Disruptions of neurological services, its causes and mitigation strategies during COVID-19: a global review

Abstract

Background
The COVID-19 pandemic leads to disruptions of health services worldwide. To evaluate the particular impact on neurological services a rapid review was conducted.

Methods
Studies reporting the provision of neurological services during the pandemic and/or adopted mitigation strategies were included in this review. PubMed and World Health Organization’s (WHO) COVID-19 database were searched. Data extraction followed categories used by WHO COVID-19 pulse surveys and operational guidelines on maintaining essential health services during COVID-19.

Findings
The search yielded 1101 articles, of which 369 fulfilled eligibility criteria, describing data from 210,419 participants, being adults (81%), children (11.4%) or both (7.3%). Included articles reported data from 105 countries and territories covering all WHO regions and World Bank income levels (low income: 1.9%, lower middle: 24.7%, upper middle: 29.5% and high income; 44.8%). Cross-sectoral services for neurological disorders were most frequently disrupted (62.9%), followed by emergency/acute care (47.1%). The degree of disruption was at least moderate for 75% of studies. Travel restrictions due to lockdowns (81.7%) and regulatory closure of services (65.4%) were the most commonly reported causes of disruption. Authors most frequently described telemedicine (82.1%) and novel dispensing approaches for medicines (51.8%) as mitigation strategies. Evidence for the effectiveness of these measures is largely missing.

Interpretation
The COVID-19 pandemic affects all aspects of neurological care. Given the worldwide prevalence of neurological disorders and the potential long-term neurological consequences of COVID-19, service disruptions are devastating. Different strategies such as telemedicine might mitigate the negative effects of the pandemic, but their efficacy and acceptability remain to be seen.

Full text

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Journal of Neurology (2021) 268:3947–3960
https://doi.org/10.1007/s00415-021-10588-5
REVIEW
Disruptions ofneurological services, its causes andmitigation
strategies duringCOVID‑19: aglobal review
DavidGarcía‑Azorín1 · KatrinM.Seeher2· CharlesR.Newton3 · NjidekaU.Okubadejo4 · AndreaPilotto5 ·
DeannaSaylor6 · AndreaSylviaWinkler7,8 · ChahnezCharTriki9 · MatildeLeonardi10
Received: 26 April 2021 / Accepted: 29 April 2021 / Published online: 22 May 2021
© The Author(s) 2021
Abstract
Background The COVID-19 pandemic leads to disruptions of health services worldwide. To evaluate the particular impact
on neurological services a rapid review was conducted.
Methods Studies reporting the provision of neurological services during the pandemic and/or adopted mitigation strategies
were included in this review. PubMed and World Health Organization’s (WHO) COVID-19 database were searched. Data
extraction followed categories used by WHO COVID-19 pulse surveys and operational guidelines on maintaining essential
health services during COVID-19.
Findings The search yielded 1101 articles, of which 369 fulfilled eligibility criteria, describing data from 210,419 partici-
pants, being adults (81%), children (11.4%) or both (7.3%). Included articles reported data from 105 countries and territories
covering all WHO regions and World Bank income levels (low income: 1.9%, lower middle: 24.7%, upper middle: 29.5% and
high income; 44.8%). Cross-sectoral services for neurological disorders were most frequently disrupted (62.9%), followed
by emergency/acute care (47.1%). The degree of disruption was at least moderate for 75% of studies. Travel restrictions due
to lockdowns (81.7%) and regulatory closure of services (65.4%) were the most commonly reported causes of disruption.
Authors most frequently described telemedicine (82.1%) and novel dispensing approaches for medicines (51.8%) as mitiga-
tion strategies. Evidence for the effectiveness of these measures is largely missing.
Interpretation The COVID-19 pandemic affects all aspects of neurological care. Given the worldwide prevalence of neuro-
logical disorders and the potential long-term neurological consequences of COVID-19, service disruptions are devastating.
Different strategies such as telemedicine might mitigate the negative effects of the pandemic, but their efficacy and accept-
ability remain to be seen.
Keywords Nervous system diseases· Neurology· Health services administration· Telemedicine· COVID-19
Background
The Coronavirus disease 2019 (COVID-19) pandemic has
caused a substantial number of deaths worldwide, surpassing
three million casualties as of April 2021 [1]. However, this
number does not even begin to quantify the hidden toll of
the pandemic—the collateral damage it has caused. Among
these are the excess deaths associated with COVID-19 [2,
3] which are at least partly due to disruptions in the health-
care systems, including the discontinuation of emergency
and acute care, difficulty accessing routine outpatient ser-
vices, and difficulties related to accessing essential medi-
cations and other therapies such as childhood vaccination
programmes contributing to increased mortality and disabil-
ity [4]. Chronic diseases requiring regular healthcare are
particularly affected by the discontinuation and/or reduced
capacities of health services and the impact on noncommu-
nicable diseases (NCDs) [5], of which neurological disorders
represent the largest part [6–8], still remains to be seen.
The World Health Organization (WHO), as part of its
COVID-19 strategic preparedness and response plan
released operational guidance on maintaining essential ser-
vices during COVID-19 [9], containing recommendations
Chahnez Charfi Triki and Matilde Leonardi These authors are
co-last authors.
* David García-Azorín
dgazorin@ucm.es
Extended author information available on the last page of the article
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3948 Journal of Neurology (2021) 268:3947–3960
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for mental, neurological and substance use (MNS) disor-
ders focusing on maintaining emergency/acute care, treat-
ment and care in outpatient settings, residential care, cross-
sectoral service delivery such as for example community
services or inclusive schooling and mental and brain health
promotion. Patient associations and scientific societies have
also published guidelines and conducted surveys in the first
months of the pandemic [10, 11]. A rapid assessment of
MNS services conducted by WHO with 130 Ministries of
Health worldwide during June–August 2020 highlighted
the disruption of essential MNS services in most countries
[4]. While the rapid assessment did not specifically focus
on neurological services (in fact, often information on neu-
rological services was not readily available to Ministries of
Health despite the fact that neurological disorders, including
dementia and stroke, represent the leading cause of disabil-
ity-adjusted life years [6, 15]), it nevertheless demonstrated
that surgery for neurological patients was disrupted in 1 out
of 3 countries, emergency care for neurological patients
was at least slightly disrupted, and outpatient neurological
care was severely disrupted in most countries. The WHO
authors concluded that valid data and better evidence, espe-
cially regarding the use of routine and innovative forms of
information and communications technology, such as tel-
ehealth or mobile phone apps [12] were needed to mitigate
the effects of the pandemic on service disruptions [4].
Telemedicine, defined as the use of information and
communication technologies to improve patient outcomes
by increasing access to care and medical information, was
coined in the 1970’s [13]. However, before the pandemic, the
service provision rate of telemedicine was just over 33% in
a survey conducted by the Global Observatory for eHealth
in 114 countries in 2009 [14]. In the context of COVID-19,
WHO defines telemedicine as “solutions (including) clini-
cal consultations conducted via video, chat or text message,
staffed helplines, e-pharmacies and mobile clinics with
remote connections to health facilities for timely access
to patient data such as medication lists and diagnostic test
results” [9].
To what extent these and other mitigation strategies are
used, and their effectiveness monitored during the pan-
demic remains unknown. To this end, we conducted a rapid
review of the published evidence regarding the impact of the
COVID-19 pandemic on disruptions of neurological services
and the mitigation strategies implemented for the care of
patients with neurological disorders.
Materials andmethods
To evaluate the impact of the COVID-19 pandemic on dis-
ruptions of neurological services and the implemented miti-
gation strategies, WHO commissioned this rapid review on
the topic. The literature search was conducted according to
the Preferred Reporting Items for Systematic Reviews and
Meta-analyses (PRISMA) [16]. A standardized data extrac-
tion sheet was designed in line with the categories used
in WHO’s COVID-19 Pulse Surveys as well as the Rapid
Assessment of MNS disorders [4]. The study was done in
parallel with a Global Survey on disruptions and mitiga-
tion strategies coordinated by the European Federation of
Neurological Associations (EFNA) in collaboration with 34
scientific and patient associations related to neurology in
support of WHO’s Neurology and COVID-19 Global Forum
working group on Essential Neurological Services. We used
the same variables, to allow future comparability between
the results of the survey and the present study.
Selection criteria
Studies were included if they addressed the impact of the
COVID-19 pandemic on the provision of neurological ser-
vices, adopted or proposed mitigation strategies, or both.
Studies were excluded in the following cases: (i) publication
before November 2019; (ii) lacking original data; (iii) pub-
lication in a language other than English, Spanish, French,
Italian, Portuguese or German; (iv) focus on basic science or
preclinical aspects of the infection; and (v) focus on clinical
aspects, diagnosis or therapeutics only.
Search strategy
Two databases were screened, PubMed and the WHO
COVID-19 database, a curated database of all COVID-19
related published articles and pre-publications. The search
was conducted on February 18, 2021 and updated on Feb-
ruary 28, 2021. The search string was developed together
with a WHO librarian combining terms on three axes: (1)
COVID-19 related terms, (2) neurological categories and
(3) outcomes related to service disruption and mitigation
strategies [17]. The full detail on the search is available in
the supplementary appendix.
Study selection criteria
A single author (D GA) screened all search results to iden-
tify studies meeting inclusion criteria. The studies were
ordered chronologically and included in a spreadsheet.
Both the title and the abstract of the studies were reviewed.
Whenever eligibility could not be determined by the title and
abstract alone, the full articles were screened for eligibility.
When the study did not fulfil eligibility criteria, the reason
for exclusion was described in the database.
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3949Journal of Neurology (2021) 268:3947–3960
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Data extraction process andextracted information
The method of data extraction was automatic from the Pub-
Med database for the following variables: title, authors,
citation, journal, digital object identifier (DOI) and date of
creation in PubMed; the remaining variables were manually
extracted. For the WHO database, all data were manually
extracted using a standardized form. The extracted informa-
tion included the publication date, the studied population
(adult, children or both), the subspecialty of neurology, lan-
guage of publication, country, where the study took place,
study design, and study setting (inpatient, emergency care,
outpatient, or a combination). The full list of subspecial-
ties and study designs is available in the supplementary
appendix.
The sample size was also described, and in those studies
that accounted for patients from 2020 and historical controls,
we only included patients studied in 2020. When the study
analyzed specialties of medicine other than neurology, only
the neurological patients were included in the sample size. If
the study described the opinion of healthcare providers, car-
egivers or students, the number of participants interviewed
was included as the sample size.
Specific variables evaluated forservice disruption
andmitigation strategies
Data extraction followed the same categories of services,
causes for disruption, and mitigation strategies as used by
WHO’s COVID-19 Pulse Surveys, the Rapid Assessment
of MNS services as well as WHO’s operational guidelines
on maintaining essential health services during COVID-19
(chapter on MNS disorders) [4, 9], with additional delinea-
tions as and when necessary.
First, we extracted whether the study described any
degree of interruption of the following categories: (1)
emergency and acute care for neurological disorders; (2)
investigations (including neuroimaging, neurophysiology,
lab diagnostics, and others); (3) treatment and care for
neurological disorders (including interventions and thera-
pies, such as planned surgeries and access to medicines);
(4) neurorehabilitation, inclusive of physiotherapy, speech
therapy, occupational therapy, cognitive rehabilitation, and
psychology/counselling; (5) cross-sectoral service deliv-
ery for neurological disorders, including community-based
services, residential long-term care, adult/child day care,
special/inclusive school educational programmes for chil-
dren, interventions for caregivers, and services/programmes
delivered by non-governmental organizations; (6) promotion
of brain health and prevention of neurological disorders, in
addition to implementation activities of national prevention
plan and neurology advocacy; (7) training of residents, PhD
students or other educational activities; (8) research.
The causes of service disruptions were assessed and clas-
sified into: (1) closure of inpatient or outpatient services or
consultations as per health authority directive; (2) decrease
in outpatient volume due to patients not presenting for care;
(3) decreased volume of patients due to cancellation of elec-
tive care; (4) inpatient services/hospital beds not available
due to saturation; (5) insufficient staff to provide services
(e.g., due to quarantine/self-isolation of health-care provid-
ers due to COVID-19); (6) clinical staff shifted to provide
COVID-19 clinical management or emergency support; (7)
insufficient Personal Protective Equipment (PPE) available
for health care professionals to provide services; (8) disrup-
tion of supply chains resulting in unavailability or stock out
of essential medicines, medical diagnostics or other health
products at health facilities; (9) travel restrictions hindering
access to the health facilities for patients.
The degree of service disruption was graded into no
disruption, mild, moderate, or severe, based on the study
findings as per the authors judgment. In case the level
of disruption was not explicitly reported, the degree was
approximated based on the change respective to the baseline
period or with other similar studies, as mild (1–39%), mod-
erate (40–69%) or severe (70% or higher).
Mitigation strategies were classified into the following
categories: (1) triaging of neurological patients to identify
priorities; (2) redirection of patients to alternate care sites
(e.g., primary care), reorientation of referral pathways or
integration of several services into a single visit; (3) tel-
emedicine deployment to replace in-person consults or
other teleconsultation formats; (4) self-care interventions,
provision of home-based care, or helplines for patients and
caregivers; (5) catch-up campaigns for missed appoint-
ments; (6) task-shifting or role delegation; (7) recruitment
of additional staff, novel supply chain management and
logistics approaches; (8) novel dispensing approaches for
medicines, novel prescribing approaches (e.g., tele-prescrip-
tion, extended drug prescriptions); (9) community commu-
nications (e.g., informing on changes to service delivery,
addressing misinformation and community fears) to ensure
that all citizens are aware and informed of continuity of ser-
vices and that routine care can always be sought; and (10)
government removal of user fees.
Risk ofbias, summary measures andsynthesis
ofresults
Since this review was not focused on the results of a thera-
peutic or diagnostic intervention, whenever any information
regarding service disruption or mitigation strategies was pre-
sent, the study was included in the review. The results were
summarized as numbers and percentage of studies per cat-
egory, over the total of included studies. Traditional tools for
the evaluation of bias were not appropriate for the purpose of
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3950 Journal of Neurology (2021) 268:3947–3960
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the study, and, therefore, were not used. Although not neces-
sarily considered a bias in itself, we analyzed whether stud-
ies were published in international journals versus national
or regional journals for the most frequently studies countries.
Additional analyses
We classified the represented countries according to the
Gross National Income (GNI) per capita, according to the
2019 World Bank atlas [17] criteria, into low income, lower
middle, upper middle and high income. The full criteria are
available in the supplementary appendix.
Results
The search yielded 1,020 matches in PubMed and 1,170
matches in the WHO COVID-19 database. Figure 1
describes the flow diagram of the study selection, includ-
ing the number of studies identified, screened, included and
excluded. Ultimately, 369 articles fulfilled eligibility criteria
and provided valid data. [Fig.1 near here].
The included studies described data from 210,419 par-
ticipants, with a median number of 127 (IQR: 48–324) par-
ticipants. The studied population was adults in 295 (81.0%)
studies, children in 42 (11.4%) studies, both adults and chil-
dren in 27 (7.3%) studies and unclear in five (1.4%) studies.
Fig. 1 PRISMA flow diagram of screened, included and excluded studies
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3951Journal of Neurology (2021) 268:3947–3960
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Descriptive analysis ofincluded studies
Publication date
The manuscripts were published in January 2020 in one
(0.3%) case, April in 12 (3.2%), May in 47 (12.7%), June in
32 (8.7%), July in 33 (8.9%), August in 48 (13.0%), Septem-
ber in 49 (13.3%), October in 44 (11.9%), November in 40
(10.8%), December in 34 (9.2%), January 2021 in 22 (5.9%)
and February 2021 in seven (1.9%) cases.
Represented countries
Thirty-five studies represented data from multiple coun-
tries (9.5%), while the remaining 334 studies described the
situation in a total of 42 different countries (Fig.2). The
most frequently studied country was the United States of
America (USA) (n = 94 studies, 25.5%), followed by Italy
(n = 53 studies, 14.4%), the United Kingdom (UK) (n = 31
studies, 8.4%), and Spain (n = 26 studies, 7.0%). Supplemen-
tary Fig.1 presents the percentage of studies published in
national journals for the most frequently studied countries.
When counting studies capturing both single and multiple
countries, 105 countries and territories covering all WHO
regions were included in the review. Table1 lists all coun-
tries that were represented in the review.
Of all the represented countries, only two were low-
income countries (1.9%); the majority were high-income
countries (n = 47, 44.8%), followed by upper-middle-
income countries (n = 31, 29.5%) and lower-middle-income
countries in 26 (24.7%). Figure2 represents the proportion
of studies per GNI category
Studied subspecialties
There were 87 (23.6%) studies that described results across
all neurological subspecialties (Fig.3). Of studies focusing
on a single subspecialty, vascular neurology was the most
frequently studied (n = 100 studies, 27.1%), followed by
epilepsy (n = 52 studies, 14.1%), and cognitive neurology
(n = 38 studies, 10.3%). There were 169 different journals,
with Epilepsy Behaviour being the most represented (n = 28
publications, 7.6% of total publications), followed by Jour-
nal of Stroke and Cerebrovascular Diseases (n = 21 pub-
lications, 5.7%), and Stroke (n = 16, 4.3%). The full list of
journals is available in the supplementary Table1.
Study aim, design andsetting
One hundred and forty-five (39.3%) publications focused on
service disruptions, 129 (35.0%) on mitigation strategies and
95 publications (25.7%) on both. The most frequent study
design was cross-sectional (n = 103, 27.9% publications),
followed by the description of an implemented protocol
(n = 99, 26.8%), before–after studies (n = 97, 26.3%), case
series (n = 57, 15.4%), prospective cohort studies (n = 10,
2.7%), and retrospective cohort studies (n = 3, 0.8%). The
most common study setting was the outpatient setting
(n = 187, 50.7%), followed by emergency care (n = 105,
28.5%), inpatient setting (n = 38, 10.3%), and multiple
Fig. 2 Countries represented in
the including studies according
to the Gross National Income
category
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3952 Journal of Neurology (2021) 268:3947–3960
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Table 1 Countries represented in the study
Country GNI group Number of multiple-
countries studies
Number of single-coun-
try studies
Percentage over the total
of single-country studies
Angola Lower middle income 1 0 0
Argentina Upper middle income 12 3 0.8
Aruba High income 1 0 0
Australia High income 13 4 1.1
Austria High income 6 1 0.3
Azerbaijan Upper middle income 1 0 0
Bangladesh Lower middle income 1 0 0
Belarus Upper middle income 1 0 0
Belgium High income 13 2 0.5
Bosnia and Herzegovina Upper middle income 1 0 0
Brazil Upper middle income 14 4 1.1
Bulgaria Upper middle income 2 0 0
Bhutan Low income 1 0 0
Cameroon Lower middle income 1 0 0
Canada High income 29 14 3.8
Chile High income 4 1 0.3
China Upper middle income 25 17 4.6
Hong Kong Lower middle income 3 3 0.8
Taiwan, China Low income 1 0 0
Colombia Upper middle income 7 0 0
Costa Rica Upper middle income 3 0 0
Croatia High income 7 0 0
Cyprus High income 2 0 0
Czech Republic High income 5 0 0
Denmark High income 9 0 0
Ecuador Upper middle income 2 0 0
Egypt Lower middle income 5 0 0
Estonia High income 3 0 0
Finland High income 7 1 0.3
France High income 23 9 2.4
Georgia Upper middle income 2 0 0
Germany High income 27 15 4.1
Ghana Lower middle income 1 1 0.3
Greece High income 7 0 0
Guatemala Upper middle income 1 0 0
Honduras Lower middle income 1 0 0
Hungary High income 3 0 0
India Lower middle income 21 11 3
Indonesia Upper middle income 5 2 0.5
Iran Upper middle income 6 4 1.1
Iraq Upper middle income 2 0 0
Ireland High income 13 5 1.4
Israel High income 4 0 0
Italy High income 68 53 14.4
Jamaica Upper middle income 1 0 0
Japan High income 6 2 0.5
Kazakhstan Upper middle income 3 0 0
Kenya Lower middle income 1 0 0
Kosovo Upper middle income 1 0 0
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3953Journal of Neurology (2021) 268:3947–3960
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Table 1 (continued)
Country GNI group Number of multiple-
countries studies
Number of single-coun-
try studies
Percentage over the total
of single-country studies
Kuwait High income 3 1 0.3
Kyrgyzstan Lower middle income 2 0 0
Laos Lower middle income 1 0 0
Latvia High income 3 0 0
Lebanon Upper middle income 1 0 0
Lithuania High income 6 1 0.3
Luxembourg High income 1 0 0
Malaysia Upper middle income 7 2 0.5
Maldives Upper middle income 1 0 0
Malta High income 3 0 0
Mexico Upper middle income 7 0 0
Moldova Lower middle income 1 0 0
Montenegro Upper middle income 1 1 0.3
Myanmar Lower middle income 2 0 0
Nepal Lower middle income 1 0 0
New Zealand High income 3 1 0.3
Nigeria Lower middle income 4 0 0
North Macedonia High income 4 0 0
Norway High income 9 3 0.8
Oman High income 3 1 0.3
Pakistan Lower middle income 4 1 0.3
Panama High income 1 0 0
Peru Upper middle income 2 0 0
Philippines Lower middle income 6 2 0.5
Poland High income 9 1 0.3
Portugal High income 10 0 0
Qatar High income 1 0 0
Romania High income 6 0 0
Russian federation Upper middle income 5 0 0
Samoa Upper middle income 1 0 0
Saudi Arabia High income 9 4 1.1
Serbia Upper middle income 3 0 0
Singapore High income 5 2 0.5
Slovakia High income 3 0 0
Slovenia High income 1 0 0
South Africa Upper middle income 6 0 0
South Korea Upper middle income 5 1 0.3
Spain High income 44 26 7
Sri Lanka Lower middle income 2 1 0.3
Sweden High income 10 1 0.3
Switzerland High income 8 1 0.3
Tanzania Lower middle income 1 1 0.3
Thailand Upper middle income 3 1 0.3
The Netherlands High income 12 3 0.8
Trinidad and Tobago High income 1 0 0
Tunisia Lower middle income 2 0 0
Turkey Upper middle income 5 1 0.3
Ukraine Lower middle income 3 0 0
United Arab Emirates High income 3 0 0
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3954 Journal of Neurology (2021) 268:3947–3960
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settings (n = 38, 10.3%). The setting was unclear in one
(0.3%) study.
Analyses ofreported service disruption, causes
ofdisruption andmitigation strategies
Service disruption
The most frequently reported disruptions occurred for
cross-sectoral service delivery for neurological disor-
ders, which was assessed in 151 of 240 studies (62.9%),
followed by emergency and acute care for neurological
disorders (n = 113, 47.1%), and treatment and care for
neurological disorders (n = 109, 45.4%). The degree of
disruption of neurological services was described in 188
studies and was most frequently classified as moderate
disruption (n = 131, 69.7%), followed by mild disruption
(n = 40, 21.3%), severe disruption (n = 10, 5.3%), and
non-disrupted (n = 7, 3.7%). Figure4 depicts the number
of studies per analyzed area of disruption, according to the
degree of disruption that they described.
Causes ofdisruption
The most frequently described reasons for service disrup-
tion were travel restrictions due to lockdowns, national
guidelines or local restriction policies (n = 196, 81.7%),
closure of inpatient and outpatient services or consulta-
tions as per health authority directive (n = 157, 65.4%),
and decrease in outpatient volume due to patients not pre-
senting (n = 135, 56.2%).
Table2 describes the main reasons for disruption and
the percentage over the total of studies assessing disrup-
tion (n = 240), disaggregated also for high- versus low- and
middle-income countries.
Table 1 (continued)
Country GNI group Number of multiple-
countries studies
Number of single-coun-
try studies
Percentage over the total
of single-country studies
United Kingdom High income 47 31 8.4
United States of America High income 114 94 25.5
Uruguay High income 1 0 0
Venezuela Lower middle income 2 0 0
Viet Nam Lower middle income 2 0 0
Zambia Lower middle income 1 1 0.3
Zimbabwe Lower middle income 1 0 0
Multiple countries NA 0 35 6.2
NA: Not applicable
Fig. 3 Neurological subspecialties studied (expressed as a proportion of all studies), broken down by all included studies versus subsamples of
studies focussing on adult and children’s populations
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3955Journal of Neurology (2021) 268:3947–3960
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Mitigation strategies
The most frequently described mitigation strategies across
224 studies were telemedicine and other telehealth formats
(n = 184, 82.1%), novel dispensing approaches for medicines
(n = 116, 51.8%), and redirection of patients (n = 95, 42.4%).
Table3 lists the different mitigation strategies and the num-
ber of studies reporting each across all studies and disag-
gregated for high- and low- and middle-income countries.
Fig. 4 Number of studies that analysed each area of disruption and the described level of disruption per study:
Table 2 Causes of service disruption described in the studies
Percentages are calculated over the 240 total studies that analyzed disruption of neurological services, and over the total number of studies that
assessed only adults (n = 184) or only children (n = 28); and over the total number of studies from high-income countries (HICs) (n = 180) or
low–middle-income countries (LMICs) (n = 30)
Reason of the disruption Number
of studies
(n = 240) (%)
Studies focused on
adults (n = 184) (%)
Studies focused on
children (n = 28)
(%)
Studies from
HICs (n = 180)
(%)
Studies from
LMICs (n = 30)
(%)
Travel restrictions hindering patient access to
health facilities
196 (81.7%) 149 (81.0%) 26 (92.9%) 146 (81.1%) 25 (83.3%)
Closure of inpatient and outpatient services or
consultations as per health authority directive
157 (65.4%) 120 (65.2%) 23 (82.1%) 114 (63.3%) 20 (66.7%)
Decrease in outpatient volume due to patients
not presenting
135 (56.2%) 113(61.4%) 13 (46.4%) 112 (62.2%) 15 (50%)
Decreased volume of patients due to cancella-
tion of elective care
109 (45.4%) 79 (42.9%) 17 (60.7%) 77 (42.8%) 11 (36.7%)
Inpatient services and or hospital beds not
available
52 (21.7%) 37 (20.1%) 7 (25.0%) 30 (16.7%) 7 (23.3%)
Clinical staff deployed and tasks shifted to
provide COVID-19 clinical management or
emergency support
40 (16.7%) 31 (16.8%) 3 (10.7%) 25 (19.2%) 5 (16.7%)
Unavailability or stock out of essential medi-
cines, medical diagnostics or other health
products at health facilities
40 (16.7%) 29 (15.8%) 3 (1.07%) 22 (12.2%) 7 (23.3%)
Insufficient PPE available for health care pro-
viders to provide services
22 (9.2%) 18 (9.8%) 1 (3.6%) 11 (6.1%) 3 (10%)
Insufficient staff to provide services due to
staff illness/quarantine
11 (4.6%) 8 (4.3%) 1 (3.6%) 5 (2.8%) 2 (6.7%)
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3956 Journal of Neurology (2021) 268:3947–3960
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Discussion
This is the first global review of the published evidence
regarding the impact the COVID-19 pandemic on the care
for people with neurological disorders and the mitigation
strategies put in place at policy, system, service level to com-
pensate for service disruptions. The number of studies that
addressed these two areas is significant but represents only
a small fraction of the total number of studies on COVID-19
and neurology published to date (> 11,000).
We conducted this review in view of existing WHO guid-
ance on maintaining essential services and surveys on ser-
vice disruption to allow for comparisons and triangulation
of results [4, 9]. Despite clear WHO guidance, this extensive
review shows that several services and areas of neurology
were affected during the pandemic with a deep impact for
the care of neurological patients across all areas of service
delivery. Service disruptions were particular prominent in
cross-sectoral service delivery and emergency and acute
neurology care, which was supported by more than 100
studies from different countries and health care system sce-
narios. Indeed, more than 75% of these studies indicated
severe disruption of essential services in acute care—the
result of the emerging impact of the first wave of pandemic
in different areas of the world. Of interest, also cross-sectoral
service delivery, treatment and investigations were affected
by the pandemic—with a different impact for patients with
chronic neurological conditions, including epilepsy, demen-
tia, neuromuscular, and neuroimmunological disorders.
With respect to causes of service disruptions, the pan-
demic, on the one hand, introduced heavy travel restrictions
for patients and sparked fears of possible infection if attend-
ing a healthcare facility—resulting in decreases of patient
volumes—reported in more than half of studies. On the other
hand, two thirds of studies indicated closure of services due
to health authorities and cancellation of elective care. Only
a minority of studies reported the need of neurological staff
being directly involved in COVID-19 clinical management
and emergency support.
Most studies described telemedicine as one of the most
important mitigation strategies adopted—but the wide
heterogeneity of reports did not allow a specific compari-
son of applicability and efficacy of different telemedicine
approaches in both acute and chronic care. About half of the
Table 3 Mitigation strategies reported in included studies
Percentages are calculated over the 224 studies that described mitigation strategies and over the total number of studies that assessed only adults
(n = 173) or only children (n = 26); and over the total number of studies from high-income countries (HICs) (n = 164) or low–middle-income
countries (LMICs) (n = 32)
Mitigation strategies Number
of studies
(n = 224) (%)
Studies focused on
adults (n = 173) (%)
Studies focused on
children (n = 26)
(%)
Studies from HICs
(n = 164) (%)
Studies from
LMICs (n = 32)
(%)
Telemedicine deployment to replace in-
person consults or other teleconsultation
formats
184 (82.1%) 140 (80.1%) 25 (96.1%) 136 (82.9%) 28 (87.5%)
Novel dispensing approaches for medicines,
novel prescribing approaches
116 (51.8%) 86 (49.7%) 18 (69.2%) 84 (51.2%) 17 (53.1%)
Redirection of patients to alternate care
sites, reorientation of referral pathways
or integration of several services into a
single visit
95 (42.4%) 74 (42.8%) 13 (50%) 68 (41.5%) 14 (43.7%)
Catch-up campaigns for missed appoint-
ments
83 (37.1%) 55 (31.8%) 18 (69.2%) 59 (36.0%) 11 (34.4%)
Triaging of neurological patients to identify
priorities
57 (25.4%) 45 (26.0%) 6 (23.1%) 42 (25.6%) 9 (28.1%)
Self-care interventions, provision of home-
based care or helplines for patients and
caregivers
84 (37.5%) 56 (32.4%) 20 (76.9% = 60 (36.6% 14 (43.7%)
Task-shifting or role delegation 44 (19.6%) 34 (19.6%) 5 (19.2%) 34 (18.3%) 4 (12.5%)
Recruitment of additional staff, novel
supply chain management and logistics
approaches
34 (15.2%) 26 (15.0%) 4 (15.4%) 27 (16.5%) 2 (6.2%)
Community communications to ensure all
citizens were aware and informed of con-
tinuity of services and that routine care
could always be sought
23 (10.3%) 15 (8.7%) 7 (26.9%) 19 (11.6%) 3 (9.4%)
Government removal of user fees 12 (5.4%) 8 (4.6%) 3 (11.5%) 9 (5.5%) 0 (0%)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

3957Journal of Neurology (2021) 268:3947–3960
1 3
reviewed studies indicated that novel approaches for drug
dispensing and care provision were implemented, such as
virtual reality-based rehabilitation or mobile app-based
monitoring of patients, but only few studies evaluated the
real impact of the mitigation strategies on patient care.
One hundred and five countries and territories are rep-
resented in the review. However, the representativeness of
the study across the globe, and even within the same coun-
try, was limited. To date, no study reported on the situa-
tion in a low-income country individually, while four high-
income countries (USA, Italy, UK and Spain) accounted
for more than 60% of all single-country studies included in
this review. This could be due to the fact that the majority
of studies focused on the first wave of the pandemic dur-
ing which these four countries were severely affected [19].
However, the underrepresentation of low- and lower-middle-
income countries hinders the analysis of the results based
on the income level of the countries. To this end, global
studies and surveys are needed to systematically assess
the effects of the pandemic and compare the results across
different resource settings in an attempt to reduce existing
health inequities. After all, what never existed cannot be
disrupted, and access to neurological services was lacking
in many countries and territories even before the pandemic.
Besides geographic differences, service disruptions and
mitigation strategies have notably varied over the course
and different waves of the pandemic [20]. So far, the most
comparable period is the first wave experienced globally by
most countries [21]. After that, the evolution of the pan-
demic followed different pathways in each country [22], so
studies accounting for a single cross-sectional evaluation
may not be fully representative of such a dynamic situation
[21]. Thus, we were not able to analyze the specific phase of
the pandemic wave that studies were evaluating. However,
in the present study, 72% of the studies had already been
published by the end of October 2020, which could be con-
sidered the end of the first wave in most territories according
to the WHO observatory [23].
For an adequate interpretation of the results, it should
be taken into account the common selective reporting bias
[24]. Indeed, the absence of evidence did not equate to the
evidence of absence [25] regarding those potentially dis-
rupted areas, but rather reflect the areas that were most fre-
quently prioritized and covered by the published studies.
Particularly, neurorehabilitation for both children and adults
deserves further investigation. Surprisingly, disruptions of
neurorehabilitation services were reported by only 39 of 240
studies. There might be several reasons for this. First, this
could be related to the different subspecialties represented in
included articles and the timing of the pandemic considered
as reporting period [26]. Many studies addressed the issue of
vascular neurology, where neurorehabilitation is a keystone
in the recovery of patients, but most studies were focused
on the disruption related to the acute phase of COVID-19,
with very limited information shared about the sub-acute and
post-acute phases of care [27]. Second, in many countries,
rehabilitation may not be considered within the neurologi-
cal sub-specialties, being part of different departments, and,
therefore, not listed within the affected areas of neurological
care, with researchers inadvertently focusing on the aspects
of care that they deliver and not always on other areas of
their multidisciplinary teamwork [28]. Third, the number
of studies that assessed pediatric population was also low,
which could also influence the underrepresentation of this
service particularly in pediatric populations.
The heterogeneous designs of the works included in this
review unfortunately precluded the comparison between the
different studies. Less than 10% of the studies were multi-
national, which also decreases the potential for comparison
between different countries and, potentially, their generaliz-
ability. There were many publications focusing on guidance
and recommendations about what to do in terms of alleviat-
ing and mitigating the disruption of the neurological ser-
vices [29, 30], but little consensus on which items should be
included in studies systematically evaluating this topic and
how the results should be presented. An important lesson
from this review is that future studies should clearly define
how representative of the studied population and territory
the data is, as well as, if possible, how the situation was
before the pandemic. In most countries and particularly so
in LMICs, neurological services were already very limited
before the pandemic [31]. In this specific case, the effects of
the pandemic might play a disrupting role on already lacking
neurological policies, systems and services and hence the
difference between before and after the pandemic may be
small, giving a false impression. The uninterrupted access
to free medication is essential for many people with neu-
rological disorders worldwide, but especially in LMICs,
health policies must ensure the access to them even during
the toughest periods of the pandemic.
Outlook andfuture recommendations
Our comprehensive approach including all types of neuro-
logical disorders and every possible area of disruption gives
a broad understanding of how neurological services in gen-
eral were disrupted by the COVID-19 pandemic. Neurologi-
cal signs/symptoms are frequent manifestations during the
acute and more chronic phases of COVID-19; hence health-
care systems must be functional to accommodate patients
with neurological disorders related or unrelated to COVID-
19 [29].
There is a need for guidance on how to evaluate disrup-
tions and which mitigation strategies should be taken. The
methodological structure and results of this review can pro-
vide a template for future studies to enhance reproducibility,
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

3958 Journal of Neurology (2021) 268:3947–3960
1 3
comparability, and generalizability of results, particularly
with regards to specific outcome measurements. This review
should also encourage researchers, public health officials
and other relevant stakeholders from LMICs to collect and
publish data on service delivery and mitigation strategies in
case of disruption to overcome data scarcity and to bring the
vulnerabilities and subsequent needs for clinical neurologi-
cal services in LMICs to the forefront of local, regional and
global decision makers. The impact of service disruption
on mortality or disability needs also further evaluation. The
mortality rates clearly exceeded these from preceding years
(2, 3), which gives an estimation of the consequences of
the pandemic; however, the total burden attributable to the
service disruption still needs specific analyses.
Conclusion
The COVID-19 pandemic has severely affected all aspects
of care of patients with neurological disorders, be it in acute,
post-acute, or long-term settings, diagnostic, therapeutic, or
rehabilitative. Most of the published evidence describes a
moderate to severe disruption of specific neurological ser-
vices. Given the large number of people living with neu-
rological conditions worldwide, this finding is devastating.
The impact of the pandemic on neurological services and
neurological disorders may be explained by travel restric-
tions for patients, fear of infections or closure of inpatient
and outpatient services as per health authority directive,
amongst others. Authors described various potential strate-
gies to mitigate the effects of the pandemic, with telemedi-
cine being the most frequently used mitigation strategy but
evidence of their effectiveness in managing neurological
disorders remains largely lacking.
Supplementary Information The online version contains supplemen-
tary material available at https:// doi. org/ 10. 1007/ s00415- 021- 10588-5.
Acknowledgements We thank the members of the WHO’s Neurology
and COVID-19 Global Forum for their valuable feedback and European
Federation of Neurological Associations for their collaboration.
Author contributions DGA: Conceptualization, data curation, formal
analysis, methodology, project administration validation, visualiza-
tion, writing of original draft. KS: Conceptualization, formal analysis,
methodology, project administration, validation, visualization, review
and editing of the manuscript. CN, DS, AP, NO, CCT and ML: Con-
ceptualization, formal analysis, methodology, project administration,
validation, visualization, review and editing of the manuscript.
Funding The World Health Organization (WHO) commissioned the
rapid review, which was conducted with no restrictions by the members
of WHO’s Neurology and COVID-19 Global Forum working group on
Essential Neurological Services, which met weekly and participated in
the design and interpretation of the results. D GA received honoraria
for the time spent reviewing all articles.
Data availability The full database is available for other researchers
upon request to the corresponding author.
Code availability The database is coded in SPSS and can be extracted
to Excel.
Declarations
Conflicts of interest DGA declares grants from the Regional Health
Administration and International Headache Society; honoraria for re-
viewing manuscripts for the review from the World Health Organiza-
tion; travel support from Teva, Lilly, Novartis and Allergan; partici-
pation in advisory board from Allergan; membership of the Spanish
Society of Neurology executive board. Only the WHO payment is
related with the present work. NO declares grants from Michael J Fox
Foundation for Parkinson’s disease research and Tertiary Education
Trust Fund (National Research Fund); payment or honoraria from In-
ternational Parkinson and Movement Disorders Society Speaker Hon-
orarium; support from International Parkinson and Movement Disor-
der Society support for attending meetings; leadership as Chairperson
of Africa Section of Steering Committee, International Parkinson and
Movement Disorder Society. DS declares grants or contracts from
National Institutes of Neurological Disorders and Stroke; national
Multiple Sclerosis Society, National Institutes of Mental Health, and
American Academy of Neurology, not related with this work; payment
honoraria for lectures for Medlink Neurology and member as Multi-
ple Sclerosis International Federation Global Access Working Group.
AP declares payment for lectures honoraria from Abbvie, Biomarin,
Chiesi, Nutricia, UCB, Zambon pharmaceuticals.
Consent for publication All authors approved the final version of the
manuscript. The manuscript underwent WHO Publication Review
Committee clearance.
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.
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3960 Journal of Neurology (2021) 268:3947–3960
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Authors and Aliations
DavidGarcía‑Azorín1 · KatrinM.Seeher2· CharlesR.Newton3 · NjidekaU.Okubadejo4 · AndreaPilotto5 ·
DeannaSaylor6 · AndreaSylviaWinkler7,8 · ChahnezCharTriki9 · MatildeLeonardi10
Katrin M. Seeher
seeherk@who.int
Charles R. Newton
Charles.newton@psych.ox.ac.uk
Njideka U. Okubadejo
nokubadejo@unilag.edu.ng
Andrea Pilotto
Andrea.pilotto@unibs.it
Deanna Saylor
Dcettom1@jhmi.edu
Andrea Sylvia Winkler
Andrea.winkler@tum.de
Chahnez Charfi Triki
Chahnezct@gmail.com
Matilde Leonardi
matilde.leonardi@istituto-besta.it
1 Headache Unit, Department ofNeurology. Hospital, Clínico
Universitario de Valladolid, Avenida Ramón y Cajal 3,
47005Valladolid, Spain
2 Department ofMental Health andSubstance Use, World
Health Organization, Geneve, Switzerland
3 Department ofPsychiatry, University ofOxford, Oxford, UK
4 Neurology Unit, Department ofMedicine, College
ofMedicine, University ofLagos, Lagos, Nigeria
5 Department ofClinical andExperimental Sciences,
Neurology Unit, University ofBrescia, Brescia, Italy
6 Department ofNeurology, Johns Hopkins University School
ofMedicine, Baltimore, MD, USA
7 Centre forGlobal Health, Department ofNeurology,
Technical University ofMunich, Munich, Germany
8 Centre forGlobal Health, Institute ofHealth andSociety,
University ofOslo, Oslo, Norway
9 Child neurology department-Hedi Chaker Hospital, LR19ES
15-Sfax University, Sfax, Tunisia
10 Neurology, Public Health, Disability Unit, Fondazione
IRCCS Istituto Neurologico Carlo Besta, Milan, Italy
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1.
2.
3.
4.
5.
6.
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