Paediatric Respiratory Reviews 35 (2020) 50–56

Contents lists available at ScienceDirect

Paediatric Respiratory Reviews

Review

European and United Kingdom COVID-19 pandemic experience:

The same but different
W.D. Carroll a, V. Strenger b, E. Eber b, F. Porcaro c, R. Cutrera c, D.A. Fitzgerald d, I.M. Balfour-Lynn e,⇑
a
Department of Paediatric Respiratory Medicine, Staffordshire Children’s Hospital at Royal Stoke, Newcastle Road, Stoke-on-Trent ST4 6QG, UK
b
Division of Paediatric Pulmonology and Allergology, Department of Paediatrics and Adolescent Medicine, Medical University of Graz, Auenbruggerplatz 34/2, A-8036 Graz, Austria
c
Pediatric Pulmonology & Respiratory Intermediate Care Unit, Sleep and Long-Term Ventilation Unit, Academic Department of Pediatrics, Bambino Gesù Children’s Hospital, Rome,
Italy
d
Department of Respiratory Medicine, Discipline of Child & Adolescent Health, Sydney Medical School, Faculty of Health Sciences, University of Sydney, The Children’s Hospital
at Westmead, Sydney, NSW 2145, Australia
e
Department of Paediatric Respiratory Medicine, Royal Brompton Hospital, Sydney Street, London SW3 6NP, UK

Educational aims

The reader will come to appreciate that:

 Under-preparedness for a pandemic was evident in all European countries.

 Diverging disease trajectories occurred with children comprising <4% of reported cases.
 Poor co-ordination between federal, state and regional jurisdictions was common.
 In the worst affected countries paediatric resources were redeployed to support adult patients.

a r t i c l e i n f o a b s t r a c t

Keywords: The global healthcare landscape has changed dramatically and rapidly in 2020. This has had an impact
COVID-19 upon paediatricians and in particular respiratory paediatricians. The effects in Europe, with its mature
SARS-CoV-2 healthcare system, have been far faster and greater than most authorities anticipated. Within six weeks
Pandemic of COVID-19 being declared a public health emergency by the World Health Organisation [WHO] in
Co-ordination
China, Europe had become the new epicentre of disease. A pandemic was finally declared by the WHO
Resource allocation
on March 11th 2020. Continued international travel combined with the slow response of some political
leaders and a variable focus on economic rather than health consequences resulted in varying contain-
ment strategies in response to the threat of the initial wave of the pandemic. It is likely that this variation
has contributed to widely differing outcomes across Europe. Common to all countries was the stark lack
of preparations and initial poor co-ordination of responses between levels of government to this unfore-
seen but not unheralded global health crisis. In this article we highlight the impact of the first wave of the
COVID-19 pandemic in Italy, Austria, Germany, and the United Kingdom.
Ó 2020 Elsevier Ltd. All rights reserved.

INTRODUCTION health emergency. On the 28th February 2020, as more countries

reported their first cases, the WHO raised the global risk level for
On the 30th January 2020, the World Health Organization the disease from ‘‘high” to ‘‘very high”, expressing serious concerns
(WHO) declared the outbreak of Coronavirus in China a public on the infection’s spread. By the 11th March 2020, the WHO
declared the worldwide spread of Coronavirus disease and spoke
for the first time of ‘‘pandemic”. Just two days later, Europe became
⇑ Corresponding author. the new epicentre of the Coronavirus pandemic. Shortly thereafter,
E-mail addresses: [email protected] (W.D. Carroll), volker.strenger@meduni- Italy, Spain, and United Kingdom would become the European
graz.at (V. Strenger), [email protected] (E. Eber), federica.porcaro@opbg.
countries with the greatest local transmission.
net (F. Porcaro), [email protected] (R. Cutrera), dominic.fitzgerald@health.
nsw.gov.au (D.A. Fitzgerald), [email protected] (I.M. Balfour-Lynn).

https://doi.org/10.1016/j.prrv.2020.06.012
1526-0542/Ó 2020 Elsevier Ltd. All rights reserved.
 W.D. Carroll et al. / Paediatric Respiratory Reviews 35 (2020) 50–56 51

ITALIAN EXPERIENCE to have SARS-CoV-2 with 6866 of eight thousand Italian Municipal-
ities included in this analysis [7].
Italian demographic data Unofficial data in children were more reassuring, as children
were less affected by severe disease [8]. Until May 14th, 4922
On the 30th January 2020, Italian health officials of the Spal- SARS-CoV-2 infected children, age 0–18 years, were reported,
lanzani Institute, in Rome, made the first diagnosis of SARS- accounting for about 2.2% of total cases. Among 4050 cases where
Coronavirus (SARS-CoV-2) infection in two Chinese tourists with data were available, 13.7% were under 1 year, 17.5% between 2 and
a travel history to Wuhan. On the 20th February 2020, the first 6 years, and 68.8% over 7 years. Just 3.3% of all paediatric cases
case of locally acquired SARS-CoV-2 (COVID-19) infection was required hospitalization and, by age group, children aged under
diagnosed in Codogno, a Northern Italian village, where a young 1 year were most frequently hospitalized. Only three children
man with no clear epidemiological link was hospitalized in a crit- who had serious pre-existing diseases died [9].
ical condition. In the next four days, the number of cases
increased rapidly in Northern Italian regions with three major Italian authorities’ response to the pandemic
clusters around the cities of Codogno, Bergamo and Cremona in
the Lombardia region [1]. By 24th February the number of In response to the outbreak of SARS-CoV-2, the Italian govern-
infected people reached 229 (Lombardia 172, Veneto 33, Emilia- ment suspended all China flights from 30th January and declared
Romagna 18, Piemonte 3, Lazio 3) with six deaths and 1 recov- a state of emergency one day later. Public health and social mea-
ered [2]. sures to slow or stop the spread of COVID-19 were initially consid-
Following this, the community spread of infection was rapid, ered in some ‘‘red areas” of Northern Italy. Finally, lockdown and
with devastating consequences. Exactly one month later, 69,176 social distancing were extended nationwide until May 3 [10].
confirmed cases of SARS-CoV-2 were reported nationwide, and Despite these restrictions, the number of new cases continued
6820 related deaths [3]. By March 24th 2020 all of the Italian to increase (Fig. 3) and patients with severe acute respiratory syn-
regions reported at least one locally acquired case of Covid-19. drome (SARS) due to COVID-19 presented a severe challenge to the
The incidence variability was related to the local transmission rate national healthcare system. The Italian Government authorised
that was highest in Northern Italy, with limited but increasing out- regions to recruit 20,000 health workers, allocating €660 million
breaks in Central-Southern Italy [4]. for the purpose; the Italian Civil Protection undertook a fast-
Despite the containment measures and lockdown ordered by track public procurement to secure ventilators, additional protec-
the Italian Government, the numbers of infected people progres- tive masks, and SARS-CoV-2 tests [11]. To address this emergency,
sively increased, reaching 192,994 cases in late April, two months each Italian region had to re-organize activities to increase the
after the infection’s outbreak in Italy (Fig. 1). The spread of infec- number of ICU beds and to address the healthcare workers and
tion was accompanied by a growing number of deaths, reaching the medical equipment shortage. Elective surgeries were post-
31,017 on May 20th 2020 [5]. poned to free beds and offer human and material resources. Non-
Lombardy and Emilia-Romagna were the most affected regions, urgent outpatient visits and private practices were suspended,
followed by Piemonte, Veneto and Liguria (Fig. 2). while medical evaluations for pregnant women, cancer patients,
Age and sex appear to be the most important prognostic indica- and fragile or unstable patients continued as before.
tors. The most severely affected patients were male (60.9%) at a Healthcare workers not directly involved in the emergency
mean age of 80 years (median 81, range 0–100). Only 312 out of were redeployed. They joined COVID-19 Internal Medicine, Respi-
the 27,955 (1.1%) positive SARS-CoV-2 patients under the age of ratory and Infectious Disease Departments, as well as Emergency
50 died. Of those who died, 59.9% had 3 or more comorbidities, Departments, often with gruelling 12-h shifts. General practition-
and cardiovascular diseases were the most common pre-existing ers modified their practice of delivering care, mostly through tele-
conditions [5,6]. phone calls or telehealth [12].
The Italian National Institute of Statistics recorded 25,354 As people avoided hospitals during the Coronavirus crisis,
deaths in the period from 20th February to 31th March; an increase Emergency Department visits across Italian hospitals were down,
of 39% over the numbers reported in the same quarters between but the number of late-presenting, serious cases increased. Control
2015 and 2019. Just over half of notified deaths were documented visits for patients with chronic medical complexity, both adults

Fig. 1. Timeline of spread infection in Italian regions.

52 W.D. Carroll et al. / Paediatric Respiratory Reviews 35 (2020) 50–56

well, the territorial health care systems were unprepared; with

an insufficient supply of personal protective equipment (PPE),
inadequate discussion and coordination with health departments
and institutions, lack of diagnostic tests, and insufficient training.
To meet these needs, private financing and the Italian government
allocated €3.5 billion to support the Italian healthcare system in
order to increase the number of beds in intensive care units, infec-
tious diseases, and respiratory units, to augment medical and nurs-
ing staff through new staff hiring and to purchase medical material
and equipment.
Collaboration between regions made it possible to decant over-
crowded hospital ICUs and to perform nasopharyngeal swab test-
ing in regions where the tests were not easily available. Despite
these efforts, the number of affected people exceeded the capabil-
ities of the workforce deployed. Italian healthcare workers paid a
Fig. 2. Italian distribution of confirmed SARS-CoV-2 deaths. very high price with more than 26,746 confirmed cases [13], 163
clinicians and 40 nurses succumbing to COVID-19, and many more
suffering with burnout.
and children, were postponed, increasing the unease of their fam-
ilies. To face this situation, healthcare workers added telehealth
monitoring visits to their already extraordinary activity. THE AUSTRIA/GERMANY PERSPECTIVES

The pandemic cases

Lessons to be learned from the Italian experience
The early establishment of contact restrictions led to a moder-
The worldwide scientific community and healthcare systems ate increase of SARS-CoV-2 infected cases in Austria (1854 tested
were caught unprepared by the sudden SARS-CoV-2 pandemic. positive per million inhabitants) and Germany (2159 tested posi-
Italy was the first European country that had to deal with this. tive per million inhabitants, data as of May 22nd) with decreasing
Under the Italian constitution, the Italian Ministry of Health con- numbers of new cases per day since late March (Austria) and early
trols the distribution of public financing and secures for free the April (Germany), respectively. Capacities of healthcare institutions
‘‘essential levels of care” (Livelli Essenziali di Assistenza, or LEA) including ICUs were never threatened in both countries. In contrast
to all residents in every region. However, recent changes in Italian to other countries, where big cities such as Paris, London, Madrid,
health policy had decreased the number of beds and healthcare and New York were the most affected areas, more rural areas were
workers; undermining the stability of the health system. In addi- affected early and more intensely in Austria (skiing areas in the
tion, the recent greater autonomy of individual regions accentu- Tyrol and Salzburg) and Germany (in Bavaria and Baden-
ated inequalities in the quality of services available. Württemberg).
Accordingly, the first challenge was a thorough re-organization Reported paediatric cases (patients <15 years of age) represent
of the healthcare infrastructure, where many units were re- 3.3% (5814 of 177,212) and 2.9% (467 of 16,360) of all registered
purposed to provide services solely dedicated to the COVID-19 cases in Germany (population of 83 millions) and Austria (popula-
emergency, while others continued to provide primary care. As tion of 8.8 millions), respectively. Hospitalised paediatric cases are

Fig. 3. Italian national trend of new positives, healed patients and deaths in the last three months (data updated to 24 May 2020). http://opendatadpc.maps.arcgis.com/apps/
opsdashboard/index.html#/b0c68bce2cce478eaac82fe38d4138b1. Yellow line: total positives; green line: discharged and healed patients; gray line: deaths.
 W.D. Carroll et al. / Paediatric Respiratory Reviews 35 (2020) 50–56 53

registered by paediatric societies in both countries. Only a minority patient was allowed. In many hospitals, fathers were also not
of paediatric patients were hospitalised (Germany, n = 196; Aus- allowed to enter delivery rooms. All these precautions were
tria, n = 16, 3.4% of paediatric cases, each), very few required inten- already taken before the peak of infections was reached.
sive care treatment (Germany, n = 19; Austria, n = 2, both with Particularly during the early phase, a shortage of personal pro-
SARS-CoV-2 associated hyperinflammatory conditions), and one tective equipment (PPE) occurred. Therefore, FFP2 and FFP3 masks
child died (Germany) (data as of May 22nd). were sterilised and reused. In some institutions and even more
among paediatric practitioners, self-made masks were used. Fur-
The precautions in response to the pandemic thermore, test capacities were also limited in the early phase. As
a consequence, restrictive and non-homogenous guidelines for
In Austria and Germany, restrictions for public life were when and in whom tests should be performed were established
imposed early on. In Austria, by March 10th indoor events with and occasionally modified. Comprehensive testing for health care
>100 and outdoor events with >500 attenders were banned, and personal was not routinely and universally performed.
universities closed. This was followed by a partial lockdown on
March 16th comprising closure of all shops except those providing
Opportunities and threats associated with the pandemic
basic supplies such as groceries and pharmacies, and closure of
restaurants, day care centres and schools. Lockdown measures
The pandemic has resulted in a more intense collaboration
included strict and monitored regulations with regard to leaving
between paediatric institutions, paediatric and adult services, spe-
home. This was only allowed for going to work (if necessary), run-
cialists in infectious diseases, pneumologists, and intensivists; and
ning errands, helping other people, and going for a walk alone or
also within professional societies in both countries [14]. Similar to
with members of the same household. Outside the home individu-
other countries, telemedicine has been more widely applied during
als were expected to keep at least 1 metre distance between them-
the pandemic, and will probably become standard practice in some
selves and other people during all activities.
areas. On the other hand, coming along with significantly
In Germany, almost identical regulations were implemented in
decreased paediatric emergency visits, outpatients in general,
the same periods of time. The early implementation of these
and hospital admissions the significance and relative importance
restrictions was followed by a delayed and initially moderate
of paediatrics in general and paediatric respiratory medicine in
increase of infections. In this phase, the healthcare systems pre-
particular might be questioned by hospital administrations.
pared for the emergence of numerous SARS-CoV-2 infected
patients.
As both Austria and Germany are federal republics, instructions
THE UNITED KINGDOM: IS IT THE SICK MAN OF EUROPE?
for testing, taking precautions in the healthcare system and
managing SARS-CoV-2 infected patients differed from federal state
By the 5th May 2020, the UK had overtaken Italy, as the worst
to federal state, and sometimes even from region to region, despite
affected country in Europe, with almost 30,000 deaths attributed
(new) federal laws regarding an epidemic, and advice from autho-
to COVID-19 (and one month later over 40,000 deaths). In common
rized and highly acknowledged entities such as the Robert Koch
with other countries, children appear to have been mildly affected
Institute.
in most instances. The precise clinical picture is still emerging but
despite a well-established and admired universal healthcare sys-
The response in hospitals
tem (the National Health Service) the mortality has been higher
than its neighbours.
All hospitals and other healthcare institutions were obliged to
It became apparent early in the course of the pandemic that
identify patients with proven or suspected SARS-CoV-2 infections
children would be likely to be less severely affected and this
by triage systems. Specific hospitals, and specific departments (in-
resulted in a very significant reorganisation of care across the
cluding paediatric departments), wards and intensive care units
National Health Service (NHS). However, a small number of chil-
(including PICUs), were designated and prepared for caring for
dren have presented far later than expected and a new condition,
COVID-19 cases.
Paediatric Inflammatory Multisystem Syndrome – Temporally
In Germany and Austria whilst some ‘non-acute’ medical
associated with SARS-CoV-2 pandemic (PIMS-TS) has emerged
departments such as dermatology and ophthalmology were desig-
[15]. Some children have had associated circulatory shock requir-
nated for the management of COVID-19 cases, no paediatric
ing PICU, a serious issue considering the reduced PICU capacity
departments were repurposed nor were paediatricians redeployed
since some have been converted into AICUs for adult patients with
for attending adult patients. Non-emergency appointments and
COVID-19.
elective surgical procedures were universally cancelled to increase
capacity for the pandemic.
In common with many other countries, emergency visits and Response to the pandemic: reorganisation of care in the UK
paediatric admissions decreased significantly for at least two rea-
sons: (1) In contrast to the pre-pandemic era, parents sought hos- For paediatricians this reorganisation resulted in the centralisa-
pital contact only when their children had more severe medical tion of paediatric services with the complete closure of some pae-
problems, and (2) social distancing not only resulted in a limited diatric departments in major (e.g. London and Birmingham). In
spread of SARS-CoV-2, but also of other pathogens causing acute many centres, paediatricians were redeployed to adult services
diseases or exacerbations of chronic respiratory diseases. Staff and adult intensive care units.
presence in the hospitals was reduced, and whenever possible Fortunately, this redeployment was associated with a very sig-
teams were divided into two groups to avoid virus transmissions. nificant fall in paediatric admissions over the same period. This ini-
In addition, visiting bans were established and strictly con- tial relief was quickly followed by a realisation that children and
trolled in many hospitals and nursing homes. Exceptions were only families were, in many instances, too frightened to attend hospital
made for children, palliative care and dying patients, again with or their general practitioner. This led to the launch of a position
regional differences. For children, often only one reference person statement from the Royal College of Paediatrics and Child Health
(resulting in usually fathers not being allowed to see their children (RCPCH) on the 3rd April 2020 regarding delayed access to care
for prolonged periods of time) or one visiting person per day and for children during COVID-19 [16].
54 W.D. Carroll et al. / Paediatric Respiratory Reviews 35 (2020) 50–56

The RCPCH also provided guidance for planning paediatric staff- tions of ‘clinically extremely vulnerable’ were brief, and there
ing and rotas. This specifically recommended reducing the number was particular difficulty with defining which asthmatic patients
of staff per shift but having more senior availability in the hospital needed to shield. There was inconsistency between information
to support decision making. Coupled with a marked reduction in sources for the public (for example NICE and Asthma UK), and def-
referrals from primary care and the difficulty in providing safe, initions kept changing. There were also many omissions from the
face-to-face outpatient reviews led to a significant change in pat- government recommendations, for example children with intersti-
terns of working for paediatricians. The most generally reported tial lung disease, bronchiectasis etc. The British Paediatric Respira-
experience is that the hours for most paediatricians have been tory Society [BPRS] produced a consensus list (Table 1).
much longer but work intensity and patient numbers have reduced
significantly. Fragmented communication and blurred lines of responsibility

Infection issues At the start, the government stated that 1.5 million people
would receive a letter telling them if they needed to shield, within
One of the biggest challenges which arose in the early phases of 7 days, starting in 2 days’ time. How they came up with that figure
the pandemic in the UK was a shortage of personal protective is uncertain, but data was being taken from primary care systems.
equipment (PPE). The situation was complicated by the lack of a Contact was haphazard missing out some patients who should be
single voice on what was required, and by whom. Individual organ- shielding and sending unnecessary advice to others who clearly
isations and professional groups issued their own, often contradic- should not. Lists of who had received the shielding letter were
tory advice to those issued by Public Health England (PHE) [17]. In eventually sent to tertiary units and they were able to identify
general, these tended to suggest that higher levels of PPE were patients from clinic lists and databases and advise accordingly.
required by their own members and this inevitably led to confu- Whilst shielding has been helpful for some families, for example,
sion and distress amongst healthcare professionals. allowing priority for supermarket home delivery, it has caused
Much time, effort and intellectual energy was consumed on problems and financial hardship when parents/carers need to go
defining what was (and what was not) an aerosol generating pro- out to work. In May, the BPRS made new recommendations to
cedure. This led to concern from families about the safety of nebu- RCPCH and thus on to Public Health England, which were defining
lisation of drugs and non-invasive ventilation in the home, those needing mandatory shielding versus those with diseases in
including safety of professional carers. Shortages of PPE, coupled which decisions could be made on a case by case basis. It was rec-
with the deaths of healthcare workers, led to national headlines. ommended that the changes be made at the end of the initial
Hopefully, greater consensus will be achieved about the relative shielding period that was due to finish at the end of June. Then sud-
risks of different procedures and patient groups in the coming denly the politicians announced on a Saturday evening (May 30th)
months, which will allow us to adequately plan the purchase, pro- with no prior warning, nor seemingly any consultation with the
vision and distribution of PPE to meet the needs of healthcare specialist groups, that shielding could stop now, in that all vulner-
professionals. able people could now go outside once a day, and if they lived
In the classic British style of ‘make do and mend’ originating alone could meet someone from a different household. Inevitably
with the clothing shortages in the Second World War, many hospi- this resulted in confusion and anxiety amongst patients and
tals have made their own PPE. For example, at the Royal Brompton families.
Hospital, the engineering department produced plastic face shields
whilst fashion students sat in the local Town Hall and made PPE Production of guidelines
gowns.
Since the pandemic, there has been a deluge of guidelines. The
Shielding advice UK based National Institute for Health and Care Excellence (NICE)
usually takes 18–24 months to produce a guideline and 11–
On 22nd March 2020 the UK government announced a recom- 13 months for short clinical guidelines. During the Pandemic their
mendation that those who may be at increased risk of severe ill- COVID-19 rapid guidelines have been produced in 1–2 weeks.
ness from COVID-19, due to significant underlying conditions, Royal Colleges, Specialist Societies and Charities/Family Support
should be shielded. This guidance is updated regularly [18]. Shield- groups have also put guidance on their websites. Most relevant
ing, known in some countries as cocooning, meant the person was to respiratory paediatrics are the NICE guidelines on severe asthma
to stay indoors at home for 12 weeks with further restrictions [19] and cystic fibrosis (CF) [20]. Inevitably, much of these NICE
within the home. As is often the case, this seemed quite orientated guidelines is generic and not too detailed, but at a time when staff
to adult patients. As regards respiratory conditions, initial defini- were being redeployed from paediatric to adult COVID work, and

Table 1
Initial BPRS guidance on which patients should shield.

 Cystic fibrosis
 Primary ciliary dyskinesia
 Significant bronchiectasis
 Chronic lung disease of prematurity with oxygen dependency
 Severe asthma – as defined by NICE
 Interstitial lung disease
 Obliterative bronchiolitis
 Children receiving additional daytime and/or night time oxygen.
 Life-dependent on long term ventilation (via tracheostomy or non-invasive ventilation)
 Neuromuscular disease on long term ventilation
 Significant underlying neurodisabilities and lung infection risk, e.g. those requiring cough assist at home
 Significant lung disease relating to underlying systemic diseases such as rheumatological disease
 W.D. Carroll et al. / Paediatric Respiratory Reviews 35 (2020) 50–56 55

Table 2
For future pandemics we must:

 Ensure the safety of healthcare professionals with effective personal protective equipment (PPE)
 Ensure training on infection prevention and control in all healthcare facilities
 Prepare evidence based national diagnostic and therapeutic pathways to improve the care of patients and healthcare workers alike
 Change the concept of patient-centred health to community-centred health by strengthening regional healthcare, to mitigate the risk of overwhelming hospitals
 Guarantee public and private economic resources for healthcare workers, healthcare facilities, and essential supplies that must be quickly mobilized to address
exceptional emergencies
 Effectively mobilize human resources to respond to a pandemic and support those dealing with heavy and potentially dangerous workloads with the risk of burnout
 Consider the immense impact on the social, economic and working life of all, especially the most vulnerable in society

paediatric wards were being closed down, it was important to state DIRECTIONS FOR FUTURE RESEARCH
that specialist CF units should retain in-patient services and that
sufficient clinical expertise (i.e., the multidisciplinary team) remain  Establish and assess the effectiveness of better protocols for
within the CF teams. centralised distribution of national resources, such as personal
protective equipment, in response to future pandemics.
 Determine the relative effectiveness of strategies of hand
hygiene, wearing of masks, physical distancing and school clo-
What have we gained from the pandemic in the UK?
sures on the disease trajectory in pandemics.
 Using economic modelling, assess the cost benefits to all coun-
There have been some aspects of the enforced changes in the
tries of improved funding to international organisations such as
delivery of health care as a result of the pandemic that have been
the World Health Organisation to monitor, intervene and co-
beneficial to patients and the National Health Service (NHS). Tele-
ordinate the response to pandemics.
medicine has taken a remarkable leap forward. It has been used in
some units, for example in adult CF care, over the last few years,
both via telephone and video conferencing. With the shutdown
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