pro- or sneezing, especially during periods of increased pol- viding them with an up-to-date action plan) from those len exposure. Delivering targeted educational programs requiring in-person visits and access to health-care facili- and action plans to enact in case of disease exacerbation ties. Psychological and physical barriers to treatment is essential. Patients should be routinely checked about adherence and comorbidities causing loss of control their technical skills (e.g. inhaler use) and treatment might be safely addressed and resolved by teleconsulta- adherence and remotely monitored for initial signs of tions. Moreover, digital teletriaging of patients experi- physical or psychological decompensation, possibly by encing worsening respiratory symptoms can provide using mobile health technology [7]. an invaluable aid at suspecting COVID-19 and activat- ing general practitioners to monitor and/or investigate Allergy clinic at COVID‑19 times: the dawn of a new suspected patients [11]. Patients waiting for diagnostic era for telemedicine and digital medicine work-up or experiencing troublesome lack of comfort Since allergic diseases are highly heterogeneous in sever- with therapeutic recommendations can access to digi- ity and risk of exacerbation, both at inter- and intra- tal platforms in order to contact their caring specialist. patient levels, in the event of acute outpatients’ service Objective questionnaires administered on-line may help rationing aimed at mitigating virus spread, patients’ deal with patients who poorly perceive their symptoms. access to allergy services has to be rationalized [8, 9]. A We specify that some of these clinical interventions and gradual escalation in acute service reduction would be ascertainments may be provided by health providers col- preferable but might not be applicable in case of tumul- laborating with allergists in multidisciplinary teams, such tuous spread of the virus. Similarly, “phase 2” re-opening as specialized nurses, dietitians, ENT physicians and policies should be based on gradualism and prudence. To psychologists. Malipiero et al. Clin Transl Allergy (2020) 10:23 Page 4 of 9 It should be noted that virtual care has to be delivered by the local Pharmacy [9]. This can prove a fruitful according to national laws and by licensed providers. This advantage of SLIT over subcutaneous immunotherapy could represent a problem where laws governing virtual (SCIT), in keeping patients adherent to AIT; transition care are not available or not up-to-date to ever modern- from SCIT to SLIT might be considered as a possible izing tools. Standardized digital platforms should be pro- management strategy during COVID-19 pandemic. SCIT vided to patients and health-care providers, accessible for hymenoptera venom allergy should be continued through a digital identity, in order to avoid misconducts although increasing administration interval can be con- and retain information in case of legal allegations [12]. sidered during long-term maintenance. In confirmed or Meantime, other more common and widespread tools suspected COVID-19 patients, AIT should not be started might be used, provided a properly informed consent to and should be temporarily interrupted if already pre- being treated via telemedicine has been obtained from scribed. AIT-specific recommendations are summarized the patient, when admitted by national laws on general in Table 1 [15]. data protection. First line anti-allergy agents, such as anti-histamines Diagnostic work-up can be postponed in the great and low-dose steroids, are not likely to affect immu - majority of allergic diseases, provided affected patients nocompetence and should not be discontinued during are well instructed about avoidance of potential environ- the pandemic (for disease specific recommendations, mental triggers and treatment of acute events, also based see  “Disease-specific management ” section), provided on written action plans [13, 14]. Anyway, diagnostic pro- systemic corticosteroid posology remains under the cedures should be reconsidered as soon as pandemic immunosuppressive threshold [16–18] and that all strat- becomes more controlled and confinement de-escalation egies to reduce systemic corticosteroid use should be begins. applied independently from the pandemic [19]. Notably, Therapeutic management deserves particular attention. regular steroid-based regimens, including inhaled and Whenever possible, therapeutic maneuvers not requiring oral corticosteroids, should not be stopped, since abrupt hospital access should be domiciled. interruption would bring along an increased risk of adre- In SARS-Cov-2 negative, low-risk individuals, allergen nal insufficiency in case of acute stressing events, as immunotherapy (AIT) should not be stopped and actu- COVID-19 is [20]. Conversely, a pulsed dose of steroids ally can be started in naive patients provided the required could result in a protective effect in such a circumstance infrastructure is in place during the pandemic [15]. We [21]. underline that sublingual immunotherapy (SLIT) for air- Second-line steroid sparing immunomodulat- borne allergens allows not suspending AIT and can be a ing agents are potentially detrimental on immunity valid and safe alternative for patients about to undergo although clear-cut distinctions exist between nonspe- SCIT, as far as a drug home-delivering service is activated cific immunosuppressive drugs, like cyclosporine and Table 1 AIT recommendations (adapted from Klimek et al. 2020), [19] Recommendations in non COVID-19 individuals Interrupting subcutaneous immunotherapy is not advised. Especially in potentially life-threatening allergies, such as venom allergy, SCIT should be regularly continued. The possibility of expanding injection intervals in the continuation phase should be checked and may be beneficial Interrupting sublingual immunotherapy is not advised. Supply the patient with sufficient medication for a minimum of 14 days isolation Sublingual immunotherapy can be taken at home. The intake of SLIT by the patient at home or any place is advantageous in avoiding contact with potentially infected persons Both subcutaneous and sublingual immunotherapy can be continued in the current COVID-19 pandemics, in any asymptomatic patient without suspi- cion for SARS-CoV-2 infection and/or contact with SARS-CoV-2 positive individuals, in any patient with negative test result (RT-PCR) or in any patient after an adequate quarantine or with detection of serum IgG to SARS-CoV-2 without virus-specific IgM Preparedness of your Allergy clinic is imperative to cope with COVID-19. Follow World Health Organization ( WHO) guidelines and advice staff accord- ingly These recommendations are conditional since there is paucity of data and they should be revised regularly with incoming new information on COVID- Recommendations in COVID-19 diagnosed cases or suspicion for SARS-CoV-2 infection Interrupting subcutaneous immunotherapy is advised Interrupting sublingual immunotherapy is advised Both subcutaneous and sublingual immunotherapy should be discontinued in symptomatic patients with exposure or contact with SARS-CoV-2 posi- tive individuals, or patients with positive test results (RT-PCR) M alipiero et al. Clin Transl Allergy (2020) 10:23 Page 5 of 9 azathioprine, and biological agents targeting discrete questionnaires and monitor domiciliary drug self- molecular pathways associated with type 2 allergic administration [9]. inflammation. In fact, besides inducing nonspecific Disease-specific measures and therapeutic recommen - suppression of anti-infective immunity, nonbiological dations are rapidly provided in the following sections agents are strong inducers of hepatic cytochromes, thus and graphically resumed in Fig.  2. In the case of atopic requiring plasma level monitoring when used in com- multimorbidity, priority should be given to uncontrolled/ bination with antimicrobial agents [22]. According to severe components over well-controlled/mild ones. a WAO paper [23], no definitive evidence is presently available to obligate clinical decision making. As anti- Disease‑specific management IgE, ant-IL5/IL5R and anti IL4/IL3R biologics are not Asthma likely to induce immunosuppression or interfere with Asthma-specific recommendations from Global Initiative virus clearance (actually the contrary seems to hold for Asthma (GINA) are reported in Table 2 [30]. Data are true, at least for omalizumab [24] and dupilumab [25], controversial regarding the interaction between asthma while mepolizumab treatment was not associated with and COVID-19 as European and Chinese data suggest a worse immunological response to viruses [26, 27]), lower risk for asthmatic patients to contract the infection they can be safely continued. Anyway, until evidence- [31] while U.S. data suggest the opposite [32]. Probably based data are available, some countries, like the UK, this association is modulated by the severity of asthma, have advised home confinement for at least 12  weeks age class, and levels of indoor and outdoor, allergen and to patients with severe asthma on systemic immuno- pollution exposures. With knowledge evolving, GINA suppressants or biological therapy. Steroid-sparing and the British National Institute for Health and Care effect of biologics is a potential advantage over steroid Excellence (NICE) guidelines recommend not stopping therapy since patients on chronic steroid therapy can the regular treatment regimen, including inhaled and oral be affected by subclinical adrenal insufficiency [20]. corticosteroids [30, 33], since abrupt interruption would Depending on the specific monoclonal antibody, in-site bring along an increased risk of acute/severe exacerba- administration or home-delivery and self-administra- tions or adrenal insufficiency [21]. Every patient should tion can be the preferred choice. When patients live be provided with a detailed and convenient action plan to far away from the Centre, National Networks can be deal with potential loss of control [13], and invited to reg- activated in order to identify a local near-home Centre ularly use mobile health technology apps to self-monitor for in-site administration (in Italy the Severe Asthma symptoms of their asthma [7]. Aerosol generating proce- Network in Italy (SANI) [28, 29]). In case of infection, dures are discouraged unless essential and lung function discontinuation should be discussed on a case-by-case testing should be postponed whenever possible [30]. basis. We should also consider the complexity of allergic Allergic rhino-conjunctivitis patients and the synchronous atopic involvement of Allergic rhino-conjunctivitis-specific recommendations multiple organs that interface with the environment’. from allergic rhinitis and its impact on asthma (ARIA) Therefore, as far as precision medicines targeting nodal and European Academy of Allergy and Clinical Immu- pathogenic pathways allow to treat “atopy” as a whole, nology (EAACI) are reported in Table 3 [15, 34]. Allergic we claim priority and lower prescription threshold rhinitis visits should not be prioritized and can be safely could be assigned to biologicals, given the good safety postponed unless exceptional circumstances supervene. profile, the lack of interference with drug metabolism Intranasal steroids do not induce immunosuppression and the favorable effect on treatment adherence. The and are not to discontinue [34]. As stated above, optimal regulatory agencies should address these new needs in disease control is mandatory as sneezing in asympto- pandemic times and coordinate with health care pur- matically infected patients can contribute to viral spread; chasers to make biological more accessible. mobile applications can contribute in improving optimal Clinical research has been seriously threatened by self-management of rhinitis [7]. For AIT-specific recom - COVID-19 epidemics. New recruitments in ongoing mendations, see Table 1 [15]. clinical trials have been temporarily suspended. Inves- tigators can consult with sponsors in order to reas- Chronic rhinosinusitis sess follow-up visit schedules and amend protocol We are unaware of specific recommendations from requirements to facilitate online visits. When accorded medical societies about this topic. For reasons analo- with the Sponsor and local Pharmacy, investigational gous to those specified for allergic rhino-conjunctivitis, product home-delivery service and a digital medi- it is commonsense to keep patients on regular treat- cine service can be activated to administer scheduled ments. Patients with uncontrolled disease or waiting for Malipiero et al. Clin Transl Allergy (2020) 10:23 Page 6 of 9 Fig. 2 An integrated model of tele- and digital-allergy clinic during COVID-19 pandemic. Suggested actions to be implemented in order to re-organize an allergy clinic are reported in boxes for asthma, rhino-conjunctivitis, atopic dermatitis and food allergy, anaphylaxis, drug and venom hypersensitivity and CSU. The truck represents the home-delivery service that should be activated for biologicals, AIT and self-injectable adrenaline Table 2 Asthma‑specific recommendations from Global Initiative for Asthma (GINA) as reported on GINA website [34] People with asthma should continue all of their inhaled medication, including inhaled corticosteroids, as prescribed by their doctor In acute asthma attacks patients should take a short course of oral corticosteroids if instructed in their asthma action plan or by their healthcare pro- vider, to prevent serious consequences In rare cases, patients with severe asthma might require long-term treatment with oral corticosteroids (OCS) on top of their inhaled medication(s). This treatment should be continued at the lowest possible dose in these patients at risk of severe attacks/exacerbations. Biologic therapies should be used in severe asthma patients who qualify for them, in order to limit the need for OCS as much as possible Nebulizers should, where possible, be avoided for acute attacks due to the increased risk of disseminating COVID-19 (to other patients AND to physi- cians, nurses and other personnel) Pressurized metered dose inhaler (pMDI) via a spacer is the preferred treatment during severe attacks. (Spacers must not be shared at home) While a patient is being treated for a severe attack, their maintenance inhaled asthma treatment should be continued (at home AND in the hospital) Patients with allergic rhinitis should continue to take their nasal corticosteroids, as prescribed by their clinician Routine spirometry testing should be suspended to reduce the risk of viral transmission, and if absolutely necessary, adequate infection control meas- ures should be taken Table 3 Allergic rhino‑ conjunctivitis‑specific recommendations from ARIA/EAACI (from: Bousquet et al. 2020) [37] With the current knowledge, in patients with COVID-19 infection, intra-nasal corticosteroid (including spray) can be continued in allergic rhinitis at the recommended dose Stopping local intra-nasal corticosteroid is not advised. Suppression of the immune system has not been proven and more sneezing after stopping means more spreading of the Coronavirus These recommendations are conditional since there is a paucity of data and they should be revised regularly with new knowledge M alipiero et al. Clin Transl Allergy (2020) 10:23 Page 7 of 9 Ear-Nose-Throat (ENT) surgery could be transitioned to chronic spontaneous urticaria), in whom shift to a bio- biological treatment whenever possible. logical agent with a more favorable safety profile might be considered on a case-by-case basis (e.g. close contact with infected individuals, active infection) [40]. For new Atopic dermatitis and food allergy evaluations, diagnostic procedures should be postponed Disseminated skin viral infections are a major compli- during the epidemics peak and reconsidered on a sec- cation of severe/uncontrolled atopic dermatitis. It is ond time, unless urgently needed (e.g. severe reactions unknown whether increased risk of SARS-Cov-2 infec- to Hymenoptera venom). We highlight that urticaria can tion or disease severity is associated with atopic der- be a presenting sign of COVID-19 and allergy to drugs matitis due to impaired cutaneous barrier. Patients on used to treat COVID-19 can present with rashes that may immunosuppressive therapy for severe atopic dermati- involve the allergist’s evaluation [4]. tis should be strictly monitored or transitioned to safer anti-IL4/IL13 immune-modulatory agents, as advocated by the European Task Force on atopic dermatitis [35, 36]. Conclusion Safe use of Dupilumab in severe AD patients affected We are now in the middle of the storm and we do not by COVID-19 has been recently reported [37]. Food know how long it will last or whether additional con- allergy and allergic gastrointestinal diseases are preva- sequences are on the horizon. In these times of sus- lent comorbidities in atopic dermatitis, especially in chil- pense, we have the responsibility of balancing individual dren; careful evaluation is needed and food challenge patients’ needs with public health issues. To our mind, a should be performed to prevent unnecessary food avoid- black-and-white thinking does not suit a scientific way ance interfering with growth and micronutrients bal- of addressing theoretical and practical problems. We ance [38]. Food allergy in asthma is of particular concern therefore advocate for a risk-stratified approach aimed since it has been associated with fatal asthma. Asthmatic at conjugating COVID-19 and non-COVID-19 health patients with food allergies may need to be provided with care needs of allergic patients. We have to reshape our epinephrine auto injectors (see the following section on practice and optimize those innovative tools that help anaphylaxis management) and should avoid introducing us reduce the risk of viral spreading while delivering up- new foods in their diets during the pandemic as long as to-date personalized care. A new era of integrated preci- the risk of contagion is high [38]. sion-digital medicine is knocking at the door. Anaphylaxis A modified anaphylaxis management algorithm dur - Abbreviations ing COVID-19 pandemic has been proposed by Casale ACE-2: Angiotensin-converting enzyme-2; AIT: Allergen immunotherapy; ARDS: Acute respiratory distress syndrome; ARIA: Allergic rhinitis and its et  al. [39]. Patients are invited to carry two epinephrine impact on asthma; COVID-19: Coronavirus-Disease 2019; CRSwNP: Chronic injectors and to activate emergency services only when rhinosinusitis with nasal polyps; DMS: Digital medicine service; EAACI: Euro- a second administration of epinephrine fails to control pean Academy of Allergy and Clinical Immunology; ENT: Ear-Nose-Throat; GINA: Global initiative for asthma; NICE: National Institute for Health and Care symptoms. It might be prudent to proactively discuss Excellence; OCS: Oral corticosteroids; pMDI: Pressurized metered dose inhaler; the modified management of anaphylaxis, if feasible, e.g., SANI: Severe Asthma Network in Italy; SARS-CoV-2: Severe Acute Respiratory via telemedicine. Home delivery service of self-injectable Syndrome-Coronavirus-2; SCIT: Subcutaneous immunotherapy; SLIT: Sublin- gual immunotherapy; TLR: Toll-like receptor; WHO: World Health Organization. adrenaline should be implemented, provided the patient has been instructed on the underlying disease, triggers Acknowledgements avoidance measures and proper use. Not applicable. Author’s contributions Drug allergy, hymenoptera venom allergy and urticaria/ GM, GP, EH and GWC contributed in conception and drafting the review article; CP, FP, FR, SF, LS, DL, GC, MM, MS: contributed in critically interpret and angioedema revise the article. All authors read and approved the final manuscript. Expert recommendations and consensus on these top- ics during COVID-19 epidemics are missing at the time Funding No funds for this review article. of this manuscript being written. As a general princi- ple, we maintain that ongoing treatment for these con- Availability of data and materials ditions should not to be discontinued in order to keep Not applicable. disease under control as far as these treatments are not Ethics approval and consent to participate likely to increase the risk of SARS-Cov-2 infection or Not applicable. complicate COVID-19 course in case of infection. A Consent for publication possible exception might be represented by patients Requested (pending) (for reproducing Tables 1 and 3). on immunosuppressive regimens (e.g. cyclosporine for Malipiero et al. Clin Transl Allergy (2020) 10:23 Page 8 of 9 Competing interests 12. Portnoy J, Waller M, Elliott T. Telemedicine in the Era of COVID- Enrico Heffler reports personal fees from AstraZeneca, Sanofi, Novartis, Teva, 19. J Allergy Clin Immunol Pract. 2020. https ://doi.org/10.1016/j. GSK, Circassia, Boehringer Ingelheim, Valeas, Nestlè Purina, outside the submit- jaip.2020.03.008. ted work. 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Clinical and Translational Allergy – Springer Journals

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