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14th December 2020
As of 10 May 2020, there were reports of over 4 million cases of SARS-coronavirus-2 disease (COVID-19) worldwide with 218,000 cases diagnosed in Italy, one of the most affected countries especially in the first three months of the pandemics.1 Cases of pneumonia of unknown origin were first reported from the Hubei Province in China and later defined COVID-19 in association with the infection by SARS-coronavirus-2. Approximately 20% of cases develop severe respiratory symptoms and may require invasive or non-invasive ventilatory support with variable mortality rates.
Two hospitals from the Humanitas Group that we represent (that is, Humanitas Clinical and Reseach Hospital and Cliniche Humanitas Gavazzeni) are located in two of the highest-impact cities (Rozzano and Bergamo, respectively) in Northern Italy and were designed with a strong surgical vocation. While both organisations were significantly affected by the pandemics, the Humanitas Clinical and Research Hospital is the larger Institution and had to develop organisational changes rapidly. By 8 March 2020, all non-emergency admissions and outpatient visits were suspended. In fact, between 1 March and 17 May 2020, a total of 736 COVID-19 patients were admitted to the Humanitas Clinical and Research Hospital; of these, 482 were dismissed and 165 patients died, mostly due to respiratory failure.
The treatments proposed for COVID-19 remain merely supportive as the main cause of death is in fact a severe acute respiratory distress syndrome2 with biochemical features resembling acute inflammation, including a progressive increase in C-reactive protein, ferritin, interleukin-6, and D-dimer.3 Based on the viral aetiology and the hyperinflammatory state, proposed agents to treat COVID-19 have included immunosuppressants such as glucocorticoids,4 anakinra,5,6 and baricitinib,7 immune modulators such as hydroxychloroquine,8 and direct antivirals,9 cumulatively with unconclusive results. Our effort in treating a large number of patients in Bergamo and Rozzano is mirrored by one of the earliest and largest studies on the use of tocilizumab, a monoclonal antibody targeting the interleukin-6 receptor, to treat inflammation in COVID-19.10 In an ancillary study, we addressed the issue of predicting the response to tocilizumab in patients with COVID-19 and utilised, for the first time, a supervised machine learning approach of artificial intelligence and we are currently validating our observations (unpublished data).
Among clinical specialties, rheumatology has been at the epicentre of COVID-19 since the earliest phases due to five pivotal observations, spanning from insights into the disease pathogenesis to organisational opportunities. These observations, indeed, well represent the challenges provided by the new condition and our responses may suggest new ways to address these challenges in other areas.
First, our understanding of the pathogenesis and treatment of rheumatic diseases has been central to understand the uncontrolled amount of literature on COVID-19. In late April 2020, it was estimated that the COVID-19 literature had grown to more than 31,000 papers since January, the biggest explosions of scientific literature ever.11 We have discussed that SARS-Cov-2 triggers a vigorous inflammatory response, as represented by the high levels of interleukin-6, especially in older subjects, and this is similar to what observed in the chronic inflammation associated with rheumatological conditions, particularly rheumatoid arthritis.12 Nearly all anti-rheumatic drugs, that is, tocilizumab, glucocorticoids, anakinra, and hydroxychloroquine, among others, have been proposed to treat COVID-19. It has been hypothesised that patients with rheumatic diseases who were already receiving these medications might be at either higher or lower risk of developing a severe infection, based on the apparent opposing factors of the ongoing immunosuppression versus a potential protective effect of the drugs.
The second issue is that patients with immune-mediated chronic diseases, including rheumatic conditions such as arthritis (that is, rheumatoid or psoriatic arthritis, ankylosing spondilitis) or connective tissue diseases (that is, systemic lupus erythematosus, Sjogren syndrome, systemic sclerosis, and myositis) had to be considered as fragile individuals that had to be strongly advised to avoid being infected by SARS-Cov-2. To address these two questions, we analysed the data from the Humanitas Immuno Center, which coordinates the clinical and research activities of gastroenterologists dedicated to inflammatory bowel diseases, dermatologists dedicated to psoriasis and atopic dermatitis, allergologists, and rheumatologists. Out of approximately 10,000 patients being followed for such immune-mediated inflammatory diseases, we identified only 41 patients who had COVID-19 infection and evaluated the factors associated with a more severe respiratory impairment or death. Our data showed that comorbidities, particularly hypertension, diabetes, obesity and chronic lung disease, were the factors increasing the risk of hospitalization and the need of oxygen supplementation while supporting using extra caution when patients were receiving glucocorticoids. Our most important conclusion, however, was that an ongoing biologic therapy is not associated with a worse pattern of COVID-19 infection,13 as also confirmed in other Italian cohorts.14
The third issue is that rheumatic diseases are largely viewed as non-emergency conditions and this has led to the cancellation of nearly all the scheduled outpatient appointments during the COVID-19 pandemics. In the case of the Humanitas Clinical and Research Hospital, a total of 544 rheumatological outpatient visits took place between 1 March and 17 May 2020, compared with 2759 performed in the same period of 2019, with an 80% decrease. At the same time, six out of nine physicians from the Division of Rheumatology were dedicated full time to attending inpatients, particularly within the COVID-19 wards, and coordinating the investigational use of anti-rheumatic drugs. Starting 17 May 2020, we could re-open non-emergency services and 1100 patient visits were rescheduled between 1 June and 1 September, 2020. The rescheduling had to consider the new rules of outpatient physical presence in the hospital (which limited the efflux to the premises and thus required a longer time allocated for each visit) as well as the previously scheduled appointments, thus requiring a dedicated task by our Operations division.
Fourth, there was the need to reach out to patients with rheumatic diseases to address their numerous questions regarding the need to continue or withdraw chronic treatments or the possible shortage of the anti-rheumatic treatments that were in use for COVID-19. Since the earliest phases of the pandemics, we received a growing number of inquiries by patients from our Division or being followed at other hospitals, especially asking whether they could continue taking their rheumatological medications or should withdraw. The Italian Society of Rheumatology was one of the first National societies to provide a clear guidance against stopping medications, based on the assumption that an inflammatory flare would have been characterized by the need for strong immunosuppression and thus a higher risk from COVID-19 infection.15 Together with four other academic Rheumatology Centres in the Lombardy region, we signed a letter to all patients which was disseminated by the local patient support organisation (ALOMAR) to prevent patients from stopping their treatments in the absence of signs of COVID-19. The Italian recommendations were then followed by the same messages provided by the American College of Rheumatology and the European League Against Rheumatism (EULAR). At a local level, a dedicated telephone line was activated to answer the patients questions and an average of 20 calls was received daily. The Divisional email address also continued to be accessible for patients to send inquiries and all messages were answered within the same day. Of note, we became aware of a very small number of cases in which patients could not find their usual medications due to a COVID-19-related shortage, which could be expected due to the widespread use of hydroxychloroquine for example to treat or prevent the infection, an assumption that was not supported by experimental data. The hospital pharmacy was proactive at contacting patients receiving biologics to provide the home delivery of refills.
Fifth, and last, considering the chronic nature of rheumatic diseases and the often non-invasive evaluations, rheumatology might be an ideal playing field to experiment the potential of teleconsultations. While physical examination remains crucial to the rheumatology practice, the natural history of chronic inflammatory diseases includes phases of activity (flares) alternating with phases of remission or low disease activity. In the former case, the therapeutic target is not reached and a tight control of patients, with frequent visits requiring physical examination, is recommended. However, if the patient condition is under acceptable control (very low or minimal disease activity or remission) visits can be scheduled with lower frequency. In these cases, teleconsultations represent an ideal option to minimise the risk related to hospital visits and reduce the inconvenience of long commuting, particularly for patients living in other regions throughout Italy. During the COVID-19 pandemics, one rheumatologist from our group started teleconsultations one day a week with very encouraging, yet preliminary, results. We envision that an integrated approach using telemonitoring of disease activity through a dedicated app that is being developed for our patients and the possibility of teleconsultation would be an ideal method to select the patients eligible for this new tool. The availability of such monitoring app would be also central to a more accurate real-time monitoring of infectious events, including COVID-19, in patients with chronic diseases.
The COVID-19 pandemic hit our hospitals very hard and affected the practice of medicine and rheumatology significantly. As we were all involved at different levels in the care of patients with COVID-19 without abandoning patients with chronic diseases, we learned several lessons that will impact our future practice:
Carlo Selmi MD PhD
Humanitas Clinical and Research Center IRCCS, Rozzano, Milan
Humanitas University, Department of Biomedical Sciences,
Pieve Emanuele, Milan
Marco Albini
Humanitas Clinical and Research Center IRCCS, Rozzano, Milan
Luciano Ravera
Humanitas Clinical and Research Center IRCCS, Rozzano, Milan
According to Dr Mankia, a significant amount of a rheumatologist’s clinical workload is undertaken in an outpatient setting where there is often a high turnover of patients. Prior to the pandemic, the department held large clinics, which typically included up to 40 patients who were seen every 15 or 20 minutes, with all of them seated in close proximity. As a consequence of the pandemic, all this changed, literally overnight, with routine face-to-face consultations suspended and moved to being largely undertaken remotely over the telephone. A further effect of the pandemic that had an important impact on the running of the service was how many of the clinical staff were re-deployed and Dr Mankia himself was tasked with working as a consultant on a general medical ward for a couple of weeks.
However, although the vast majority of consultations were undertaken remotely, it was still possible for urgent cases to be seen in the clinic.
Nevertheless, an interesting phenomenon observed by Dr Mankia was the existence of a fear factor among patients, that occurred across all specialties and even led to lower attendance at Accident and Emergency departments. People were simply concerned about catching the virus and, in many cases, newly referred patients were happy to effectively ‘sit it out’ and receive telephone advice from a clinician, rather than visiting the department. However, this has led to increased pressure on certain services. For example, there has been a surge in calls to the rheumatology advice telephone line; this service, usually managed by clinical nurse specialists, has required significant additional support from consultants and other doctors.
Fortunately over the last few months, services have gradually re-opened and Dr Mankia felt that the department has reached a new equilibrium, whereby the stable patients, who under normal circumstances would be asked to attend the department for a review appointment, are instead being managed remotely. With protective measures in place in the rheumatology department, confidence has begun to return and more patients are being seen at the department although several precautionary measures are in place. For instance, those with an appointment are contacted a few days prior to their appointment and asked whether they have any COVID-19 symptoms and are required to wear face masks at the department and seen by clinical staff in full personal protective equipment (PPE). The rheumatology department is therefore divided into areas where phone consultations take place and designated rooms in which patients can have face-to-face consultations. A downside to this approach is that fewer patients can be seen and appointment times have been extended, due to the need for thorough cleaning of the consultation rooms between each patient and to give time to clinicians to change their PPE.
While initially most consultations were conducted via phone, some video consultations were undertaken by some staff either in clinic rooms at the department or even from home. This was particularly useful for members of staff, who for various medical reasons, were themselves required to shield. Video conferencing also became the new platform for multi-disciplinary team (MDT) meetings, case reviews and educational meetings.
At the start of the pandemic, Dr Mankia explained how the Leeds Teaching Hospitals NHS Trust developed PPE guidance for clinical staff although specific guidance for patients has evolved over time. Initially, the British Society for Rheumatology (BSR) produced guidance for members, as many patients with rheumatological conditions were prescribed immunosuppressant therapy and were thus presumed to be at high risk from the virus. The consultant body at Leeds developed an algorithm adapted from a risk stratification document originally produced by the BSR and the algorithm is now available on the Leeds Teaching Hospital Rheumatology website. This allows patients to check for themselves as to whether they should be shielding or socially distancing based on their individual circumstances. Interestingly, Dr Mankia noted that the Trust’s guidance has been used by other hospitals and can even be seen on YouTube, although Leeds has been cited as the original source.
While initially most consultations were conducted via phone, some video consultations were undertaken by some staff either in clinic rooms at the department or even from home. This was particularly useful for members of staff, who for various medical reasons, were themselves required to shield. Video conferencing also became the new platform for multi-disciplinary team (MDT) meetings, case reviews and educational meetings.
The pandemic forced a re-think in many areas of medicine and, as Dr Mankia explained, there was an urgent need to triage patients and ensure those with the most urgent cases could access services in a timely manner. For a speciality such as rheumatology, it was case of adapting to achieve a balance that you think will work. For example, some rheumatology care has been delivered remotely provided that staff have access to information such as blood test results. Moreover, the chronic nature of many rheumatological conditions mean that talking to the patient about their symptoms, and any possible treatment-related side-effects, is an extremely useful part of the assessment process. Nevertheless, remote consulting is not perfect and there will be plenty of instances where a patient is having problems or experiencing a disease flare which requires that they are seen and examined due to the obvious difficulty of remotely assessing the extent of joint inflammation.
Perhaps the most important thing is that the departmental team have all worked together and managed to adapt and transform a service that had been established over many years in response to the pandemic. Dr Mankia also believes that the pandemic has highlighted to staff that remote consultations could work for stable patients and that even if the pandemic were to disappear tomorrow, it is possible that remote consultations, for some patients, would remain. However, the long-term implications of such changes on patient care would need to be considered carefully.
One of the more challenging aspects of the pandemic, which has required a lot of thought, has been the modification of practical services such as ultrasound and joint injection clinics. The ultrasound service requires staff to be in close contact with patients for three to four hours per session and was thought to be one of the higher-risk practices in rheumatology. Factors that needed to be considered ranged from the size of the room in which the ultrasound scanner was housed, current levels of ventilation, the need for before and after cleaning of equipment, even down to where patients would have to sit and wait before their scan. While it was relatively straightforward to simply move the ultrasound scanner to another room with sufficient ventilation, appointment times have had to be extended to allow for cleaning between patients. A further difficulty created for clinicians and patients was that immediate ‘ad hoc’ scans were no longer possible. Whereas in the past, if a clinician felt that a patient needed a scan, this could happen after their consultation; now, all of these requests have to be planned and the department has had to create a new standard operating procedure for the ultrasound service.
Though there has been a clear impact on the number of scans than can be performed at any one time, a further difficulty highlighted by the pandemic has been how staff receive training on use of the ultrasound scanner. Ultrasound training, by its very nature, requires a ‘hands-on’ approach that invariably involves a degree of closeness with a trainer as the trainee needs to be able to read a scan on the screen to interpret the data and has to become familiar with how to operate the machine. During the pandemic, such practical training was no longer possible and is in the process of being re-designed to include a significant amount of online teaching including demonstration videos.
Rheumatology departments also provide joint injection clinics for patients and these have also reduced, although as Dr Mankia found, early in the pandemic, many patients were initially reluctant to visit the hospital and made the decision to try and manage for longer periods of time between injections. Again, this procedure has required a lot of thought because it involves close contact with patients.
Dr Mankia says how navigation through the department has changed radically because of the pandemic and is carefully structured with patients only brought in if they have a specific appointment and that relatives are no longer allowed in the same area. Patients are seated outside the specific room for their appointment and then leave the department. Overall, he feels that face-to-face consultations have reduced considerably and in fact currently, even new referrals are initially contacted by telephone to discuss their symptoms. With access to the GP records, relevant blood tests and the patient history, Dr Mankia felt that a diagnosis can sometimes by made armed with these facts. However, in many cases a physical examination is required and the patient will need to be seen in person.
One of the key learnings from the pandemic has been that the conventional model in which every patient consultation had to be face-to-face may be adapted and clinicians are now very much in tune with new ways of managing patients. Furthermore, there are possible benefits for those patients who are stable and for whom regular blood tests and monitoring are performed, in that they might no longer need to travel to the hospital for some routine appointments.
Dr Mankia thought that many of the changes implemented as a consequence of the pandemic could remain in place and that it was not really a question of regaining momentum to go fully back to the old way of working. It was highly probable that the department would continue with some virtual MDT meetings and, as he pointed out, interestingly, more people can attend these compared with the original face-to-face meetings. Both case discussions and academic educational meetings have been successfully delivered via a virtual platform and a proportion of these may continue to be done remotely. He thinks the pandemic has forced the pace of change, not just in rheumatology but in different specialties, as witnessed from discussion with consultant colleagues. Out of necessity, most colleagues in other clinical areas appear to have embraced the new mode of working and patients seem to be adapting to this as well.
Kulveer Mankia BMBCh MA (Oxon) DM MRCP PGDip Health Res
Leeds Teaching Hospitals NHS Trust, UK
At the beginning of full lockdown (23 March 2020 in the UK), elective imaging services virtually ceased overnight. Referrals from primary care were hugely reduced. There was a significant reduction in elective referrals from secondary care. Emergency referrals reduced drastically to those either with COVID-19 or those with immediate life-threatening emergencies, especially in surgery.
An unexpected bonus of this was that imaging backlogs were rapidly demolished. The imaging service functioned for the full benefit of patient care with reporting in real time aiding patient discharge and flow through secondary care. Changes in acute service delivery meant a more effective dialogue between senior clinicians with targeting imaging to the problem to be answered rather than the quickest imaging test available. This improved patient experience in that fewer, more relevant tests were done, to enable the patient to move forward on their pathway.
Infection prevention and control (IPC) measures in the form of personal protective equipment (PPE) and social distancing as well as deep cleaning of COVID exposed equipment significantly reduced the capacity and throughput of imaging across all modalities. In some geographies, where excess staff time was available due to reduced throughput, imaging staff were redeployed to medical wards to support acute COVID activity. In other geographies staff sickness rates and the requirement for shielding further reduced patient throughput.
In the UK, the aerosol-generating nature of anaesthesia coupled with perceived poor outcomes for those patients developing COVID post-operatively, resulted in a shift of care from surgery to interventional radiology (IR). This was most marked in those hospitals with dedicated IR beds and/or day case facilities. This improved patient outcomes and experience with a reduced risk of nosocomial exposure to COVID.
With anaesthetic and intensivist time being taken up dealing with patients in intensive care (ITU), IR also provided an invaluable resource to assist in central venous line placement and effusion aspiration for the sickest of our patients. They also trained juniors from other disciplines in these procedural skills.
The main protection for patients and clinicians was the introduction of enhanced IPC measures, including social distancing and the use of PPE. Guidance on PPE was at times difficult to tease out for different clinical areas and presence of aerosol generating procedures (AGPs). Many medical special interest groups developed their own guidance, sometimes at odds with Public Health England (PHE) – government – guidance, leading to further confusion. Anecdotally, some hospitals did not feel that the imaging service was sufficiently patient facing to require PPE, which led to higher levels of infection amongst imaging staff than would have been expected, especially those in image acquisition. This was addressed in updated PPE guidance issued during the pandemic. Shortages of PPE were widely reported at the start of the pandemic but, for the health sector, were addressed at a reasonable pace, given global supply chain issues. The social care sector struggled throughout lockdown, but especially during the initial weeks, with PPE supplies.
Individualised risk assessments were introduced for staff groups including those who were pregnant, immunocompromised or had significant medical comorbidities. Generally, adjustments such as remote working were introduced for those high risk groups. The emerging understanding of the excess risk to Black, Asian and other minority ethnic (BAME) groups was wholly unexpected and required reconsideration of what being ‘at risk’ meant. Expansion of risk assessments with a further depletion of patient facing staff was necessary to protect those at highest risk.
Testing infrastructure and therefore capacity was poor initially and took a long time to reach levels able to assist positively with contact tracing and aiding restoration of elective services including imaging. To maintain ‘COVID-lite’ diagnostic spaces patients were requested to self-isolate for two weeks prior to having an imaging test (if possible) and undergo PCR swab testing 72 hours in advance of the test. Swab testing capacity is now at the required level. All NHS staff who wish to undergo antibody testing have been given the opportunity to do this.
Initially there was concern raised by surgical colleagues about poorer outcomes in patients operated on who were, or subsequently became COVID positive. The Royal College of Radiologists (RCR) in conjunction with the surgical colleges developed interim guidance on preoperative chest CT imaging in those with an acute abdominal presentation. We went on to audit the outcomes for patients treated under this protocol, determine that it did not alter clinical judgement or patient outcomes so withdrew the guidance at the earliest opportunity.
Expansion of home reporting allowed the workforce to socially distance more effectively, reducing risk of COVID transmission. It also allowed those shielding or self-isolating due to viral exposure to contribute to maintenance of the imaging service. Unfortunately, not all NHS staff had access to sufficiently high-quality home reporting equipment or hospitals had sufficient IT bandwith to support a massive increase in the number of remote workers. Home workers sometimes lacked sufficient IT bandwidth to report from home. Many hospitals invested in rapid deployment of equipment. Hospitals also invested in remote solutions for attendance at cancer multi-disciplinary team meetings (MDTs).
Training of junior colleagues has been hugely disrupted. Expanded access to home reporting for trainees has allowed vulnerable doctors to continue to support the service and gain the competencies to progress through their training. This challenge to our traditional model of training can be built upon to deliver high quality training throughout a region, reducing doctors’ time spent travelling. Improved IT connectivity is necessary to fully realise the benefits of this. Networked reporting solutions also help with making maximal use of available radiologist time to report, but need to be supported with high quality IT.
High fidelity simulation has allowed IR, as well as other practical procedural training, to continue with risk to patients, staff and trainees mitigated to the fullest extent.
Artificial intelligence solutions looking to spot classical characteristics of COVID on chest CT scans are being accelerated through NHSX, including the necessary image sharing protocols. A national chest imaging database has been set up, with input from the British Society of Thoracic Imaging (BSTI), hosted by NHSX, to allow training and validation of COVID related algorithms.
As with everywhere and everything else, the impact of COVID on imaging services has been massive. Time needs to pass for the full impact to be demonstrated. Improved access to home reporting coupled with better IT connectivity allow best use of limited radiologist time. Coupled with an acceptance of increasingly flexible working patterns, this should promote retention of the workforce, especially towards retirement age. With the current workforce shortage of at least 20%, the UK desperately needs to retain all competent radiologists within the workforce. All measures which assist this need to be supported by all employers as well as government.
New ways of working remotely, including providing training, have been rapidly adopted proving the flexibility and adaptability of the workforce.
The impact on patient care and outcomes from IR procedures has been demonstrated. The ability to treat patients under mild sedation, avoiding the risk of anaesthesia, with same day discharge have proven that investment in a sustainable IR workforce is both clinically and cost effective.
As with all aspects of life, turning off a service is much easier than turning it back on. The chronic under-investment and subsequent lack of capacity in UK imaging services has been revealed, especially in the relative slowness of service recovery.
In the UK, there has been a significant amount of discussion around how best to regain momentum. Nationally, this work has been titled “service restoration”. Restoration of imaging services is complex and multi-factorial covering issues related to baseline demand for imaging as well as the necessary “catch-up” of imaging requests paused during the pandemic.
Prior to the pandemic imaging services in the UK suffered from chronic underinvestment with a lack of capacity in both image acquisition and reporting. These were related to significant workforce, but also equipment shortages. Coupled with new IPC measures, especially social distancing of 2m in all healthcare settings, these shortages have meant current CT capacity at the time of writing is 40 – 70% of pre-COVID levels. MRI is slightly better at 80%. Prior to the pandemic, timely image reporting was a greater problem than image acquisition. Post-pandemic image acquisition is the main bottleneck in the imaging pathway. An investment in extra equipment would aid restoration but not without matched funding to support workforce expansion in both radiographer and radiology staff.
Patient attendances to primary care (the main route into diagnostic pathways) remain below the expected pre-pandemic level. The urgent suspected cancer referral pathway has recovered to 75% of expected in July (compared with 30% nadir in April), but there is still a cohort of patients who have worrying symptoms who are not utilising the health service as expected. The outcomes for patients, for cancer and other potentially life-threatening conditions such as cardiovascular disease, are likely to be negatively impacted for some time to come. There was a media campaign running to assure the public that NHS services are ‘open for business’ and to encourage those with worrying symptoms to seek healthcare advice.
At the end of July, the shielding restrictions on the most vulnerable patients – the elderly and those with significant underlying health problems – were lifted. These patients had been encouraged to stay at home since March, with allowance of outside exercise not being recommended until June. Some patients, especially the elderly and most clinically vulnerable, remain worried about attending hospital to undergo imaging tests. In the UK, the majority of imaging equipment is located in acute hospital settings. A media campaign on the safe practices adopted by imaging departments to ensure patient safety is also running in the UK at present.
The NHS has retained (at time of writing) extra independent (private) sector capacity in some areas of the country. This is enabling development of ‘COVID-lite’ or ‘COVID minimal’ hubs for diagnostic procedures, including imaging, endoscopy, and low risk elective surgery. In some hospitals, mobile CT scanners are being deployed to support on-site ‘COVID-lite’ areas, maximising image acquisition capacity.
Reduced capacity has shone a light on appropriateness of imaging investigations. This has become more, not less of a problem, as remote consultations for patients in both primary as well as secondary care become the accepted default position. The relative difficulty in examining (or in some cases just seeing) a patient has meant clinicians are anecdotally more likely to request imaging as a result of a consultation. RCR has, for many years, been encouraging the NHS to deploy iRefer, a web tool, which highlights the evidence base for requesting imaging. We have, with partners, launched a clinical decision support software version of iRefer, which is inter-operable with electronic imaging order comms, enabling best use of limited resources. The RCR have also supported the national Evidence Based Interventions programme looking at, amongst other procedures, which imaging tests were of no or limited clinical utility for various clinical presentations.
Prior to the pandemic, the NHS was looking at establishing rapid diagnostic centres (RDCs). The need for ‘COVID-lite’ diagnostic spaces to maximise available capacity has shifted this toward the development of Community Diagnostic Hubs. These require extra funding in terms of buildings and equipment as well as staffing but are an attractive solution to expand capacity in a way that maximises patient safety and confidence in the COVID endemic era.
Although imaging services are working hard to regain momentum by restoring capacity and regaining patient confidence, it remains clear that fundamental changes can only be made with significant investment to address the chronic underfunding in radiologists, radiographers, and imaging equipment.
Jeanette Dickson MB ChB MRCP(UK) FRCR MSc MD
Mount Vernon Cancer Centre, UK; President, Royal College of Radiologists, UK
In late 2020, less than a year after reports of a new virus first emerged from China, we are only just beginning to appreciate the potential impact of the COVID pandemic on healthcare in general, and on emergency care in particular. This view offers one perspective on our journey so far.
As information started flowing about the potential impact of COVID on emergency care, our initial preparations focused on:
Initial thinking centred on what seemed likely to be an overwhelming surge of patients requiring hospitalisation, intensive care and/or ventilation.
For EDs, the focus was on protecting staff and patients and generating additional capacity, while maintaining core business. This primarily involved the adoption of more stringent IPC measures, and separation of flows so that patients deemed at higher risk of COVID were managed in cohorted areas or were treated in rooms deemed more suitable for aerosol-generating procedures (cubicles). In many departments, there was rapid adaptation of existing facilities, or co-located areas were subsumed into the ED footprint to help generate floorspace. In some departments, minor injuries and illness were moved off-site. Additionally, there was widespread development of ambulatory treatment or ‘streaming’ pathways designed to avoid admission. There was improved access to specialist teams, whose availability was in turn enhanced as a result of service reconfiguration and changes to working patterns.
There was considerable attention to generation of ICU capacity within hospitals, with early models suggesting the need for substantially increased numbers of ventilated beds. Additionally, much elective surgery was cancelled nationally to free up inpatient beds, and there was extensive redeployment of clinical teams to acute areas. These included the ED, ICU and inpatient medical floors. Arrangements to improve discharge of ‘medically fit’ patients from hospitals were introduced, designed to reduced ‘delayed transfers of care.’ In England seven ‘Nightingale’ Hospitals were developed, mostly in convention centres, with an additional three hospitals in each of Wales, Scotland and Northern Ireland. These were intended to provide additional critical care capacity.
Underpinning the creation of additional capacity was a massive effort to increase the available workforce. This not only included redeployment, but also the early awarding of medical qualifications to final year medical students, deployment of nursing students to wards, and a call for volunteers from retired staff. There was extensive reorganisation of rotas with cancellation or postponement of what was deemed non-essential work. Regulators produced guidance designed to offer regulatory and legal protection for staff working outside of their normal scope. Planned rotations of medical trainees to different specialities, due in April for the final four months of the training year (August to August) were postponed so that staff were working in areas already familiar to them. Lockdown also resulted in the cancellation of most educational events and exams. This will of course require some unpicking down the line and regulators are working together with training bodies to do this.
Within the wider system there was attention to demand management strategies. Existing prehospital telephone services were developed as a source of enhanced remote clinical advice, with additional clinical support brought on-line. There was also a drive to introduce improved access to alternatives to hospital admission, such as ambulatory care (known as Same Day Emergency Care). Ambulance services focused heavily on prioritisation and the need for conveyance. Many specialties changed the way they delivered care to their most vulnerable patients, again through the use of virtual consultations. The increase in the use of telemedicine extended to many sectors in acute care, including fracture clinics, primary care and mental health services. There was also careful consideration around the value of hospital admissions and end-of-life care for some patients. Many of these changes were welcome, perhaps overdue, but they were implemented at pace and the normal safeguards to ensure they worked as intended may have been missing. In these cases, it is important to consider the changes carefully and adapt them where necessary.
When COVID did start appearing in hospitals, it was doing so contemporaneously with efforts to ramp up capacity. There was an early initial focus on ensuring that staff working in higher risk areas had access to adequate higher-level PPE, and that the risk to patients from cross infection was reduced. The basic pathways adopted in most organisations involved separation of patients more likely to have COVID. These patients were managed through higher risk areas until their COVID status was known, and those who were COVID-positive were then treated in cohorted areas. There was also a need to ensure that access for patients needing the services of EDs and hospitals was maintained. These pathways have subsequently been improved and embedded, such that they are now part of routine NHS practice.
National lockdown was introduced in the face of rising infections. The impact of lockdown on demand for emergency care was profound, with significant reductions in attendances, although patients with more severe illness did continue to present. Possible reasons for this include changes in disease patterns or behaviour, patients being treated by alternative pathways, or anxiety over presenting to hospitals. The balance of each possibility is not fully understood, nor is the harm that may have arisen from delayed presentation for either emergency or less acute care. The impact of COVID itself was more variable, with some parts of the country much harder hit than others. The NHS as a whole was never completely overwhelmed, although some urban hospitals did reach full general and ICU capacity. Nightingale facilities were, in most cases, not required.
During the initial phase of the pandemic crowding disappeared from EDs. This is an observed phenomenon internationally and prompted emergency medicine leaders to call for improvement in the emergency care system to be made so that it did not return. In the UK, the Royal College of Emergency Medicine published ‘COVID-19, Resetting Emergency Care’ with this in mind.
Many organisations reported an improved sense of cohesion, and better collaboration between specialists and the ED. In addition, there was a reduction in bureaucracy and perceived barriers to innovation, with clinicians feeling more in-control. One might observe that the scope to leverage the organisational capacity of the NHS was demonstrated, with the entire national health service across four nations reorientated towards a single problem, whilst at the same time continuing to provide ongoing care for the population as a whole.
Information sharing, along with sharing of experience, was crucial. Within emergency medicine the introduction of video conferencing involving clinical leaders from across the nation has proved extremely valuable and is likely to continue into the future. International networking has also been improved in a similar fashion.
Lockdown eventually suppressed the first COVID peak and has gradually been easing, although at the time of writing there is concern about rising cases. Demand for emergency care has steadily risen from its nadir and is returning to normal. There is concern that the phenomenon of ED and hospital crowding is threatening to return. There are considerable challenges ahead for the emergency care system, particularly as we enter winter with a predicted increase in respiratory illness. Primary care services are still adjusting to the current situation and calibrating what can be safely achieved through virtual consultation, and with the demands of face-to-face assessment of potentially higher risk patients. Similar challenges exist for mental health services. EDs and hospitals now have systems to deal with symptomatic patients, although developments in more rapid testing may help decision making. Acute hospital capacity is believed to be significantly reduced as the result of attempts to distance patients (for instance, by reducing the numbers of patients in shared bays), while elective services have restarted with a need to start reducing backlogs. There is also an imperative to ensure that patients leaving hospital to care and residential facilities are discharged safely with regard to potential contagion.
In the immediate future, the NHS is investing more in forward-facing facilities, with a view to increasing capacity. There is a drive towards improved triage and direction of patients seeking urgent and emergency care to reduce ED attendances and help patients find the best avenue to secure the help they need. There is also a focus on the use of ambulatory care and early specialist involvement in care to avoid admission. The biggest challenge remains around overall acute capacity and workforce, along with the ongoing need to make improvements in hospitals around acute flow, since the main driver of ED crowding in the UK remains exit block. ED crowding in the face of a highly communicable endemic disease, which is so dangerous for many of the patients likely to be in our departments, is even more unacceptable than it was before the pandemic.
COVID 19 has proved an immense challenge to the emergency care system in the UK. The speciality of emergency medicine has demonstrated its ability to adapt to change and work to continue providing care to its patients, whilst the acute care system on the whole has changed profoundly in the face of this threat. The effects will be long lasting, with some of the adaptations likely to become permanent. Although there is a tendency to focus on the technological innovations, it is how we use existing technology that is new. However, it is the changes in culture, resource, and process in our systems that will have the greatest long-term impact, and our ability to learn from mistakes, and embed the positive lessons, which will be the greatest measure of our determination to change.
Ian Higginson BM MSc FACEM FRCEM
Emergency Physician; Vice President of The Royal College of Emergency Medicine, UK
In January 2020, the World Health Organization (WHO) was informed that a novel coronavirus had been identified in Wuhan City, Hubei Province, China.1 WHO declared the outbreak as a pandemic on 11 March,2 and, by 1 July, more than 10.4 million cases worldwide, in more than 188 countries and territories had been recorded.3
The Royal Brompton & Harefield NHS Foundation Trust is a specialist centre for the treatment of heart and lung diseases in London with 480 beds across both hospital sites. It is the largest cystic fibrosis (CF) centre in the UK, treating adult and paediatric patients and is one of the largest and most experienced centres for cardiothoracic transplantation and ventricular assist devices (VADs). Other services offered across the Trust include treatment of interstitial lung disease, cardiothoracic surgery, a dedicated heart attack centre, and intensive care.
Once the pandemic reached the UK, there became an urgent need for a significant expansion of critical care beds, including an escalation into unusual ward areas. Critical care capacity across the UK is around 4000 adult critical care beds under normal circumstances; however, it was reported that this would need to be increased to 10,000.4
In order to prepare for a large surge in the number of critical care patients at each hospital site, adult and paediatric cardiothoracic and cardiology elective pathways were changed. Adult and paediatric patients with complex cardiac or respiratory conditions such as pulmonary hypertension, CF, asthma, interstitial lung disease, heart/lung transplantation and those supported with VADs were increasingly largely managed as ambulatory care or in the community, to reduce their risk of contracting the virus. At the peak of the pandemic in London in April 2020, 117 patients were concurrently being treated at both the Brompton and Harefield hospitals, 90 of which required level 3 critical care support. The number of patients requiring veno-veno extracorporeal membrane oxygenation support for severe acute respiratory failure due to COVID-19 also reached a new milestone of 27 patients at a single point in time across three critical care units compared with five patients under normal circumstances.
Alongside the wider NHS, the pharmacy department had to adapt quickly to the overwhelming challenges ahead. Participation in face-to-face ward rounds and multi-disciplinary team meetings moved to more innovative methods of communication using virtual platforms, and senior pharmacists took on additional roles such as replenishing medicine stock lines (usually the responsibility of pharmacy technicians or assistants) to monitor stock levels very carefully and reduce pharmacy staff numbers on the wards. Individuals visiting COVID-19 Red Zones were expected to wear full personal protective equipment and working hours at the weekend were extended to support the medical and nursing teams to focus on their complex case load. Working from home, where possible, was encouraged to reduce footfall within the department and to implement social distancing.
There were also challenges in writing and updating guidelines with evidence as it emerged necessitating a couple of ‘live documents’ that were presented and ratified at bi-weekly virtual Trust committee meetings.
The demand for oxygen to cater for a surge of ventilated patients was a great cause for concern for the senior pharmacy management team. This is not normally an issue for hospitals as most patients are on no oxygen or low-flow oxygen. A substantially greater proportion of patients requiring oxygen therapy and ventilation was seen during COVID-19.
A patient safety notice from NHS England requested immediate attention to the use of high-flow oxygen therapy devices during the pandemic.5 There was a collaborative effort between Pharmacy, Estates and Clinical Engineering to ensure that adequate oxygen delivery could be provided to all areas with patients with critical care needs.
To monitor oxygen capacity, it was necessary to ascertain the maximum flow rate (l/min) from the vacuum insulated evaporator oxygen tank and a daily review of the number of high flow rate ventilatory systems. Urgent upgrade work was undertaken to increase output of piped oxygen across the organisation, by more than twofold.
As the number of critical care patients increased, staff were redeployed to critical care areas, which necessitated timely and extensive training in a very short period of time. This urgent need to upskill staff was recognised both internally and externally by the Royal Pharmaceutical Society and the UK Clinical Pharmacy Association and live seminars hosted by expert panellists on various aspects of critical care on a twice-weekly basis were available/provided. Training was provided to staff required to undertake alternative roles, in addition to internal presentations and support provided by the adult critical care pharmacy team. Nursing staff, re-deployed to critical care wards, were also trained on commonly used drugs on an intensive care unit.
Educating the paediatric medical and nursing teams on medications in adult critical care was supported by the paediatric pharmacy team who upskilled themselves quickly under the guidance of their adult counterparts. A guide to critical care medication for adult COVID patients was created, the most challenging aspect of this being weaning from sedation and managing adults with delirium.
All pharmacy teams outside critical care had to adapt their services to provide safe care to long-term patients shielding in the community.
The paediatric pharmacy team were particularly challenged as children were required to be cared for at home to make way for the increase in adult COVID patients and the paediatric intensive care unit (PICU) changed to an adult unit (PAICU).
Children who required home IV antibiotics and would previously have been seen in out-patient clinics were now being reviewed in their own home, via video platforms or telephone clinics, to reduce face to face contact and medication was sent out by post or courier. Independent prescribing scopes of practice were expanded to support the medical teams. Home care arrangements were extended, and new contracts set up, enabling biologics for asthma and other treatments to be undertaken at home.
The respiratory pharmacy team also supported innovative ways to treat patients at home. In excess of 400 patients with asthma were taught how to self-administer biologics at home to reduce the need to attend a face-to-face hospital appointment. Home intravenous therapies were expanded for patients with CF and non-CF bronchiectasis. Out-patient clinics became virtual and medication posted to a patient’s home address to ensure shielded patients did not have to venture out to collect their supplies. Patients requiring regular IV immunoglobulin had dose adjustments to extend the infusion interval and some patients were also switched to a subcutaneous route for self-administration at home.
Cardiothoracic transplant and VAD patients continued to require specialist support in the hospital and the occasional in-person follow-up in out-patients, however, where possible patients were supported at home. The specialist pharmacy team developed new ways of working to support this vulnerable group of shielded patients in their homes by using Telehealth (virtual and telephone clinics), a roll-out of finger-prick testing for the immunosuppressant tacrolimus, expanding homecare service for intravenous antibiotics, and oral immunosuppressants and other medicines as required. Tailored information was provided to patients via SMS texts, patient support groups newsletters and social media platforms. A ‘live webinar’ was established between consultant physicians, a consultant pharmacist and a clinical psychologist to support lung transplant recipients, with approximately 140 patients joining the event; this provided an exciting platform to answer numerous questions and concerns from patients.
The anticoagulation service was also adapted to meet the needs of patients requiring these where appropriate. Patients were switched to direct-acting oral anticoagulants to reduce test requirements, local INR testing with GPs and district nurses for warfarin was actively encouraged, and there was an expansion of self-testing at home to reduce need to attend hospital sites.
The randomised evaluation of COVID-19 therapy (Recovery) and Remap-Cap are novel adaptive clinical trials that commenced during the pandemic to evaluate several treatments, simultaneously, as new evidence emerged. These trials were adopted into the Trust very quickly, providing huge challenges to the pharmacy clinical trials team. A number of steps were necessary for the successful implementation of a particular domain such as the creation of a dispensing prescription template, design of standard prescription orders on two electronic prescribing systems and dissemination of administration guidelines. It was also necessary to ensure that all staff were familiar with the randomisation process (particularly at the weekend) and ensuring that patients transferred from other NHS Trusts were continued on a particular domain or standard of care arm. It was also necessary to respond to substantial amendments when treatments were suspended, or new arms created.
In line with NHS guidance at the time, clinical teams were also discouraged from using novel therapies (hydroxychloroquine, remdesivir, angiotensin 2, azithromycin) outside of clinical trials due to unproven benefit and risk of harm to patients and depletion of supply to existing patients with other long-term conditions.
A SITREP report was set up to identify concerns regarding the supply of critical medicines. This was to assure the senior management and clinical teams in the Trust of drug availability before accepting new patients. A significant proportion of these drugs were supplied on allocation to regions and Trusts, under central control and delivered on a ‘just-in-time’ basis to ensure supplies were shared across all hospitals and to prevent stockpiling. At the height of the pandemic in Europe, stockpiles of essential drugs were depleted and stock within the EU was under pressure from several countries. An example SITREP is shown in Table 1.
In order to create this SITREP table, it was necessary for members of the pharmacy purchasing team to conduct a stock count of critical drugs daily. This table was pivotal in informing clinicians of drug shortages, and clinical teams were very supportive to switching to alternative agents.
A SITREP for dialysis fluid and filter sets was also launched, as it became clear very early on that a substantial proportion of COVID-19 patients requiring critical care support were suffering from acute renal failure that required haemofiltration. Levels were assessed daily to inform clinicians of potential shortage issues. Haemofiltration bags were in very short supply and meetings were held regularly to discuss and monitor the use of renal replacement therapy and citrate haemofiltration was used as an alternative for non-COVID elective cardiac surgery patients. Nurses were supported where they were required to use unfamiliar products and, in some circumstances, additional electrolytes had to be added to bags. A risk assessment of adding high-strength potassium to these bags had to be undertaken rapidly between the pharmacy and clinical teams and gain approval by the Medicines Management Board, which would have taken longer, under normal circumstances.
A doubling of the fleet of nitric oxide machines and cylinders across both hospital sites was necessary as emerging evidence suggested that pulmonary vasodilatation may provide some benefit in the short-term to treat the complications of COVID-19 infection.
Following discussions with the senior nurse management team, it was clear that nurses on the front line were having difficulties with the demand for complex infusions due to the sheer volume and frequency of syringe changes. Pre-prepared drug syringes were outsourced to reduce nursing time in preparing commonly used parenteral medicines and to free up time for other clinical duties. The senior pharmacy management team were ready to deploy pharmacy staff to make up IV drugs on the ward, but the procurement of pre-filled syringes became a more viable option with a longer shelf life. Pre-filled syringes that proved very successful were magnesium injection 20mmol in 50ml, noradrenaline injection 8mg in 50ml and rocuronium injection 500mg/50ml.
Following discussion and approval between pharmacy critical care and clinical teams, other measures were taken to reduce intravenous drug burden and reduce reliance on drug infusion pumps by opting for medicines with longer half-lives (for example, pantoprazole IV 40mg od instead of ranitidine IV 50mg tds) and the administration of drugs as bolus/short infusions in favour of extended infusions (pip/tazobactam IV 4.5g over 30mins and meropenem IV 1g over 5mins instead of over 4 hours as per protocol). Novel ways to administer intravenous drugs in the same syringe, namely sedation, were also explored should the availability of infusion pumps become limited.
Temporary changes were made to the Medicines Management Policy to enable nursing staff to access CD in a more timely manner. The requirement for using the paper register to record entries of administrations was replaced with the use of the electronic register for critical care areas with automated drug cabinets.
The requirement for a second witness check was also temporarily removed for some CDs where a second check was undertaken as part of the administration process. This represented a huge challenge, particularly for a large number of staff re-deployed to critical care areas unfamiliar with local procedures and availability of opioid and sedative agents. Additional guidance was frequently updated and circulated and support made available. Temporary changes were kept under regular review.
Any stock discrepancies which occured during the height of the crisis were resolved in a timely manner by thorough scrutiny of the electronic CD register, dispensary records and paper CD orders. The main factor in the majority of discrepancies was due to unfamiliarity of a particular product line and subsequently it was decided to re-instate the second witness check. Positive user experience meant that electronic register could continue to be used to record CD transactions in automated drug cabinet areas in line with pre-existing project plans.
The COVID-19 pandemic has caused significant loss of life and disruption in every walk of life. For pharmacy staff, it has represented the most intense and stressful time of their career, causing anxiety, near burnout and emotional stress. The critical care pharmacy team has had to deal with a very high number of critical care patients; other teams have re-modelled their services to care for their patients safely in the community and the procurement team have had to deal with very challenging drug shortages. Regular ward stock checks and monitoring of drug shortages to prevent interruptions in therapy were very time consuming and stressful. Teams had to quickly adapt to latest critical medicine drug shortages and communicate this in a timely and effective manner. Coupled with daily uncertainty and an ever-changing landscape, few would argue that this pandemic has presented a situation like no other.
This challenging period of our careers has provided some positive developments to service delivery, that would normally take months or years to develop and implement. Some of the successes that can be celebrated include the use of virtual platforms for MDT and patient consultations and the use of IT to make processes more efficient, such as record keeping for CDs, ordering of parenteral nutrition and the use of electronic outpatient prescribing.
Information sharing between organisations across various specialties and regions (national and international) was pivotal to help hospital Trusts manage themselves effectively through different stages of the pandemic. Well-established critical care networks across north and south London were vital to update users on critical care bed capacity, guideline updates and drug shortages. As a specialist heart and lung institute, our specialist teams were able to provide advice to other centres on the use
of anticoagulation, steroids and pulmonary vasodilators to treat the complications of COVID-19 infection.
Chris Remmington* MPharm PgDip IP
Guy’s and St Thomas’ NHS Foundation Trust, UK
*at time of writing CR represented Royal Brompton & Harefield NHS Foundation Trust, UK
Nicola Holt BPharm
Sukeshi Makhecha BSc (Hons) MSc IP
Elaine Bowman BSc (Hons) MSc IP
Sian Bentley BPPharm PgDipPharmPrac IP
Haifa Lyster MSc FRPharmS FFRPS
Alastair Hill MPharm PgDip IP
Jaimisha Patel MPharm PgDip IP
Richard Di Palma MPharm PgDip IP
Sharon Clarke
Keith Thompson LLM MPharm MRPharmS
Royal Brompton & Harefield NHS Foundation Trust, UK
The first cases of COVID-19 in Italy were diagnosed on 30 January 2020; these were two Chinese tourists who were visiting Rome. Other isolated cases – all arriving or returning from China – had already been reported in France (24 January) and Germany (27 January). At that time, isolated cases or small outbreaks, all related to people who had recently been to China, had been reported in most European countries.
On 20 February 2020, in a climate of growing concern, in which – however – the real risk still seemed ‘far away’ (the World Health Organization would only declare a Sars-CoV-2 ‘pandemic’ on 11 March), the Italian public and the world of healthcare were shaken by the news. The first Italian case (‘Patient 1’) was a 38-year-old man admitted to Codogno Hospital (in a village of 15,000 inhabitants in the province of Lodi, Lombardy, Northern Italy) with severe pneumonia and the need for ventilatory support in the intensive care unit. He was defined as Patient 1 because he was considered the first to fall ill with COVID-19 on Italian soil, having not made trips abroad previously.
Over the next 24 hours, another 16 patients between Lombardy and Veneto tested positive for Sars-CoV-2; all of whom had not travelled to China recently. This was the start of the outbreaks of COVID-19 in Italy. As of 1 March 2020, Italy had 3089 confirmed cases and 109 deaths, most of them in the northern regions, and was, by far, the European country most affected by COVID-19, second only to China and South Korea.
It was almost impossible to understand what was happening in Italy: we were the first western country hit by a large-scale spread of Sars-CoV-2, where the virus seemed to have arrived extremely suddenly and disruptively, thereby seriously impacting on the response capacity of the public health service.
Epidemiologists in regions of northern Italy were on the hunt for ‘Patient 0’; that is the person who – after returning from other countries already affected by COVID-19 – had infected Patient 1 and spread the virus between Lombardy and Veneto.
Over time, however, it became clear that there was no Patient 0 because Patient 1 was evidently not the first Italian case. In retrospect, the common opinion, and also the official position of the Italian Ministry of Health, was that the Sars-CoV-2 virus had already been circulating in Italy for at least a few weeks prior causing, for the most part, less acute (and therefore more difficult to identify) cases, together with sporadic cases of interstitial pneumonia (which is also associated with other infections such as influenza) that would go undiagnosed.
As early as 21 February, the Italian Prime Minister had ordered the creation of ‘red zones’ for the municipalities of Lombardy and Veneto, which were the most affected. Knowing that the situation was no longer contained at a local level, a national lockdown was decreed from 4 March, with the closure of schools of all levels, universities, and non-essential production sites and a lockdown on free movement.
At the time of writing, 35,154 people have died as a result of COVID-19 in Italy, which is one of the highest mortality rates per million inhabitants in the world. We have had to pay a very high price in terms of human life, not to mention accompanying psychological impacts and economic repercussions. But the health service and civil society endured, perhaps unexpectedly according to some observers, so much so that The New York Times conceded: “…when Italy was the stuff of COVID nightmares, Trump and Biden, and much of Europe, mocked it as a shorthand for uncontrolled contagion. Now the pariah has become a model – however imperfect – of viral containment as the US and Europe struggle.”
Now the situation here has improved, many families are taking vacation at the sea or in the mountains. But we are keeping our guard up, the memories of the days of March and April still etched in the minds of the population and the healthcare workers at the forefront of care. We sincerely hope a second wave of COVID-19 will not come, but if it does, we hope to be able to face this fully prepared.
Filippo Fassio MD
Allergy and Clinical Immunology Unit, Azienda USL Toscana Centro, Italy
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