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research-article2021
PMJ0010.1177/02692163211018342Palliative MedicinePiers et al.

Short Report

Palliative Medicine

Early resuscitation orders in hospitalized oldest-


2021, Vol. 35(7) 1288­–1294
© The Author(s) 2021
Article reuse guidelines:
old with COVID-19: A multicenter cohort study sagepub.com/journals-permissions
DOI: 10.1177/02692163211018342
https://doi.org/10.1177/02692163211018342
journals.sagepub.com/home/pmj

Ruth Piers1,2 , Eva Van Braeckel2,3, Dominique Benoit2,4


and Nele Van Den Noortgate1,2

Abstract
Background: In particular older people are at risk of mortality due to corona virus disease 2019 (COVID-19). Advance care planning is
essential to assist patient autonomy and prevent non-beneficial medical interventions.
Aim: To describe early (taken within 72 h after hospital admission) resuscitation orders in oldest-old hospitalized with COVID-19.
Setting/participants: A cohort of patients aged 80 years and older admitted to the acute hospital in March and April 2020 with
COVID-19 were retrospectively recruited from 10 acute hospitals in Belgium. Recruitment was done through a network of geriatricians.
Results: Overall, 766 octogenarians were admitted of whom 49 were excluded because no therapeutic relationship with the
geriatrician and six because of incomplete case report form. Early decisions not to consider intensive care admission were taken in
474/711 (66.7%) patients. This subgroup was characterized by significantly higher age, higher number of comorbidities and higher
frailty level. There was a significant association between the degree of the treatment limitation and the degree of premorbid frailty
(p < 0.001). Overall in-hospital mortality was 41.6% in patients with an early decision not to consider intensive care admission (67.1%
in persons who developed respiratory failure vs 16.7% in patients without respiratory failure (p < 0.001)). Of 104 patients without
early decision not to consider intensive care admission but who developed respiratory failure, 59 were eventually not transferred to
intensive care unit with in-hospital mortality of 25.4%; 45 were transferred to the intensive care unit with mortality of 64.4%.
Conclusions: Geriatricians applied all levels of treatment in oldest-old hospitalized with COVID-19. Early decisions not to consider
intensive care admission were taken in two thirds of the cohort of whom more than 50% survived to hospital discharge by means of
conservative treatment.

Keywords
COVID-19, resuscitation orders, aged, 80 and over, in-hospital mortality, advance care planning, multicenter study, cohort study,
intensive care unit

What is already known?


•• Oldest old with COVID-19 are at increased risk of mortality.
•• The outcome is related to the level of premorbid frailty.
•• Goals of care conversations are desired by patients and are feasible but often neglected in acute care settings.

What this paper adds?


•• Oldest old admitted with COVID-19 were frequently co-managed by geriatricians in Belgian hospitals.
•• Early resuscitation orders were taken in two thirds of the cohort.
•• The degree of anticipatory treatment limitation was associated with the degree of premorbid frailty.
•• More than half of hospitalized oldest old with an early decision not to consider intensive care treatment survived by
means of conservative treatment.

1Department of Geriatric Medicine, Ghent University Hospital, Ghent, Corresponding author:


Belgium Ruth Piers, Department of Geriatric Medicine, Ghent University
2Department of Internal Medicine and Pediatrics, Ghent University, Hospital, C. Heymanslaan 10, Ghent 9000, Belgium.
Ghent, Belgium Email: ruth.piers@uzgent.be
3Department of Respiratory Medicine, Ghent University Hospital, Ghent,

Belgium
4Department of Intensive Care Medicine, Ghent University Hospital,

Ghent, Belgium
Piers et al. 1289

Implications for practice, theory or policy


•• Geriatricians frequently and timely think about the ceiling of treatment in oldest old with COVID-19. Maximum conserva-
tive supportive treatment can save lives, while also taking palliative care principles like advance care planning into account.

Introduction hospital in March and April 2020 with COVID-19.


Recruitment was performed through means of an existing
COVID-19 is characterized by a broad spectrum of disease network of geriatricians working in 10 different hospitals
severity, including severe pneumonia with high risk of (convenience sample) who collected the data retrospec-
developing respiratory failure requiring oxygen therapy, tively by means of an electronic case report form. In
non-invasive ventilation or invasive mechanical ventila- Belgium, patients aged 80 years and older admitted to
tion in the intensive care unit (ICU). acute hospitals are mainly hospitalized in geriatric beds
The older patient seems to have a higher susceptibility and treated by geriatricians.
for SARS-CoV-2 infection, a higher risk of developing Inclusion criteria were being 80 or older at the time of
severe COVID-19 and of COVID-19 related mortality.1,2 A hospital admission and having been diagnosed with
meta-analysis gathering data from China, Italy, Spain, UK COVID-19 (based on SARS-CoV-2 PCR positivity and/or
and New York found that persons aged 80 or older had a based on characteristic anomalies on chest computed
six-times higher risk of dying compared to younger tomography, biochemistry and suggestive signs and symp-
patients, with case fatality rates varying between 14.8% toms, and/or consensus on COVID-19 diagnosis within
(China) and 53.7% (New York).3 The level of frailty, defined multidisciplinary team meeting).
as the level of reduction in ability to withstand acute
stress situations, is known to be a robust risk factor for
adverse outcome in older adults in different settings.4,5 Ethics
Recent studies confirm the relation between frailty and The study was approved by the central ethics committee
outcome in COVID-19.6,7 (Ghent University Hospital, Belgian Registration number
Clinicians should always carefully balance benefits and BC-07858) and all local ethics committees. Informed con-
harms in deciding whether or not to escalate care, also in sent was waived because of the retrospective and non-
COVID-19.8,9 In-hospital, the level of supportive care may interventional nature of the study and because strict
range from pursuing all life-sustaining therapies including anonymity during data processing was guaranteed. The
mechanical ventilation to comfort-directed care. The deci- treating geriatricians looked into their medical files and
sion as to which level is most appropriate for an older indi- delivered the anonymized data through a secure web
vidual is based on the interplay between the estimated application REDCap (https://www.project-redcap.org).
outcome and the patient’s goals of care.8 Timely, honest
and compassionate conversations may help frail patients
and their families to prepare for uncertain but possible Data collection and measures
adverse outcome.9,10 Acute hospitals are known to be
places where advance care planning is often lacking.11,12 Participating geriatricians filled out a short survey on the
However, there is evidence that a majority of patients resuscitation order policy in their ward (consultation of
who know they are at the end of their life want to avoid patients, families, nursing team and other medical spe-
ICU13,14 and that goals of care conversations during the cialties in making up the resuscitation order in March and
COVID-19 pandemic are feasible even in acute care April 2020).
settings.15 The total number of octogenarians admitted to their
To the best of our knowledge, transparent description hospital was retrieved through the official registration
of early resuscitation orders in COVID-19 is lacking in lit- data for the government. The geriatricians collected data
erature.16 This study aimed to describe early resuscitation from those patients with whom they had a therapeuthical
order decisions in relation to premorbid frailty in oldest- relationship. Socio-demographic information, premorbid
old admitted with COVID-19. level of frailty, comorbidities, respiratory characteristics of
the peak of the COVID-infection during admission, resus-
citation orders and in-hospital mortality were collected
Methods from the medical record after patient discharge. All data
were collected before August 2020, in order to minimize
Design, participants, settings recall bias.
This is a multicentre retrospective cohort study of patients An ‘early’ resuscitation order was defined as a treat-
aged 80 years and older who were admitted to the acute ment limitation decision taken within 72 h after hospital
1290 Palliative Medicine 35(7)

admission. The resuscitation orders were predefined into Participants


five levels: (1) full code: pursue all life-sustaining treat-
ments including mechanical ventilation in case of respira- Overall, 766 octogenarians were admitted of whom 49
tory failure; (2) do-not-resuscitate only: pursue all patients were not included because there was no thera-
life-sustaining treatments excluding cardiopulmonary peutic relationship with the geriatrician. Additionally, six
resuscitation (CPR); (3) do-not-intubate: pursue all life- cases were excluded because of incomplete case report
sustaining treatments including non-invasive ventilation form, leaving 711 cases for the study. In Table 1, premor-
but excluding mechanical ventilation and CPR; (4) ward- bid characteristics are shown. Premorbid CFS was filled
based medical treatment only: pursue all life-sustaining out by the treating geriatrician post-hoc for study purpose
treatments excluding, CPR, intubation, non-invasive venti- in 68%. Mean premorbid CFS was 5.44 (95% CI [5.32–5.55]
lation; (5) comfort-directed care: no life-sustaining treat- on a scale that ranges from 1 (very fit) to 9 (terminally ill)).
ments, only treatment supporting comfort of the patient. Early decisions not to consider admission in the ICU
Throughout the article these five levels are dichotomized: were taken in 474 (66.7%) patients. This subgroup was
one to three consider intensive care versus four and five: characterized by significantly higher age, more comorbid-
do not consider intensive care admission. ity, more often coming from a nursing home and higher
The Clinical Frailty Scale (CFS) is often put forward as a premorbid CFS (Table 1). There was a significant associa-
preferred tool for assessing frailty in older adults to be tion between the degree of anticipatory treatment limi-
used for timely ICU admission decisions.17,18 The CFS© was tation and the degree of premorbid CFS (p < 0.001)
used with official permission to assess premorbid frailty (Figure 1).
and was scored by the geriatrician.19 The CFS ranks frailty In-hospital mortality was 41.6% in 474 patients in
from 1 (very fit) to 9 (terminally ill). A patient with CFS 7 is whom an early decision not to consider ICU admission
severely frail without limited prognosis, and patients with was made. Half of patients with a decision not to consider
CFS 8 and 9 have a life expectancy lower than 6 months. ICU admission developed respiratory failure (234/474); in
As geriatricians are experts in comprehensive geriatric those persons who developed respiratory failure, in-hos-
assessment, they are best placed to score CFS. pital mortality was 67.1% (157/234) versus 16.7% (40/240)
Severity of COVID-19: criteria for respiratory failure in patients who did not develop respiratory failure
were predefined as follows: PaO2 ⩽ 60 mmHg and/or low (p < 0.001).
SpO2 (⩽ 90% with supplemental oxygen or ⩽88% without In-hospital mortality was 20.7% in 237 patients with-
supplemental oxygen) and/or in need of more than 5 L/ out early decision not to consider ICU. Of 104 patients
min oxygen supplementation at any moment during hos- without early decision not to consider ICU admission but
pital stay. who developed respiratory failure, 59 were eventually not
transferred to ICU, and of those 15 (25.4%) died on the
regular ward. About 45 were transferred to the ICU, of
Statistical analysis whom 64.4% died in the ICU.
Descriptive statistics and Chi Square test for association
between the degree of treatment limitation and patient Discussion
characteristics were computed using IBM SPSS Statistics
software version 25 (IBM Corp., Armonk, NY, USA). The Main findings
exact p-values are reported, with statistical significance The majority of oldest old admitted in 10 acute Belgian hos-
defined as p⩽0.05. pitals with COVID-19 were treated by a geriatrician.
Anticipatory decision-making was frequent with an early
decision not to consider ICU admission in case of respiratory
Results failure in two thirds of the cohort. The degree of anticipa-
Hospital resuscitation order policy tory treatment limitation was associated with the degree of
characteristics premorbid frailty. The group with early decision not to con-
sider ICU admission was characterized by significantly higher
Concerning the resuscitation order policy on their wards, age, more comorbidity, and higher level of premorbid frailty.
geriatricians informed their patients and/or families The mortality was 20.7% in patients without early decision
‘always’ in 70% of hospitals and ‘often’ in 30%. Consultation and 41.6% in the group with early decision not to consider
with the nursing team occurred ‘always’ in 50% of hospi- ICU admission.
tals, ‘often’ in 40% and ‘occasionally’ in 10%. Consultation
with other colleagues occurred in 30% of hospitals with
Strengths and limitations
the general practitioner, emergency physician and pulmo-
nologist, in 20% of hospitals with the intensive care To the best of the author’s knowledge, this is one of the
physician. first studies openly describing anticipatory resuscitation
Piers et al. 1291

Table 1. Premorbid clinical characteristics in 711 hospitalized oldest-old COVID-19 patients: comparison between patients without
versus with early decision not to consider ICU admission.

Characteristic Total no. (%) Patients in whom early Patients in whom p-Value
decision to consider ICU early decision NOT
in respiratory failure (%) to consider ICU (%)
Age category
 80–84 299 (42.1) 153 (64.6) 146 (30.8) <0.001
 85–89 271 (38.1) 68 (28.7) 203 (42.8)
 ⩾90 141 (19.8) 16 (6.8) 125 (26.4)
Gender
 Female 401 (56.4) 124 (52.3) 277 (58.4) 0.128
 Male 310 (43.6) 113 (47.7) 197 (41.6)
Residency before hospital admission
 At home 447 (62.9) 192 (81.0) 255 (53.8) <0.001
 Not at home 264 (37.1) 45 (19.0) 219 (46.2)
 Assisted-living facility 43 (6.0) 15 (6.3) 28 (5.9)
 Nursing home 221 (31.1) 30 (12.7) 191 (40.3)
Comorbidity
 Malignancy 192 (27.0) 51 (21.5) 141 (29.7) 0.020
 Metastatic solid tumor or progressive 38 (5.3) 1 (0.4) 37 (7.8) <0.001
hematological malignancy
 Cardiovascular 582 (81.9) 195 (82.3) 387 (81.6) 0.918
 Hypertension 439 (61.7) 61 (67.9) 278 (58.6) 0.018
 Coronary artery disease 197 (27.7) 67 (28.3) 130 (27.4) 0.859
 Carotid artery disease 66 (9.3) 13 (5.5) 53 (11.2) 0.013
 Heart failure 195 (27.4) 52 (21.9) 143 (30.2) 0.021
 Cerebrovascular accident 126 (17.7) 40 (16.9) 86 (18.1) 0.755
 Peripheral arterial disease 84 (11.8) 23 (9.7) 61 (12.9) 0.267
 Chronic lung condition 129 (18.1) 43 (18.1) 86 (18.1) 1.000
 Asthma 28 (3.9) 12 (5.1) 16 (3.4) 0.308
 Chronic obstructive pulmonary disease 101 (14.2) 31 (13.1) 70 (14.8) 0.571
 Obstructive sleep apnea 11 (1.5) 3 (1.3) 8 (1.7) 0.760
 Immunosuppressiona 30 (4.2) 8 (3.4) 22 (4.6) 0.554
 Chronic kidney disease 291 (40.9) 72 (30.4) 219 (46.2) <0.001
 End-stage renal failure of hemodialysis 21 (3.0) 8 (3.4) 13 (2.7) <0.001
 Chronic liver diseaseb 19 (2.7) 5 (2.1) 14 (3.0) 0.626
 Metabolic disease 260 (36.6) 88 (37.1) 172 (36.3) 0.869
 Obesity (BMI ⩾ 30) 98 (13.8) 31 (13.1) 67 (14.1) 0.118
 Diabetes mellitus 201 (28.2) 66 (27.9) 135 (28.5) 0.233
 Dementia 283 (39.8) 39 (16.5) 244 (51.5) <0.001
Number of affected organs/systemsc
 Mean (95% CI) 2.5 (2.4–2.6) 2.11 (1.97–2.26) 2.71 (2.60–2.82) <0.001
Clinical frailty scale
 Mean (95% CI) 4.42 (4.21–4.62) 5.95 (5.83–6.07) <0.001

ICU: intensive care unit.


aImmunosuppression includes HIV, organ transplant, chronic intake of immunomodulatory medication or systemic corticosteroids.
bChronic liver disease includes cirrhosis or chronic hepatitis.
cNumber of comorbidities was determined by calculating in how many of the eight organ systems there was at least one disease.

orders in patients with COVID-19. Another main strength in 68% the CFS was filled-out post-hoc by the geriatrician
is its multicentre design. However, there are some limita- on basis of the comprehensive geriatric assessment by
tions. The main limitation is that we lack information on the multidisciplinary team which is standard practice.
patient level about the decision-making process (varying Last, in order to really perform a causal analysis, we lacked
from explicit individual preferences of the patient, over detailed and longitudinal data on severity of illness and
shared decision-making to unilateral medical decision). lacked data associated with the resuscitation order such
Second limitation is the retrospective nature of the study; as preference of the patient. As such, we can neither
1292 Palliative Medicine 35(7)

Figure 1. Early resuscitation orders in relation to premorbid Clinical Frailty Scale score.
p < 0.001 (Chi-Square);
There was one missing value on Clinical Frailty Scale (CFS); CFS was known during hospital admission in 32%; CFS was filled out post-hoc for study
purpose in 68%. The CFS ranks frailty from 1 (very fit) to 9 (terminally ill). A patient with CFS 7 is severely frail without limited prognosis, and patients
with CFS 8 and 9 have a life expectancy lower than 6 months.
There are five levels of resuscitation orders: Full code: pursue all life-sustaining treatments (LST) including mechanical ventilation in case of respira-
tory failure; Do-not-resuscitate only: pursue all LSTs excluding cardiopulmonary resuscitation (CPR); Do-not-intubate: pursue all LST including non-
invasive ventilation but excluding mechanical ventilation and CPR; Ward-based medical treatment only: pursue all LSTs excluding, CPR, intubation,
non-invasive ventilation; Comfort-directed care: no LST, only treatment supporting comfort of the patient.
Throughout the article these five levels are dichotomized to decisions to (not) consider intensive care unit (ICU) admission.

confirm nor reject if early resuscitation orders and ICU pandemic, 78% of hospitalized patients and their surro-
treatment selection caused excess mortality. However, we gates opted to forego mechanical ventilation. In a study
found two recent publications showing that ICU admis- performed on an acute geriatric ward before the pan-
sion was not associated with improved outcome.6,20 demic, 74% of SPICT identified patients had a resuscita-
tion order, which is a similar prevalence as found in this
study.25 This reflects that geriatrician value to discuss
What this study adds timely the treatment plan in frail patients with a life-
Treatment limitation decisions have been made all over threatening disease. In line with De Bock et al.,25 the
the world in the older population with COVID-1916,21 but degree of treatment limitation was related to the degree
were seldom discussed openly. We observed a prevalence of premorbid frailty as (mostly retrospectively) assigned
of 66.7% of early decisions not to escalate treatment in by geriatricians also in this study. Geriatricians affirmed
case respiratory failure would occur. This is transcending that patients and/or families were consulted concerning
the prevalence of hospital resuscitation orders taken in the treatment limitation decision, as required by Belgian
non-COVID times with prevalence ranging from 20% to law.
40%.22–24 A possible explanation may be that COVID Importantly, more than half of hospitalized patients
patients are expected to have a higher need for ICU refer- with an early resuscitation order survived by means of
ral, a longer duration of mechanical ventilation followed conservative treatment on the regular ward by geriatri-
by much longer and as consequence less successful reha- cians. This under scribes that maximum conservative sup-
bilitation process, compared to non-COVID patients. portive treatment can save lives, while also taking
These facts reflect more urge to discuss treatment limita- palliative care principles like advance care planning into
tion in patients with COVID. This is also reflected in a account. This might support that geriatricians are in the
report of a Dutch cohort of 100 COVID-patients with an right place to take care of oldest old with COVID-19, also
average age of 68 years, admitted on non-ICU wards, in because they are experts in assessing the level of frailty, a
which 39% had an early do-not-intubate order.20 Also in major risk factor for poor outcome in the oldest old.6
accordance with our findings, Lee et  al.15 showed that When a palliative care approach is integrated early in
after palliative care consultation focusing on goals of care the appropriate patients, more attention can be given to
conversations in seriously ill patients during the COVID-19 symptom control and (online) connection with loved ones
Piers et al. 1293

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