Neurosurgery and coronavirus: impact and challenges—lessons learnt from the first wave of a global pandemic

Abstract

Introduction and objectives
The novel severe acute respiratory syndrome coronavirus 2 (COVID-19) pandemic has had drastic effects on global healthcare with the UK amongst the countries most severely impacted. The aim of this study was to examine how COVID-19 challenged the neurosurgical delivery of care in a busy tertiary unit serving a socio-economically diverse population.

Methods
A prospective single-centre cohort study including all patients referred to the acute neurosurgical service or the subspecialty multidisciplinary teams (MDT) as well as all emergency and elective admissions during COVID-19 (18th March 2020–15th May 2020) compared to pre-COVID-19 (18th of January 2020–17th March 2020). Data on demographics, diagnosis, operation, and treatment recommendation/outcome were collected and analysed.

Results
Overall, there was a reduction in neurosurgical emergency referrals by 33.6% and operations by 55.6% during the course of COVID-19. There was a significant increase in the proportion of emergency operations performed during COVID-19 (75.2% of total, n=155) when compared to pre-COVID-19 (n = 198, 43.7% of total, p < 0.00001). In contrast to other published series, the 30-day perioperative mortality remained low (2.0%) with the majority of post-operative COVID-19-infected patients (n = 13) having underlying medical co-morbidities and/or suffering from post-operative complications.

Conclusion
The capacity to safely treat patients requiring urgent or emergency neurosurgical care was maintained at all times. Strategies adopted to enable this included proactively approaching the referrers to maintain lines of communications, incorporating modern technology to run clinics and MDTs, restructuring patient pathways/facilities, and initiating the delivery of NHS care within private sector hospitals. Through this multi-modal approach we were able to minimize service disruptions, the complications, and mortality.

Full text

ORIGINAL ARTICLE - INFECTION
Neurosurgery and coronavirus: impact and challenges—lessons
learnt from the first wave of a global pandemic
Keyoumars Ashkan
1,2
&Josephine Jung
1,2
&Alexandra Maria Velicu
1,2
&Ahmed Raslan
1
&Mohammed Faruque
1
&
Pandurang Kulkarni
1
&Cristina Bleil
1
&Harutomo Hasegawa
1
&Ahilan Kailaya-Vasan
1
&Eleni Maratos
1
&
Gordan Grahovac
1
&Francesco Vergani
1
&Bassel Zebian
1
&Sinan Barazi
1
&Irfan Malik
1
&David Bell
1
&Daniel Walsh
1
&
Ranjeev Bhangoo
1
&Christos Tolias
1
&Sanjeev Bassi
1
&Richard Selway
1
&Nick Thomas
1
&Christopher Chandler
1
&
Richard Gullan
1
Received: 22 September 2020 /Accepted: 12 November 2020
#The Author(s) 2020
Abstract
Introduction and objectives The novel severe acute respiratory syndrome coronavirus 2 (COVID-19) pandemic has had drastic
effects on global healthcare with the UK amongst the countries most severely impacted. The aim of this study was to examine how
COVID-19 challenged the neurosurgical delivery of care in a busy tertiary unit serving a socio-economically diverse population.
Methods A prospective single-centre cohort study including all patients referred to the acute neurosurgical service or the
subspecialty multidisciplinary teams (MDT) as well as all emergency and elective admissions during COVID-19 (18th
March 2020–15th May 2020) compared to pre-COVID-19 (18th of January 2020–17th March 2020). Data on demographics,
diagnosis, operation, and treatment recommendation/outcome were collected and analysed.
Results Overall, there was a reduction in neurosurgical emergency referrals by 33.6% and operations by 55.6% during the course
of COVID-19. There was a significant increase in the proportion of emergency operations performed during COVID-19 (75.2%
of total, n=155) when compared to pre-COVID-19 (n= 198, 43.7% of total, p< 0.00001). In contrast to other published series,
the 30-day perioperative mortality remained low (2.0%) with the majority of post-operative COVID-19-infected patients (n=13)
having underlying medical co-morbidities and/or suffering from post-operative complications.
Conclusion The capacity to safely treat patients requiring urgent or emergency neurosurgical care was maintained at all times. Strategies
adopted to enable this included proactively approaching the referrers to maintain lines of communications, incorporating modern
technology to run clinics and MDTs, restructuring patient pathways/facilities, and initiating the delivery of NHS care within private
sector hospitals. Through this multi-modal approach we were able to minimize service disruptions, the complications, and mortality.
Keywords Coronavirus .Emergency referrals .Neurosurgery .Pandemic
Introduction
King’s College Hospital NHS Foundation Trust (KCH), built
in 1840, is one of the largest teaching hospitals in the UK,
serving a local inner-city population of 700,000 in the London
districts of Southwark and Lambeth. The tertiary neurosurgi-
cal service is amongst the busiest in the country covering a
regional catchment population of approximately 4 million
across South East London and the county of Kent [13].
The local London boroughs have a multi-ethnic population
with a comparatively high proportion of Black people
(25.9%), compared to the whole London (10.9%). Amongst
the largest ethnic minority groups are Black African (16.1%)
and Black Caribbean (8.0%). Approximately half of the local
population identifies as White British (52.2%), much lower
than the national average. The socio-economic profile of the
local population shows the lowest level of employment
amongst all London districts [16,21].
This article is part of the Topical Collection on Infection
*Josephine Jung
Josephine.Jung@nhs.net
1
Department of Neurosurgery, King’s College Hospital, Denmark
Hill, London SE5 9RS, UK
2
Neurosciences Clinical Trials Unit, King’s College Hospital,
London, UK
https://doi.org/10.1007/s00701-020-04652-8
/ Published online: 21 November 2020
Acta Neurochirurgica (2021) 163:317–329
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The novel severe acute respiratory syndrome coronavirus 2
(COVID-19) pandemic had a drastic effect on global
healthcare and Europe was at the epicentre of the pandemic
from March to May 2020. The UK had one of the highest
death tolls across Europe and London was the worst affected.
KCH had at its peak 517 inpatients with COVID-19 of which
96 were being cared for in the intensive treatment unit (ITU).
The GlobalSurg group recently published that surgical ser-
vices, both elective and emergency, were severely impacted
by COVID-19 and that there was an increased 30-day mortal-
ity of up to 23.8% in patients infected with COVID-19 [2].
The aim of the paper here was to examine specifically the
impact of the COVID-19 pandemic on the neurosurgical de-
livery of care in a busy unit serving a socio-economically
challenging population. We also examined the patient out-
comes as well as described the strategies adopted to allow safe
delivery of neurosurgical services.
Methods
Study design
On 18th March 2020, our unit entered the acute “COVID-19”
phase, demarcated by the day of the first pre-operatively
suspected COVID-19 infection in a neurosurgical patient,
and when neurosurgical rota and service changes were
adopted. The phase officially ended on 15th May (59 days
later) when our hospital, in line with the NHS directive, en-
tered the recovery phase. During the COVID-19 period, data
were collected prospectively on all patients referred to the
acute neurosurgical service, patients who were admitted elec-
tively, and patients referred to subspecialty multidisciplinary
teams (MDT). These data were then compared to those ob-
tained in the immediately preceding 59-day period (18th
January to 17th March), the “pre-COVID-19”,toassessthe
impact of the pandemic. The manuscript was written follow-
ing the Strengthening the Reporting of Observational Studies
in Epidemiology (STROBE) checklist [24].
Data collection and outcome measures
Data on the acute neurosurgical referrals were obtained
through an online Patient Care System (PCS) and data on
referrals to the MDTs were obtained from the relevant coor-
dinators. Emergency and elective operating lists were sourced
through the software “Galaxy Operating Theatres”.Electronic
patient records were accessed to capture the following: age,
gender, diagnosis, type of procedure (emergency vs. elective,
adult vs. paediatric, cranial vs. spinal), subspecialty (function-
al, neuro-oncology, trauma, neurovascular, skull base, spinal,
paediatric neurosurgery), COVID-19 infection (pre-operative-
ly vs. post-operatively), and post-operative complications. For
COVID-19-infected patients, data on ethnicity, co-morbid-
ities, perioperative complications, ITU/hospital stay, dis-
charge destination, and mortality were also included.
Additionally, referral data included type of referral (new vs.
follow-up), pathology, MDT outcome, and treatment delay/
recommendation.
Rota change, guidelines, and operating theatre
adjustments
Rota and service provision changes were put in place during
the pandemic on 18th of March 2020. Given the rapidly
evolving Public Health England [20], NHS England [15],
and the Society of British Neurological Surgeons guidelines
[22], a local KCH Neurosurgery working group was
established to actively review the evidence and synthesize a
Guidance [12] for adjustments to elective and emergency op-
erations, theatre ventilation, and use of personal protective
equipment (PPE).
KCH had its first two COVID-19-positive patients on 04th
of March 2020 (Fig. 1—day 0) and reached its peak on the 8th
of April 2020 with 517 COVID-19-positive inpatients of
which 96 were in ITU. The first change to our neurosurgical
practice was put in place on 18th March 2020 where the rota
was revised from a subspecialty team-based system
(consisting of 1–2 neurosurgical trainees working for a specif-
ic consultant) to a twilight rota with 1 “green”team (no
COVID-19 patient contact), 1 “red”team (COVID-19-posi-
tive/suspected patient contact), and 1 stand-by team in case
other team members fell ill and had to consequently self-iso-
late. Consultant and trainee rotas both switched to a 24-h shift
with one on-site consultant at all times and another on-call in
reserve.
The three daily elective operating lists were condensed into
one list per day from the 23rd of March 2020. Throughout the
pandemic, one emergency neurosurgical theatre remained ac-
tive. The allocation of theatre resources was undertaken by the
Executive board of the hospital. The neurosurgical lists were
arranged/triaged by the on-call neurosurgery consultant on the
day. Trust guidelines recommended that ventilation in both
laminar flow and conventionally ventilated theatres should
remain fully switched on during surgical procedures where
patients may have COVID-19 infection. All operations were
performed with full PPE, including either FFP3 mask (for
aerosol-generating procedures) or fluid-resistant mask (non-
aerosol-generating procedures), hat, visor, gloves and fluid-
resistant disposable gown. Staff training for proper donning
and doffing was mandatory.
Our inpatient neurosurgical service usually consists of one
purely elective 31-bedded ward, three wards for emergency
and additional elective neurosurgical patients (~ 50–60 beds),
and one dedicated 12-bedded neurosurgery high dependency
unit (HDU). During COVID-19, out of these, one emergency
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admission ward and its adjacent HDU were closed to neuro-
surgery admissions to provide capacity for the hospital’sgen-
eral COVID-19 patients. The HDU was relocated to replace
one of the other neurosurgical wards with level 2 bed numbers
expanded to 32. The remaining two neurosurgical wards were
divided into “dirty”(COVID-19 positive) and “clean”(non-
COVID-19) wards (Fig. 2).
Nearly all face-to-face outpatient appointments were can-
celled and essential appointments were conducted via phone
consultations. The MDT referral process remained un-
changed; however, meetings took place virtually via
Microsoft® Teams (Redmond, USA) from 01st April 2020.
Statistical analysis
Descriptive statistics were used to characterize the patient
population. Statistical analysis was performed using
GraphPad Prism V7. Chi-squared test and the Mann-
Fig. 2 Flowchart describing admission pathway for patients requiring urgent
treatment during COVID-19. All neurosurgical patients were swabbed for
COVID-19 upon arrival at KCH. If urgent surgery was required, they were
taken to theatre and treated as COVID-19 positive until the test result was
available. If urgent surgery was not required, they were isolated in a side room
in a dedicated holding ward until the COVID-19 test result was available and
then either cared for in a COVID-19-positive ward or allocated to a COVID-
19-negative ward based on the results
Fig. 1 This graph describes the
number of patients admitted to
our hospital with COVID-19
infection. Overall number of
inpatients is depicted in black,
and the number of patients in
intensivecareisprovidedingrey.
Day 0 was the 04th of
March 2020
319Acta Neurochir (2021) 163:317–329
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Whitney Utest were used to assess the statistical significance
of observed differences between cohorts before and during the
COVID-19 pandemic.
Results
Emergency referrals during COVID-19
Pre-COVID-19, the median number of new acute referrals
was 31 (range 17–45) per 24 h. During COVID-19, this de-
creased to 21 (range 10–34) per day. There was a statistically
significant reduction in the overall number of referrals from
1847 to 1227 (Table 1;p<0.05).
Subspecialty emergency referrals changed to proportion-
ately fewer skull base and spinal referrals, but proportionately
increased trauma, vascular, oncology, and paediatric referrals
(Table 1;p< 0.01). Approximately 10% of patients referred as
an emergency pre-COVID-19 (n= 190) and during COVID-
19 (n= 119) were accepted for emergency transfer. There was
no change to the definition of what constituted an emergency
during or pre-COVID-19, namely being a condition that was
life or limb threatening within a matter of days if left untreat-
ed. There was no significant change in the proportion of pa-
tients with neurological deficit, GCS ≤8, or age > 65 years
being transferred to our neurosurgical centre (p>0.05).
In fact, there was no statistically significant difference in
age amongst patients that were admitted pre-COVID-19 (me-
dian age 53 (range 0–92) years) and during COVID-19 (me-
dian age 51 (range 0–89) years. There was however a change
in gender of patients admitted pre-COVID-19 and during
COVID-19 with proportionately more males being admitted
during COVID-19 (59.67% compared to 52.31% pre-
COVID-19, p< 0.05). This may potentially reflect the gener-
ally more health averse and risk-prone occupational and non-
occupational behaviour amongst men resulting in acute ad-
missions. The distribution of ethnic minority patients admitted
pre-COVID-19 (8.15% Black, 3.94% Asian, 0.41% Hispanic)
and during COVID-19 (9.54% Black, 3.54% Asian, 0.54%
Hispanic) remained stable, albeit in a higher proportion of
patients the ethnicity was not recorded during COVID-19
(24.73% pre-COVID-19, 36.24% during COVID-19), possi-
bly reflecting the limited availability of hospital administrative
support staff to record these during COVID-19.
Emergency and elective neurosurgical operations
performed before and during COVID-19
The total number of operations decreased from n= 453 (pre-
COVID-19) to n= 206 (Table 1;p< 0.0001) with the daily
median number of operations decreasing from 8 to 3. A higher
percentage of emergency operations was performed during
COVID-19 (75.2% of total, n= 155) compared to pre-
COVID-19 (n= 198, 43.7% of total, p< 0.00001). There
was no significant change in the proportion of cranial versus
spinal operations (Table 1). Overall, significantly fewer pa-
tients aged > 65 years underwent an operation during
COVID-19 (p< 0.01). The operations for adults and paediat-
rics per neurosurgical subspecialty changed significantly (p<
0.01) with subspecialties with a high proportion of elective
work, such as functional, skull base, and spinal neurosurgery,
being affected the most.
Tables 2and 3summarize the data on patients undergoing
neurosurgery in adult and paediatric cases, respectively. The
total number of adult operations performed dropped from n=
408 to n= 173 during COVID-19, with a significant amount
of functional and degenerative spinal neurosurgical work be-
ing deferred or cancelled (p<0.01;Table2). The number of
operations amongst the emergency subspecialties, such as
trauma and vascular neurosurgery, also decreased during
COVID-19 by approximately 50%; however, the case mix
remained similar. The most common traumatic pathologies
requiring emergency operation were chronic subdural hema-
toma (pre-COVID-19 n= 26, COVID-19 n=19),vertebral
fracture (pre-COVID-19 n= 11, COVID-19 n=5),andacute
subdural hematoma (pre-COVID-19 n= 9, COVID-19 n=3).
Although all the numbers decreased, the smallest drop in cases
was amongst surgeries for chronic subdural haematomas, pos-
sibly related to their relatively more chronic presentation.
Similarly, vascular operations decreased with fewer aneu-
rysms being clipped during COVID-19 (n=1)comparedto
pre-COVID-19 (n=9).
Within the neuro-oncology service, the overall number of
operations decreased from n=60(14.7%oftotal)ton=31
(17.9% of total) during COVID-19. Similarly, the number of
craniotomies for high-grade gliomas decreased from n=31
(7.6% of total) to n= 12 (6.9% of total) during the pandemic.
Our skull base service was severely affected during
COVID-19 with only 3 operations for pituitary adenoma/
apoplexy being performed during COVID-19 (1.7% of total)
from a previous number of 16 operations pre-COVID-19
(3.9% of total). No operations for trigeminal neuralgia, vestib-
ular schwannoma, or chiari malformation were performed
during COVID-19.
In functional neurosurgery, no new implantations for deep
brain stimulation (DBS), spinal cord stimulation, or occipital
nerve stimulation were performed. The battery change service
for patients with movement disorders, however, continued
albeit in the day case setting (DBS battery change n=5in
both periods). All spinal surgeries decreased during COVID-
19; however, notably, operations for cauda equina syndrome
(pre-COVID-19 n=26,COVID-19n= 14) and myelopathies
(pre-COVID-19 n=28,COVID-19n=8)werereducedby≥
50% during COVID-19, whereas operations within spinal on-
cology category remained stable (pre-COVID-19 n=14,
COVID-19 n=15).
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Neurovascular referral service
The total number of referrals to the vascular MDT decreased
from n=245ton= 161 during COVID-19 (p<0.05).The
total number of patients referred with an intracranial aneurysm
decreased from n= 185 (75.5% of total pre-COVID-19) to n=
132 (82.0% of total during COVID-19; Table 4). Within that
group, referred unruptured symptomatic aneurysms remained
approximately stable (~ 2.5 of total). The number of AVMs
referred decreased from n= 34 (13.9% of total pre-COVID-
19) to n= 8 (5.0% of total during COVID-19).
Sixteen patients underwent emergency treatment pre-
COVID-19, 6 of those underwent open surgery and 10
underwent endovascular treatment. During COVID-19, only
Table 1 Characteristics of
emergency referrals and
operations
Period Pre-COVID-19 COVID-19 pvalue
Emergency referrals, total (%) 1847 (100.0) 1227 (100.0) p<0.01
Trauma/vascular 956 (51.8) 656 (53.5)
Oncology 210 (11.4) 171 (13.9)
Skull base 36 (1.9) 12 (1.0)
Spinal 428 (23.2) 229 (18.7)
Paediatrics 75 (4.1) 59 (4.8)
Other* 141 (7.6) 100 (8.1)
Emergency transfer, total (%) 190 (100.0) 119 (100.0) p>0.05
Neurological deficit 92 (48.4) 55 (46.2)
GCS
a
≤8 12 (6.3) 10 (8.4)
Age > 65 years 42 (22.1) 21 (17.6)
Surgery, total (%) 453 (100.0) 206 (100.0)
Emergency 198 (43.7) 155 (75.2) p< 0.00001
Elective 255 (56.3) 51 (24.8)
Cranial 263 (58.1) 134 (65.0) ns
Spinal 190 (41.9) 72 (35.0)
Adult 408 (90.1) 173 (84.0) p<0.05
Paediatric 45 (9.9) 33 (16.0)
Age at operation (years) p>0.05
Mean ± SD 50 ± 21 47 ± 22
Range 0–92 0–86
Operative age groups (years) p<0.01
0–17 44 33
18–65 292 178
>65 117 41
COVID-19 infection
Pre-operatively 0 4
Post-operatively (during inpatient stay) 7 6
Mortality, total (% of operations) 5 (1.1) 4 (2.0)
30-day perioperative (emergencies) 5 (2.5) 3 (1.9)
30-day perioperative (electives) 0 (0.0) 1 (2.2)
Operations per subspecialty (adult and paediatric) p<0.01
Trauma/vascular 75 (16.6) 44 (21.4)
Oncology 67 (14.8) 40 (19.4)
Skull base 37 (8.2) 8 (3.9)
Spinal 149 (32.9) 55 (26.7)
Functional 43 (9.5) 8 (3.9)
Other* 82 (18.1) 51 (24.8)
*Emergency referrals and operations for other reasons such as hydrocephalus and infection were excluded from
statistic calculation
a
Glasgow coma scale
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Table 2 Number and
composition of adult operations
performed by subspecialty
Adult Pre-COVID-19 COVID-19 pvalue
Number of operations in N(% of total) 408 (100.0) 173 (100.0)
Functional 37 (9.1) 8 (4.6) p<0.01
DBS
a
for Parkinson’s disease/tremor 8 (2.0) 0 (0.0)
Intractable epilepsy/VNS
b
18 (4.4) 1 (0.6)
Peripheral nerve 3 (0.7) 1 (0.6)
Baclofen pump/other 2 (0.4) 1 (0.6)
DBS battery change 5 (2.7) 5 (2.9)
Spinal 145 (35.5) 51 (29.5) p<0.01
Myelopathy 28 ( 6.9) 8 (4.6)
Radiculopathy 73 (17.9) 13 (7.5)
Cauda equina syndrome 26 (6.4) 14 (8.1)
MSCC
d
and spinal tumour 14 (3.4) 15 (8.7)
Spinal haematoma and other 4 (1.0) 1 (0.6)
Trauma 50 (12.3) 31 (17.9) p>0.05
Acute subdural hematoma 9 (2.2) 3 (1.7)
Chronic subdural hematoma 26 (6.4) 19 (11.0)
Extradural hematoma 4 (1.0) 2 (1.2)
Traumatic brain injury/other 0 (0.0) 1 (0.6)
Traumatic vertebral fracture 11 (2.7) 5 (2.9)
Vascular 22 (5.4) 9 (5.2) p>0.05
Aneurysm 9 (2.2) 1 (0.6)
Intracranial haemorrhage 5 (1.2) 5 (2.9)
Ischemic stroke 1 (0.2) 1 (0.6)
Arteriovenous malformation 7 (1.7) 0 (0.0)
Arteriovenous fistula 1 (0.2) 2 (1.2)
Oncology 60 (14.7) 31 (17.9) p>0.05
Low-grade glioma 4 (1.0) 1 (0.6)
High-grade glioma 31 (7.6) 12 (6.9)
Cerebral metastasis 6 (1.5) 6 (3.5)
Meningioma 13 (3.2) 7 (4.0)
Other 6 (1.5) 5 (2.9)
Skull base 36 (8.8) 7 (4.0) p>0.05
Pituitary adenoma/apoplexy 16 (3.9) 3 (1.7)
Sphenoid wing meningioma 5 (1.2) 2 (1.2)
Vestibular schwannoma 6 (1.2) 0 (0.0)
Chiari malformation 5 (1.2) 0 (0.0)
Chondrosarcoma 2 (0.5) 0 (0.0)
Trigeminal neuralgia 1 (0.2) 0 (0.0)
Craniopharyngioma 1 (0.2) 2 (1.2)
Other 58 (14.2) 37 (21.4) p>0.05
Hydrocephalus 30 (7.4) 18 (10.4)
Primary infections 7 (1.7) 4 (2.3)
Secondary infections 15 (3.7) 11 (6.4)
Post-operative hematoma 2 (0.5) 0 (0.0)
CSF leak/pseudomeningocele 4 (1.0) 4 (2.3)
a
Deep brain stimulation
b
Vagal nerve stimulator
c
Metastatic spinal cord compression
d
Cerebrospinal fluid
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1 patient underwent emergency open surgery and 17 patients
underwent emergency endovascular treatment. All elective
surgery was halted during COVID-19 (Table 4).
Neuro-oncology and skull base referral service
The total number of referrals to the neuro-oncology MDT
decreased from n=443ton= 275 during COVID-19 (p<
0.05) with the median number of referrals per MDT dropping
from 53 ± 11.63 to 37 ± 9.58. There was no significant change
in the ratio of new to follow-up referrals during these periods.
Equally, there was no significant change in the treatment rec-
ommendation provided for patients with high-grade gliomas
(HGG), low-grade gliomas (LGG), and cerebral metastases
(CM) (p>0.05;Table5). However, there was a significant
treatment delay (surgery or adjuvant therapy), n= 4 patients
(0.9% of total) pre-COVID-19 versus n=32patients(11.6%
of total, p< 0.00001) during COVID-19, with patients with a
meningioma affected more severely (n=16overall)compared
to patients with gliomas or malignant tumours (n= 7 HGG, n
= 2 LGG, n= 3 CM). The most common reasons for treatment
delay were surgery delay due to COVID-19 because of re-
source limitations (n= 26), secondly unrelated reasons (n=
7), patient preference due to fear of infection (n= 2) and
chemotherapy delay due to COVID-19 (n=2).
Within the skull base service, the number of referrals was
significantly reduced from n=329ton= 101 during COVID-
19 (p< 0.001). Notably, the overall number of patients referred
for a pituitary adenoma reduced from n=80ton=31(p<
0.001). Out of those, n= 11 were referred with pituitary apo-
plexy pre-COVID-19 and n= 3 during COVID-19. There was
no statistically significant difference in treatment recommenda-
tion between patients referred pre-COVID-19 and during
COVID-19 for patients with vestibular schwannoma and pitu-
itary adenoma/apoplexy. However, in a higher proportion of
patients referred with a meningioma during COVID-19, active
treatments such as surgery or SRS, instead of monitoring were
recommended, possibly indicating that larger or more clinically
symptomatic lesions were being referred during the COVID-19
period (p< 0.05; Table 5). All meningioma cases, where spe-
cialist intervention was recommended, were located in the me-
dial sphenoid wing. Surgery was recommended to 3 patients
with pituitary adenomas during COVID-19: 1 had pituitary
apoplexy, 1 had progressively deteriorating vision, and in 1
patient, the pituitary mass had progressed over a short period
of time and turned out to be a metastasis. Surgical intervention
was deferred in n= 5 for sphenoid wing meningiomas, and n=
15 for pituitary adenoma.
Referrals to the spinal MDT
The total number of referrals to the spinal MDT decreased
significantly during COVID-19 from n=526ton=248(p
< 0.001; Table 4). The proportion of patients referred with
Table 3 Number and
composition of paediatric
operations performed by
subspecialty
Paediatric Pre-COVID-19 COVID-19 pvalue
Number of operations in N(% of total) 45 (100.0) 33 (100.0)
Functional (intractable epilepsy) 6 (13.3) 0 (0.0)
Spinal 4 (8.9) 4 (12.1) p>0.05
Myelomeningocele 3 (6.7) 4 (12.1)
Tethered cord 1 (2.2) 0 (0.0)
Trauma 2 (4.4) 5 (15.2) p>0.05
Acute subdural hematoma 0 (0.0) 1 (3.0)
Extradural hematoma 1 (2.2) 0 (0.0)
Traumatic brain injury/intracranial haemorrhage 0 (0.0) 3 (9.1)
Traumatic vertebral fracture 1 (1.1) 1 (3.0)
Vascular (cavernoma) 1 (2.2) 0 (0.0)
Oncology 7 (15.6) 9 (27.3) p>0.05
LGG 1 (2.2) 4 (12.1)
HGG 5 (11.1) 2 (6.1)
Medulloblastoma 1 (2.2) 2 (6.1)
Ependymoma 0 (0.0) 1 (3.0)
Skull base (chiari malformation) 1 (2.2) 1 (3.0)
Other 24 (53.3) 14 (42.4) p>0.05
Hydrocephalus 20 (44.4) 14 (42.4)
Primary infections 2 (4.4) 0 (0.0)
Secondary infections 2 (4.4) 0 (0.0)
323Acta Neurochir (2021) 163:317–329
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cauda equina syndrome increased significantly from 4.0% (n
= 21) to 10.5% (n=26,p< 0.001). There was no statistically
significant difference between spinal MDT treatment recom-
mendations before and during COVID-19 (Table 4).
Functional and paediatric neurosurgery
The number of functional neurosurgery MDTs was reduced
from twice-weekly pre-COVID-19 to 3 during COVID-19.
No elective functional neurosurgery took place during
COVID-19 although battery replacement for movement dis-
order patients continued (Table 2).
In the paediatric service, the total number of operations
performed was not as severely affected as the adult service
(pre-COVID-19 n= 45, during COVID-19 n=33)butthe
case load amongst the subspecialties changed (Table 3). In
particular, trauma cases increased from n= 2 (4.4% of total
pre-COVID-19) to n= 5 (15.2% of total during COVID-19).
Oncology operations also increased from n= 7 (15.6% of
total) to n= 9 (27.3% of total) during COVID-19. No func-
tional or neurovascular operations were performed during
COVID-19 within our paediatric cohort.
Surgical outcomes and COVID-19 infections in neuro-
surgical patients
Overall, 30-day perioperative mortality remained low during
COVID-19 (n= 4, 2.0%) compared to pre-COVID-19 (n=5,
Table 4 Referrals to
neurovascular and spinal
multidisciplinary teams
Period Pre-COVID-19 COVID-19 pvalue
Vascular referral age groups (years) p<0.01
0–17 7 5
18–65 183 97
>65 55 59
Vascular diagnosis, total (%) 245 (100.0) 161 (100.0) p<0.01
Aneurysm(s) 185 (75.5) 132 (82.0)
Previously ruptured 79 (32.2) 22 (13.7)
Unruptured symptomatic 6 (2.4) 4 (2.5)
Unruptured incidental 100 (40.8) 106 (65.8)
AVM
a
34 (13.9) 8 (5.0)
Previously ruptured cranial 12 (4.9) 1 (0.6)
Unruptured cranial 20 (44.4) 7 (4.3)
Spinal 2 (0.8) 0 (0.0)
Cavernoma 1 (0.4) 5 (3.1)
Other* 25 (10.2) 17 (10.6)
Vascular treatment
Emergency, clip/coil 6/10 1/17 p>0.05
Ruptured or dissecting intracranial aneurysm 4/6 1/13
Ruptured or symptomatic AVM
a
or AVF
b
2/4 0/4
Elective, clip/coil 8/9 0/0
Intracranial aneurysms 5/8 0/0
AVM
a
or AVF
b
3/1 0/0
Spinal MDT
c
referrals, total (%) 526 (100.0) 248 (100.0) p<0.001
Cauda equina syndrome 21 (4.0) 26 (10.5)
Degenerative spine 505 (96.0) 222 (89.5)
Spinal treatment recommendation (% of total) p>0.05
Routine outpatient 334 (63.5) 151 (60.9)
Urgent outpatient 24 (4.6) 7 (2.8)
Conservative or other 168 (31.9) 90 (36.3)
*Intracranial haemorrhage—noabnormality, non-aneurysmal subarachnoid haemorrhage, stenosis, family history
a
Arteriovenous malformation
b
Arteriovenous fistula
c
Multidisciplinary team
324 Acta Neurochir (2021) 163:317–329
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Table 5 Referrals to neuro-
oncology and skull base
multidisciplinary teams
Period Pre-COVID-19 COVID-19 pvalue
Neuro-oncology diagnosis, total (%) 443 (100.0) 276 (100.0) p>0.05
New referrals 298 (67.3) 185 (67.0)
High-grade glioma 65 (14.7) 33 (12.0)
Low-grade glioma 22 (5.0) 9 (3.3)
Cerebral metastasis 80 (18.1) 60 (21.7)
Meningioma 59 (13.3) 37 (13.4)
Other* 72 (16.3) 46 (16.7)
Follow-up (including post-operative) 145 (32.7) 91 (33.0)
High-grade glioma 34 (7.7) 26 (9.4)
Low-grade glioma 11 (2.5) 8 (2.9)
Cerebral metastasis 41 (9.3) 32 (11.6)
Meningioma 35 (7.9) 17 (6.2)
Other* 24 (5.4) 8 (2.9)
Treatment recommendation
High-grade glioma, total 99 59 p>0.05
Surgery, % 32 (32.3) 12 (20.3)
Monitoring, conservative or other, % 67 (67.7) 47 (79.7)
Low-grade glioma, total 33 17 p>0.05
Surgery, % 6 (18.2) 4 (23.5)
Monitoring, conservative or other, % 27 (81.8) 13 (76.5)
Cerebral metastasis, total 121 92 p>0.05
Intervention (surgery/SRS
a
), % 30 (7/23) (24.8) 32 (6/26) (34.8)
Monitoring, conservative or other, % 91 (75.2) 60 (65.2)
Skull base diagnosis, total (%) 329 (100.0) 101 (100.0) p<0.05
New referrals 112 (34.0) 48 (47.5)
Meningioma 25 (7.6) 14 (13.9)
Vestibular schwannoma 17 (5.2) 7 (6.9)
Pituitary adenoma and/or apoplexy 29 (8.8) 14 (13.9)
Chiari malformation 11 (3.3) 2 (2.0)
Other
&
30 (9.1) 11 (10.9)
Follow-up (incl. post-operative) 217 (66.0) 53 (52.5)
Meningioma 68 (20.7) 20 (19.8)
Vestibular schwannoma 56 (17.0) 10 (9.9)
Pituitary adenoma and/or apoplexy 51 (15.5) 17 (16.8)
Chiari malformation 3 (0.9) 0 (0.0)
Other
&
39 (11.9) 6 (5.9)
Treatment recommendation
Meningioma, total 93 34 p<0.05
Intervention (surgery/SRS
a
), % 9 (5/4) (9.7) 9 (7/2) (26.5)
Interval imaging, % 84 (90.3) 25 (73.5)
Vestibular schwannoma, total 73 17 p>0.05
Intervention (surgery/SRS
a
), % 9 (6/3) (12.3) 2 (1/1) (11.8)
Interval imaging, % 64 (87.7) 15 (88.2)
Pituitary adenoma/apoplexy, total 80 31 p>0.05
Surgery, % 16 (20.0) 3 (9.7)
Interval imaging, % 64 (80.0) 28 (90.3)
*Ependymoma, nerve sheath tumour, haemangioblastoma, arachnoid/colloid cyst, etc.
a
Stereotactic radiosurgery
&
Chondrosarcoma, chordoma, craniopharyngioma, etc.
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1.1%; Table 1). Within emergency operations, 30-day periop-
erative mortality was lower during COVID-19 (1.9%, n=3)
compared to pre-COVID-19 (2.5%, n= 5), partly reflecting
the process of patient selection with higher threshold for trans-
fer and surgery in critically ill patients during the COVID-19
period. The single elective mortality in the COVID-19 period
related to a 28-year-old patient with a solitary CM who sub-
sequently passed away due to leptomeningeal disease
(Table 1; 30-day perioperative elective mortality during
COVID-19 n=1,2.2%).
There were 17 neurosurgical patients who were diagnosed
with COVID-19 either pre-operatively (n=4)orpost-
operatively (operation pre-COVID-19 n= 7, operation during
COVID-19 n= 6; all patients tested negative before surgery;
Table 1), representing 2.6% of total neurosurgical operations.
Out of these 17 patients, 6 (35.3%) were from a black and
minority ethnic (BAME) background (Table 6) and one of
these BAME patients died of post-operative COVID-19 infec-
tion (accounting for 20.0% of all deaths after emergency op-
eration). This was an 86-year-old Asian man with hyperten-
sion who underwent burr hole drainage of a chronic subdural
hematoma but developed COVID-19 infection 15 days post-
operatively and died 6 days later of COVID-19-related pneu-
monia. This was the only single mortality of a neurosurgical
patient with COVID-19 infection within our cohort. There
was no difference in the ethnic mix of our patients between
the pre-COVID and COVID periods. The median age
amongst these 17 patients was 63 ± 15.44 years and
male:female ratio was 10:7. Overall, n= 4 patients (23.5%)
were admitted to ITU because of COVID-19-related compli-
cations. The majority of patients who were infected with
COVID-19 had underlying co-morbidities such as hyperten-
sion and diabetes mellitus, and all patients admitted to ITU
had underlying health problems. Out of the 13 patients who
developed post-operative COVID-19 infection, 53.8% (n=7)
had suffered from a post-operative complication (n= 6 wound
infection, n= 1 hematoma, n= 1 CSF leak) with a median
time to post-operative infection of 18 ± 9.5 days. The median
length of stay for the 17 patients diagnosed with COVID-19
was 36 ± 23.97 days; 4 (23.5%) were discharged to a rehabil-
itation unit, and 11 (64.7%) were discharged home.
Discussion
Impact of COVID-19 on neurosurgical referrals and
service
Overall, we saw a reduction in acute referrals during COVID-
19 by approximately 33.6% and in the number of operations
performed by approximately 55.6%. This is comparable to the
published literature where a reduction of more than 50% has
been described by 226 respondents from more than 60
countries [9]. Mathiesen et al. demonstrated in a European
snapshot that in 80% of respondents (20 neurosurgical depart-
ments), neurosurgical beds and neuro-intensive care beds
were rationalized by postponing elective surgery, fewer acute
traumatic brain injuries and subarachnoid haemorrhages ad-
missions, and changing surgical indications in order to ration
resources [14]. Although we did not see a statistically signif-
icant difference in patients with neurological deficit, GCS ≤8,
or age > 65 years being transferred to our neurosurgical unit
during COVID-19, there was a trend towards admitting fewer
elderly patients with depressed GCS. This may represent the
tendency to protect the ventilated ITU bed capacity by limit-
ing the admission of patients with extremely poor prognosis.
Additionally, referrals to our neurosurgical subspecialist
MDTs were decreased although subspecialties with a more
elective case mix (skull base, spine, functional) were worse
affected than those with a more urgent case mix (neuro-oncol-
ogy, neurovascular, paediatrics).
Hecht et al. described a similar percentage reduction for
neurosurgical emergency admissions although across all sub-
specialties (p= 0.0007) during COVID-19 [6]. In keeping
with their findings, we observed a reduction in the total num-
bers of patients presenting with sub-/epidural hematomas,
traumatic vertebral fractures, and hydrocephalus (as described
in Table 2). Interestingly, operations for cauda equina syn-
drome and spinal myelopathy decreased during COVID-19,
which could be either due to a delay in presentation to the
emergency department (patient-related factors) or due to a
delay in referral through the general practitioner as many
had their practice disrupted during COVID-19 (physician-re-
lated factors). In contrast though, we observed a similar num-
ber of patients with neurovascular emergencies (i.e. ruptured
intracranial aneurysm) presenting during and pre-COVID-19
with a higher proportion undergoing endovascular treatment
during COVID-19; the treatment decision was not based on
resource allocation but was merely a result of the type of
aneurysms presenting during the COVID-19 period.
However, this also helped to reduce theatre usage and length
of hospital stay.
Although there was a reduction in the referrals to our sub-
specialist MDTs, we developed strategies to avoid critical
delays. For example, in neuro-oncology, we actively reached
out to our referring centres to encourage continued referral of
patients. Importantly, there was no significant change in treat-
ment recommendation with regard to gliomas and CMs in our
cohort (p> 0.05; Table 5). In terms of delivery of surgery, we
mitigated the effects of reduced theatre space during COVID-
19 in our unit by securing additional theatre capacity in the
private healthcare sector, contracted through the NHS. This
also meant that the operations performed during COVID-19 in
the private sector (n= 26) were provided by a “clean”neuro-
surgical team to a “clean”(COVID-19 negative) cohort of
neuro-oncology patients, further reducing the risks. Similar
326 Acta Neurochir (2021) 163:317–329
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Table 6 Characteristics of neurosurgical patients with COVID-19 infection
Nr. Age, sex Ethnic group Admission Co-morbidities Diagnosis Procedure Complications ITU Outcome LoS
Type COVID
1 54, M White Em d0 HTN Pineal lesion Endoscopic third
ventriculostomy + biopsy
None Yes Home 46 days
2 38, M Black Em d0 Illicit drugs Subarachnoid haemorrhage External ventricular drain None Yes Home 15 days
3 54, M White Em d0 Pancytopaenia Colloid cyst Endoscopic resection None No Home 27 days
4 41, M White Em d0 HTN, NIDDM, asthma Intracranial haemorrhage Craniotomy None Yes Home 55 days
5 59, M White Elec d16 Metastatic cancer Cerebral metastasis Craniotomy None No Home 24 days
6 67, M White Em d34 HTN, NIDDM, Cholesterol↑Meningitis External ventricular drain None Yes Rehab 90 days
7 51, M White Em d20 None Degenerative spine Lumbar fixation Cerebrospinal fluid leak,
wound infection
No Home 36 days
8 72, M White Elec d31 None Parkinson’s Deep brain stimulation Wound infection No Inpatient 94 days
9 72, F Asian Elec d42 HTN, NIDDM Meningioma Craniotomy Wound infection No Home 65 days
10 86, M Asian Em d15 HTN, dementia Subdural hematoma Burr hole evacuation None No RIP 21 days
11 64, F White Em d14 None Meningioma Craniotomy/cranioplasty Wound infection No Rehab 29 days
12 86, F White Em d18 HTN, AF, cholesterol↑Spinal hematoma Decompression Wound infection Yes Rehab 31 days
13 48, F Black Elec d21 Asthma, cholesterol↑Meningioma Craniotomy Haematoma Yes Rehab 67 days
14 66, M White Em d14 Metastatic cancer Metastatic cord compression Decompression + fixation None No Home 22 days
15 33, F Hispanic Elec d11 None High-grade glioma Craniotomy Wound infection No Home 23 days
16 81, F Black Em d11 HTN, NIDDM, AF Cauda equina syndrome Laminectomy + discectomy None No Home 37 days
17 63, F White Em d24 None Meningitis Endoscopic third
ventriculostomy + Rickham
None No Home 47 days
Admission: Type—Em(ergency) vs. Elec(tive); COVID—time to COVID-19 infection from day of admission (days)
ITU, admission to intensive treatment unit; LoS, length of inpatient hospital stay (days)
Co-morbidities: hypertension (HTN), non-insulin-dependent diabetes mellitus (NIDDM), atrial fibrillation (AF)
327Acta Neurochir (2021) 163:317–329
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arrangements were used to maintain the delivery of the degen-
erative spine disease for medically refractory neural compres-
sion, with no significant difference in waiting times between
pre-COVID-19 and COVID-19 periods, matching the capac-
ity to referrals (p> 0.05, median waiting times 28 and 27
weeks respectively).
Impact of COVID-19 on subspecialties and neurosur-
gical training
There has been little focus on the impact of COVID-19 on
neurosurgical training [1]. During the COVID-19, and as part
of restructuring the services to release capacity to deal with
COVID-19, most of our neurosurgical trainees were rede-
ployed to ITU or COVID-19 wards. This combined with the
fact that fewer operations were performed, meant a reduction
in training opportunities. There was a move to teach through
Zoom (Communications Technology Company, San Jose,
CA) conference calls within our unit as elsewhere [19]tokeep
theoretical knowledge up-to-date; however, this cannot re-
place actual operative experience. This is further confounded
as certain subspecialties have had to modify their operative
techniques based on recommendations from various neurosur-
gical societies, particularly to avoid approaches through the
respiratory tract (e.g. trans-sphenoidal surgery) or to limit the
use of aerosol-generating instruments (including drills, ultra-
sonic aspirator) [3,7].
As part of an effort to reduce physical contacts, in our unit,
face-to-face outpatient clinic appointments were almost exclu-
sively changed to telephone. The majority of telephone clinics
were for patients being under regular follow-up with stable
imaging findings and clinical course. All postponed or can-
celled elective patients were equally kept under close tele-
phone follow-up and prioritized for re-scheduling according
to disease/symptom severity. Follow-up outcomes included
further telephone consultations, repeat imaging, face-to-face
assessment, or rescheduled surgery. None of these patients
required emergency admission. Only patients who required
neurosurgical intervention were seen in face-to-face clinic in
order to be pre-assessed for surgery. Overall, this system
worked well and may have potential implications on outpa-
tient management for the future [4,10]. In our experience,
remote access platforms such as Attend Anywhere®
(Melbourne, Australia) or secure patient online chat-rooms
such as The Brain Tumour Charity’s BRIAN [23] provide
invaluable tools in keeping contact with patients.
COVID-19-positive patients and perioperative
mortality
The GlobalSurg reported a 30-day perioperative mortality of
23.8% amongst COVID-19 patients undergoing emergency or
elective surgery [2]. In contrast, within our cohort, 30-day
perioperative mortality remained low during COVID-19
(2.0%). In fact, none of our four neurosurgical patients that
underwent surgery whilst infected with COVID-19 died. We
noted that 13 patients (2.0%) who underwent neurosurgery
before and during COVID-19 were infected with COVID-19
whilst being an inpatient; however, no single factor could be
identified to trace the cause of these post-operative inpatient
infections. Importantly, the majority of these patients had un-
derlying co-morbidities or suffered a post-operative complica-
tion, hence making them more susceptible to COVID-19 in-
fection [5]. There is new evidence suggesting that people from
a BAME background are more severely affected by COVID-
19 [8,11,17,18]. 35.3% of our patients with COVID-19 were
from a BAME background, of which one died. More data and
larger cohorts are needed to further study this aspect.
Limitations of this study
Patient numbers were limited due to the relatively short time
period observed. This was however inevitable and a reflection
of the dynamic nature of the pandemic since the last day of
recruitment was dictated by a national change in strategy to-
wards the next phase to restore services. Our retrospective
data collection for the pre-COVID-19 phase may also be an-
other limitation here. We further did not analyse the impact of
COVID-19 on excess/indirect neurosurgical mortality due to
lack of presentation to hospitals such as the case maybe, for
example, for ruptured aneurysms.
Conclusions
There was a reduction in neurosurgical referrals by 33.6% and
operations by 55.6% during the course of COVID-19. The 30-
day perioperative mortality, however, remained low at 2.0%,
considerably lower than that in other published series [2], with
the majority of patients who contracted post-operative
COVID-19 infection having underlying co-morbidities and/
or suffering from post-operative complications. Despite the
challenges, capacity to treat patients requiring urgent or emer-
gency neurosurgical care was maintained at all times. The
strategies we adopted allowed creation of new capacity and
safe delivery of neurosurgical care, with restructuring the pa-
tient pathways and facilities into COVID-19 positive and non-
COVID-19, arguably as the most important step. We strongly
believe our multi-modal approach was the key to minimize the
disruptions, complications, and mortality and that lessons
learned will have direct relevance for neurosurgical care dur-
ing the current and future pandemics.
Contributors All authors made substantive intellectual contributions to
the development of this research. KA, JJ, AMV, and AR contributed to
study conception and development, data collection and data
328 Acta Neurochir (2021) 163:317–329
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interpretation, and critical revision of the manuscript. All other authors
contributed to study conception and development, and critical revision of
the manuscript, and approved the final version of this manuscript. The
corresponding author attests that all listed authors meet authorshipcriteria
and that no others meeting the criteria have been omitted. JJ is the
guarantor.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval All procedures performed in studies involving human
participants were in accordance with the ethical standards of the institu-
tional and/or national research committee (King’s College Hospital clin-
ical governance approval has been obtained for this audit) and with the
1964 Helsinki declaration and its later amendments or comparable ethical
standards. For this type of study, formal consent is not required.
Open Access This article is licensed under a Creative Commons
Attribution 4.0 International License, which permits use, sharing, adap-
tation, distribution and reproduction in any medium or format, as long as
you give appropriate credit to the original author(s) and the source, pro-
vide 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
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statutory regulation or exceeds the permitted use, you will need to obtain
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licence, visit http://creativecommons.org/licenses/by/4.0/.
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