Physicians’ Attitudes on Resuscitation

of Extremely Premature Infants: A

Systematic Review
Alice Cavolo, MA,a Bernadette Dierckx de Casterlé, RN, PhD,b Gunnar Naulaers, MD, PhD,c Chris Gastmans, PhDa

CONTEXT: Whether to resuscitate extremely premature infants (EPIs) is a clinically and ethically
difficult decision to make. Indications and practices vary greatly across different countries and
abstract
institutions, which suggests that resuscitation decisions may be influenced more by the
attitudes of the individual treating physicians. Hence, gaining in-depth insight into physicians’
attitudes improves our understanding of decision-making regarding resuscitation of EPIs.
To better understand physicians’ attitudes toward resuscitation of EPIs and factors
OBJECTIVE:
that influence their attitudes through a systematic review of the empirical literature.
DATA SOURCES: Medline, Embase, Web of Science, and Scopus.
STUDY SELECTION: We
selected English-language articles in which researchers report on empirical
studies of physicians’ attitudes toward resuscitation of EPIs.
The articles were repeatedly read, themes were identified, and data were
DATA EXTRACTION:
tabulated, compared, and analyzed descriptively.
RESULTS: Thirty-four articles were included. In general, physicians were more willing to
resuscitate, to accept parents’ resuscitation requests, and to refuse parents’ nonresuscitation
requests as gestational age (GA) increased. However, attitudes vary greatly for infants at GA 23
to 24 weeks, known as the gray zone. Although GA is the primary factor that influences
physicians’ attitudes, a complex interplay of patient- and non–patient-related factors also
influences their attitudes.
LIMITATIONS: Analysis
of English-only articles may limit generalizability of the results. In addition,
authors of only 1 study used a qualitative approach, which may have led to a biased
reductionist approach to understanding physicians’ attitudes.
Although correlations between GA and attitudes emerged, the results suggested
CONCLUSIONS:
a more complex interplay of factors influencing such attitudes.

a
Interfaculty Centre for Biomedical Ethics and Law, bAcademic Centre for Nursing and Midwifery, and cSection of Pregnancy, Foetus and Newborn, Department of Development and
Regeneration, Katholieke Universiteit Leuven, Leuven, Belgium

Ms Cavolo contributed to the study design, screened the bibliographic search results, reviewed all included articles, drafted the initial manuscript, and reviewed and
revised the manuscript; Dr Gastmans contributed to the study design, screened search results, reviewed all included studies, reviewed the manuscript, and provided
mentorship; Dr Dierckx de Casterlé contributed to the study design, reviewed the manuscript, and provided mentorship; Dr Naulaers critically reviewed the manuscript
for important clinical intellectual content and provided mentorship; and all authors approved and are accountable for the final manuscript as submitted.
DOI: https://doi.org/10.1542/peds.2018-3972
Accepted for publication Mar 5, 2019
Address correspondence to Alice Cavolo, MA, Center for Biomedical Ethics and Law, Katholieke Universiteit Leuven, Kapucijnenvoer 35/3, 3000 Leuven, Belgium. E-mail:
alice.cavolo@kuleuven.be

To cite: Cavolo A, Dierckx de Casterlé B, Naulaers G, et al. Physicians’ Attitudes on Resuscitation of Extremely Premature Infants: A Systematic Review. Pediatrics.
2019;143(6):e20183972

Downloaded from www.aappublications.org/news at Moldova, Republic of:AAP Sponsored on September 16, 2020
PEDIATRICS Volume 143, number 6, June 2019:e20183972 REVIEW ARTICLE
Extremely premature infants (EPIs)
are infants born before the 28th
complete week of gestation (the full
gestational period being 40 weeks).1
The mortality rates of EPIs vary
depending on gestational age (GA)
at birth, technological equipment
and pharmaceuticals available at the
hospital, and ethical decision-
making about how to proceed with
the infants’ care.2 In highly
developed countries, survival rates
for EPIs are ,10% at GA 22 weeks,
1% to 64% at GA 23 weeks, 31% to
78% at GA 24 weeks, and 59% to
86% at GA 25 weeks.3–5 EPIs are at
an increased risk of having
a moderate or severe disability,
including a wide range of physical
and intellectual impairments such
as neurosensory, motor, cognitive,
and behavioral impairments.3,6,7
Mortality and morbidity of EPIs are
also influenced by sex and birth
weight, whether they are twins,
whether they are exposed to
prenatal steroids and magnesium
sulfate, their condition at birth
(eg, presence of congenital
abnormalities), and postnatal
events (eg, sepsis or cerebral
complications).6,8
When an extremely preterm
delivery occurs, the first decision to
be made is whether to resuscitate
the infant.9 According to physicians,
this decision is ethically complex.10–
13
There is uncertainty about
individual prognosis (ie, probability
of survival, seriousness of short-
and long-term impairments, and
future quality of life).10,13,14 Such
uncertainty makes it difficult to
decide whether active care is
appropriate and whether physicians
are “going too far.”15 Moreover,
deciding whether to resuscitate EPIs
raises questions regarding to what
extent parents’ requests should be
respected.16
Clinical and moral uncertainties exist
at different levels of the decision-
making process regarding whether to
resuscitate EPIs. First, although
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2 CAVOLO et al
national and institutional guidelines
indicate when resuscitation should be
provided or withheld, agreement on
best practices has yet to be
reached.12,17,18 Second, the advice
and practice of professionals and
institutions vary greatly regarding
different aspects of the decision-
making, such as advised practice for
infants of different GAs.2,10–12,19
Given the diversity of practices and
the lack of professional consensus,
the decision about whether to
resuscitate EPIs is at least partially
influenced by the attitudes of the
individual physicians who are
bearing the clinical and ethical
responsibility for the decision
made.2 Hence, insight into
physicians’ attitudes toward
resuscitation of EPIs can contribute
to a better understanding of this
ethically sensitive decision-making.
Therefore, we aim to understand
physicians’ attitudes toward
resuscitation of EPIs and the factors
influencing their attitudes as
reported in the empirical literature.
METHODS
Design
We performed a systematic review
of empirical studies on physicians’
attitudes toward resuscitation of
EPIs. We followed Peer Review of
Electronic Search Strategies20 and
Preferred Reporting Items for
Systematic Reviews and Meta-
Analyses (PRISMA) 21 guidelines.
Search Strategy
A systematic search of Medline,
Embase, Web of Science, and Scopus
electronic databases was conducted
on March 30, 2018. Search strings
consisted of 4 categories of search
terms: (1) professionals’ subjective
dimension (eg, perceptions and
attitudes), (2) target population (ie,
medical doctors), (3) resuscitation,
and (4) EPI. The search strings were
developed in collaboration with
a librarian (Katholieke Universiteit
Leuven) (Table 1). The results from
the databases were merged, and
duplicate hits were deleted before
conducting the title, abstract, and
full-text screening. The search was
implemented with snowballing and
citation tracking to avoid
overlooking relevant publications.22
The search process is presented
in the PRISMA flow diagram21
(Fig 1).
Inclusion and Exclusion Criteria
Guided by predefined criteria, 2
authors (A.C. and C.G.) independently
conducted the abstract and full-text
screening. Disagreements about
article inclusion were resolved by
discussion until consensus was
reached. Inclusion and exclusion
criteria were defined on the basis of
type of study, participants, and
outcome measures (Table 2).
Regardless of these strict inclusion
and exclusion criteria, some biases
may be introduced in the review. For
instance, studies reporting on self-
reported attitudes may be affected
by social desirability bias. In
addition, resuscitation and
additional treatment of EPIs
requires technological and
pharmaceutical equipment, which
means that in low-income countries
where there is lack or scarcity of
such equipment, EPIs may not be
resuscitated. This may lead to the
exclusion of low-income countries
from the review and the
introduction of cultural bias.
Quality Appraisal
The included quantitative studies
were appraised by using the tool
developed by Hawker et al,23 whereas
the included qualitative studies were
appraised by using the Critical
Appraisal Skills Programme (CASP).24
Quality appraisal was conducted by 2
authors (A.C. and C.G.) independently.
The 2 sets of assessments were
compared, and in cases of
disagreements, assessments were
discussed until a consensus was
achieved. Quality assessment was
 TABLE 1 Overview of Bibliographic Databases Searched, Search Strings Used, and Search Results of Articles Identified
Database Group 1: Subjective Dimension
Medline (((((“Attitude”[Mesh:NoExp] OR attitude Physician[MeSH] OR Physician*[tiab]
[tiab] OR attitudes[tiab] OR opinion*
[tiab])) OR (“Attitude of Health
Personnel”[Mesh:NoExp] OR health
personnel attitudes[tiab] OR staff
attitudes[tiab]) OR (“attitude to
death”[Mesh] OR attitudes to death
[tiab])) OR (“Health Knowledge,
Attitudes, Practice”[Mesh] OR
experience*[tiab] OR perspective*
[tiab] OR preference*[tiab] OR
PEDIATRICS Volume 143, number 6, June 2019
argument*[tiab] OR insight*[tiab] OR
view*[tiab] OR feeling*[tiab])) OR
“Intuition”[Mesh] OR intuition*[tiab]
OR intention*[tiab])
Embase 'attitude'/de OR 'health personnel
attitude'/de OR 'attitude to death'/
exp OR 'intuition'/exp OR ((attitude:
ab,ti OR attitudes:ab,ti OR health)
AND personnel AND attitude:ab,ti OR
attitude) AND to AND death:ab,ti OR
intuition*:ab,ti OR experience*:ab,ti
OR perspective*:ab,ti OR preference*:
ab,ti OR opinion*:ab,ti OR argument*:
ab,ti OR insight*:ab,ti OR feeling*:ab,ti
OR intention*:ab,ti OR view*:ab,ti
Web of TS= (attitude OR attitudes OR opinion* TS=(Physicians* OR doctor* OR
Science OR health personnel attitude OR
health personnel attitudes OR staff
attitude OR staff attitude OR attitude
to death OR experience* OR
perspective* OR preference* OR
argument* OR insight* OR view* OR
feeling* OR intuition* OR intention*)
Scopus TITLE-ABS-KEY attitude OR attitudes OR TITLE-ABS-KEY (physicians* OR doctor* TITLE-ABS-KEY (resuscitation OR
opinion* OR “health personnel
attitud*” OR “staff attitude*” OR
experience* OR perspective* OR
preference* OR argument* OR
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insight*or AND view* OR feeling* OR
intuition* or intention*)
ABS, abstract; TS, topic.
a Number of articles returned for the indicated search.
3
Group 2: Target Population
((((((“Resuscitation”[Mesh] OR resuscitation
OR doctor*[ tiab] OR clinician*[ tiab]
OR neonatologist[MeSH] OR
neonatologist*[ tiab] OR
pediatrician*[ tiab] OR obstetrician*[
tiab] OR healthcare provider*[ tiab]
'physician'/de OR 'neonatologist'/de OR ('resuscitation'/exp OR 'newborn intensive
'pediatrician'/de OR 'health care
personnel'/de OR ((physician:ab,ti OR
physicians:ab,ti OR neonatologist:
ab,ti OR neonatologists:ab,ti OR
pediatrician:ab,ti OR pediatricians:
ab,ti OR pediatrician:ab,ti OR
pediatricians:ab,ti OR doctor:ab,ti OR
doctors:ab,ti OR clinicican:ab,ti OR
clinicians:ab,ti OR obstetrician:ab,ti
OR obstetricians:ab,ti OR healthcare)
AND provider:ab,ti)
TS= (Resuscitation OR cardio pulmonary
clinician* OR obstetrician* OR
healthcare provider* OR
pediatrician* OR pediatrician* OR
neonatologist*)
OR clinician* OR obstetrician* OR
“healthcare provider*” OR
pediatrician* OR pediatrician* OR
neonatologist*)
Group 3: Resuscitation Group 4: EPIs Results,a n
(((“Infant, Newborn”[Mesh] OR infant[tiab] OR 1506
[tiab] OR cardio pulmonary resuscitation infants[tiab] OR newborn[tiab] OR newborns
[tiab] OR CPR[tiab] OR basic cardiac life [tiab] OR neonate[tiab] OR neonates[tiab] OR
support[tiab] OR reanimation[tiab] OR low-birth-weight infant*[tiab] OR premature
neonatal resuscitation[tiab])) OR (“Decision infant*[tiab] OR preterm infant*[tiab] OR
Making”[Mesh:NoExp] OR decision making extremely premature infant[tiab] OR neonatal
[tiab] OR treatment decisions[tiab] OR end- prematurity[tiab] OR viability[tiab] OR extreme
of-life decisions[tiab])) OR (“Intensive Care, prematurity[tiab])) OR (“Premature
Neonatal”[Mesh] OR neonatal intensive care Birth”[Mesh] OR premature birth[tiab] OR
[tiab])) OR (“Intensive Care Units, preterm birth[tiab]))
Neonatal”[Mesh] OR neonatal ICU[tiab] OR
NICU[tiab] OR neonatal intensive care units
[tiab])))
'infant'/exp OR infant:ab,ti OR infants:ab,ti OR 127
care'/exp OR 'NICU'/exp OR 'ethical decision newborn:ab,ti OR newborns:ab,ti OR neonate:ab,ti
making'/de OR 'decision making'/de OR OR neonates:ab,ti OR 'extremely low birth
'clinical decision making'/de OR weight'/de OR 'extremely low birth weight':ab,ti
resuscitation:ab,ti OR 'NICU':ab,ti OR OR 'extremely premature infant*':ab,ti OR
'newborn intensive care':ab,ti OR 'decision 'prematurity'/exp OR 'premature labor'/exp OR
making':ab,ti OR ((treatment NEXT/1 'premature labor'/de OR ((extreme NEXT/1
decision*):ab,ti) OR end:ab,ti) AND of:ab,ti prematurity):ab,ti) OR 'preterm birth':ab,ti OR
AND life:ab,ti AND decision*:ab,ti 'premature birth':ab,ti OR 'viability':ab,ti
TS=(infant OR infants OR newborn OR newborns OR 1115
resuscitation OR CPR OR basic cardiac life neonate OR neonates OR low-birth weight infant*
support OR reanimation OR neonatal OR premature infant* OR preterm infant* OR
resuscitation OR decision making OR extremely premature infant OR neonatal
treatment decisions OR end-of-life decisions prematurity OR viability OR extreme prematurity
OR neonatal intensive care OR neonatal ICU OR premature birth OR preterm birth)
OR NICU OR neonatal intensive care units)
TITLE-ABS-KEY (infant OR infants OR newborn OR 342
“cardiopulmonary resuscitation” OR CPR OR newborns OR neonate OR neonates OR “low-
“neonatal resuscitation” OR “decision birth-weight infant*” OR “premature infant*” OR
making” OR “treatment decision*” OR “end- “preterm infant*” OR “extremely premature
of-life decision*” OR “neonatal intensive infant” OR “neonatal prematurity” OR viability OR
care” OR “neonatal ICU” OR “neonatal “extreme prematurity” OR “premature birth*” OR
intensive care unit*”) “preterm birth*”)
indicative rather than evaluative,
meaning that articles were not
excluded on the basis of their
methodologic quality.

Data Extraction and Synthesis

Data extraction and synthesis
consisted of several steps. The results
of each step were discussed within
the research group comprising
experts in neonatology, nursing
science, philosophy, and bioethics.
First, the included articles were
repeatedly read to familiarize
ourselves with the material. Next, the
results section of each article was
read, and relevant data were
extracted to identify the articles’ main
themes. This step produced 4 themes,
providing the structure to describe
the results: (1) physicians’ attitudes
toward resuscitation versus
nonresuscitation, (2) physicians’
attitudes toward parents’ requests to
resuscitate versus to not resuscitate,
(3) influence of physicians’
demographic characteristics, and (4)
influence of case-related factors on
attitudes. Finally, data within each
theme were tabulated to identify
comparable sets of data. On the basis
of the tables, data were analyzed and
compared to identify relevant
attitudinal patterns and influencing
factors. The general trends were then
described, and exceptions were
further analyzed to understand their FIGURE 1
Electronic literature search for the identification and selection of articles dealing with physicians’
basis. Given the lack of sufficient data attitudes toward the care of EPIs. The flowchart is organized according to the PRISMA guidelines
for EPIs younger than GA 22 weeks, outlined by Liberati et al.21
only data related to the period
between the 22nd and 27th weeks Thirty-three studies were the studies. The custom questionnaire
were extracted. quantitative, and 1 was qualitative developed by Janvier et al58 was used
(Table 3). In all of the quantitative in 4 studies.16,25,36,40 Similarly, other
studies, authors used a descriptive questionnaires were used twice in
RESULTS design (ie, questionnaire survey) different studies.
with closed-ended or graded
Study Characteristics The study setting was indicated in
questions. Fictional cases or
only 13 studies, the majority of which
The systematic search yielded 34 different scenarios linked to
were conducted either in NICUs
relevant publications (Table 3). The attitudinal questions were used
(n = 4) or in perinatal and neonatal
publication dates range from 1998 to in 18 studies, and in-depth
centers (n = 5).
2017. The studies originated from 27 interviews were used in the
countries, representing 5 continents: qualitative study. Overall, 8682 physicians participated
North America (n = 14), Oceania in the included studies, with reported
(n = 6), Asia (n = 3), Europe (n = 10), An in-house custom questionnaire sample sizes ranging from 16 to
and Africa (n = 1). was developed and used in most of 1401. In a majority of the studies,

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4 CAVOLO et al
TABLE 2 Inclusion and Exclusion Criteria for Selection of Articles on Physicians’ Attitudes Toward
Resuscitation of EPIs
Includeda
Types of study • Published empirical studies with
reported on quantitative, qualitative, or mixed-
methods designs
• Publication language is English
• Inclusion was not restricted to
a particular time period
Types of • Practicing physicians in studies
participants in sampling their attitudes alone, or
the study • Practicing physicians in combined
studies of nonphysician clinicians or
parents, only if physicians’ data could
be separately extracted
• Physicians’ attitudes, perceptions,
feelings, opinions toward and
Outcome measures arguments for or against
in study reported resuscitation versus nonresuscitation
on • Measures of resuscitation as
a holistic process and measures
focusing on the different steps of
resuscitation separately
Infants born before 28 weeks’ gestation.1
a Screening of articles was not limited by publication date; the entire date range was included in searches of the Medline,
Embase, Web of Science, and Scopus databases.
b When identifying premature infants, we recognize that EPIs and infants with extremely low birth weight partially overlap.
To ensure homogeneity and comparability of the cross-study data, we excluded articles in which the study considered
only birth weight as the identifying factor and analysis of variables related to infants with low birth weight in general.
authors reported on the attitudes of
neonatologists (n = 13), physicians
(n = 7), obstetricians (n = 2), or
consultants (n = 1) alone or in
combination (n = 7). The remaining
studies were used to compare
attitudes of physicians and nurses
(n = 4).
Methodologic Quality
The quality assessment results for
the included quantitative and
qualitative studies are summarized
in Tables 4 and 5. Only 4 low-quality
studies emerged from our
evaluation. All quantitative studies
had good or fair results on quality,
meaning that their findings were
appropriately described and easily
understandable.23 Moreover, with
only a few exceptions, most of the
reports had abstracts, introductions,
and aims that we rated as having
fair or good quality. However, in 12
studies, researchers failed to
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PEDIATRICS Volume 143, number 6, June 2019
Excluded
• Dissertations, books, book chapters,
theoretical articles, guidelines, and
reviews
• Studies in which only the attitudes of
nonphysician clinicians (eg, nurses,
midwives, trainees, or students)
were sampled
• Studies in which only the attitudes of
EPI parents, relatives, and other
nonphysician stakeholders were
sampled
• Measures of the actual involvement
of physicians in the decision-making
process and the current decision-
making practice
• Measures of withholding or
withdrawal of active treatments or
intensive care in general
• Measures of infants with extremely
low birth wt in generalb
adequately describe their data
analysis, and in 17 reports,
researchers failed to include an
adequate ethics section. Finally,
although the qualitative study was
of high quality, the researchers
failed to consider limitations
resulting from the relationship
between researchers and
participants.
Attitudes Toward Resuscitation and
Nonresuscitation
In 19 studies, researchers
investigated physicians’ attitudes
toward resuscitation or
nonresuscitation of EPIs. The
researchers of these studies
considered the issue from different
perspectives. Most researchers
examined attitudes according to the
GAs of the EPIs. Fewer studies were
used to examine this aspect in terms
of physicians’ lower threshold for
resuscitation, which is defined as the
lowest GA below which physicians
would not resuscitate (Table 6).
Attitudes According to GA
With only few exceptions, the 15
studies in which researchers
investigated how physicians’ attitudes
differ depending on GA reveal a clear
trend: With increasing GA, physicians
were more willing to resuscitate the
EPIs, and with decreasing GA, they
were less willing to resuscitate.
Results from these studies are
grouped according to GA (Fig 2).
GA 22 and 23 Weeks
The majority of physicians
(85%–100%) would not resuscitate
infants born at GA 22 weeks33,37,38,41,
48
; only 0% to 4.4% said they
would.37,38,41,48 Even for infants born
at GA 23 weeks, most physicians
(57%–81.9%) still would not
resuscitate,38,41,48,55 whereas more
said that they would (4%–47%)28,38,
41,48,55
compared with 22 weeks. One
exception is the study by Arzuaga
et al27 of North American physicians
who identified themselves as Muslim:
51% and 85% would resuscitate at
GA 22 and 23 weeks, respectively.
GA 24 Weeks
The percentage of physicians willing
to resuscitate EPIs at GA 24 weeks
varied widely, spanning from 38% to
99%.16,25,32,33,36–38,40,41,48,55
Similarly, 2% to 27.2% were
unwilling to resuscitate.32,38,41,46,48,55
However, the study of physicians in
11 European countries32 found that
the majority surveyed in the
Netherlands (63%) would not
resuscitate EPIs at this GA, whereas in
the other 10 countries, between 82%
and 96% would resuscitate.
GA 25 Weeks
The majority of physicians
(85.4%– 100%) would resuscitate at
GA 25 weeks,38,41,48,55 whereas
a minority (0%–4.2%) still would
not.38,41,48,55 In only 1 study were
different results reported.47 That
study included a fictitious scenario in
5
6
TABLE 3 Overview of Studies in the Included Articles
Study Country Aim Sample Size and RR Data Collection Ethical Considerations
Quantitative
studies
Armstrong Ireland To determine how physicians apply the 200 health care professionals and Questionnaire included 8 resuscitation Anonymity of participants was
et al25 best-interest standard medical students. RR: 74% scenarios of incompetent, critically ill ensured
(n = 148); health care patients and questions about
professionals’ RR: 63% (n = 93); resuscitation preferences
students’ RR: 37% (n = 55)
Arzuaga and United States To identify differences in resuscitation 2123 members of the perinatal section Questionnaire included collection of Approval of the institutional review
Meadow26 practices for EPIs (GA 22–25 wk) and of the American Academy of demographic data, presentation of board was obtained
influencing factors Pediatrics. RR: 30% (n = 637) scenarios, and attitudinal questions
Arzuaga United States To investigate the associations between 626 physician members of the Islamic Questionnaire included presentation of Anonymity of participants was
et al27 physicians’ personal characteristics Medical Association of North scenarios and attitudinal questions ensured
and attitudes toward resuscitation of America. RR: 41% (n = 255)
EPIs (GA 22–23 wk).
Ballard United States To investigate the associations between 949 neonatologists from the American Survey included a vignette and Approval of the Institutional Review
et al28 fear of litigation and attitudes toward Medical Association Masterfile. RR: attitudinal questions (2 different Boards of the Children’s Hospital of
resuscitation 63.0% (n = 598) versions used) Philadelphia and University of
Pennsylvania was obtained
Bell et al29 Romania To investigate physicians’ attitudes 95 neonatologists participating at the Survey included 36 multiple-choice or Anonymity of participants and
toward withholding or withdrawing National Congress of Neonatology in close-ended questions voluntary participation was
intensive care for impaired infants Iasi, Romania. RR: none ensured
Charafeddine Lebanon To determine physicians’ attitudes 328 practicing neonatologists and Questionnaire included demographic Approval from the institutional review
et al30 toward resuscitation of EPIs (GA pediatricians registered in the data, closed-ended questions on board and verbal consent to
23–26 wk) and influencing factors for Lebanese Order of Physicians. RR: management of preterm deliveries participate were obtained
attitudes 36% (n = 120) and EPIs, and counseling
Cummings United States To determine physicians’ opinions 65 neontologists in the perinatal Questionnaire included demographic Anonymity of participants was
et al31 regarding threshold for resuscitating section of the American Academy of data, different scenarios, and ensured
EPIs (GA 21–27 wk) Pediatrics. RR: 69% (n = 45) attitudinal questions
De Leeuw Italy, Spain, France, To determine physicians’ attitudes 1574 physicians. RR: 89% (n = 1401) Questionnaire included different ethical Anonymity of participants was
et al32 Germany, Netherlands, toward resuscitation for infants at scenarios ensured
Luxembourg, United the borderline of viability
Kingdom, Sweden,
Hungary, Estonia, and
Lithuania
Duffy and United Kingdom To determine pediatricians’ attitudes 123 consultants and trainees. Questionnaire included demographic Approval of the Surrey Research
Reynolds33 toward parental treatment Consultants’ RR: 49% (n = 54); data, closed-ended questions on Ethics Committee was obtained
preferences trainees’ RR: 51% (n = 57) management of EPIs and counseling,
and freedom for text comments
Geurtzen Netherlands To explore physicians’ preferences 205 obstetricians and neonatologists. Survey questionnaire included Approval of local institutional review
et al34 toward treatment of EPIs (GA 22–26 RR: 60% (n = 122) demographic data, 1 scenario, and 3 board was obtained, and anonymity

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wk) despite the guidelines attitudinal questions of participants was ensured
Gooi et al35 Australia To explore nontertiary obstetricians’ 232 obstetricians. RR: 75% (n = 174) Questionnaire included demographic Voluntary participation was ensured
opinions toward treatment of EPIs (GA data, clinical case, and questions
22–28 wk) about treatment preferences and
outcomes
Norway —

CAVOLO et al
 TABLE 3 Continued
Study Country Aim Sample Size and RR Data Collection Ethical Considerations
Hansen To determine physicians’ attitudes 1650 practicing physicians. RR: 65% Questionnaire included 8 resuscitation
et al36 toward resuscitation of critically ill (n = 1069) scenarios involving incompetent,
patients (aged 24 wk–80 y) critically ill patients; questions about
resuscitation preferences
Kariholu United Kingdom To determine staff’s opinions toward 37 participants: consultant Questionnaire included questions on Anonymity of participants was
et al37 resuscitation for EPIs (,GA 27 wk) pediatricians and neonatologists opinions about the GA at which to ensured
(n = 20), specialists’ registrars start resuscitation
(n = 13), and nursing staff (n = 4)
Khan et al38 Ireland To determine health care providers’ 300 health care providers. RR: 55% Questionnaire included questions on the Anonymity of participants was
attitudes toward resuscitation for (n = 175); neonatologists’ RR: 70%; antenatal, intrapartum, and postnatal ensured
EPIs (GA 22–27 wk) and the influence obstetricians’ RR: 74%; management of mother and infant

PEDIATRICS Volume 143, number 6, June 2019

of the expected outcomes pediatricians’ RR: not reported;
senior midwives’ and nurses’ RR:
70%
Kunkel et al39 United States and Canada To determine the influence of maternal 3000 neonatologists in the United Web-based survey contained 8 clinical Approval of Institutional Review Board
characteristics on neonatologists’ States and Canada. RR: 16% case vignettes portraying mother of Indiana University was obtained
recommendations for periviable (n = 471); included in the study: with different characteristics
pregnancies n = 328
Laventhal United States To determine physicians and 4450 pediatricians and obstetricians; Questionnaire included demographic Anonymity of participants and
et al40 obstetricians’ attitudes toward 743 participants: physicians data, 8 resuscitation scenarios of voluntary participation was
resuscitation of critically ill patients (n = 204), nurses (n = 539). RR: 15% incompetent critically ill patients, and ensured
(n = 695) questions about resuscitation
preferences
Lavin et al41 United States To explore health care providers’ RR: not reported Questionnaire included questions on —
opinions about resuscitation of EPIs opinions about resuscitation and
(GA 22–26 wk) counseling
Lavoie et al42 Canada To describe neonatologists’ attitudes 169 neonatologists. RR: 74% (n = 121) Phone survey questionnaire included Approval of the University of British
toward delivery room resuscitation of demographic data, whether parents Columbia’s Behavioral Research
EPIs (GA 23–26 wk) requested withholding resuscitation, Ethics Board and the Children’s and
and open-ended attitudinal questions Women’s Health Centre Research
Ethics Board was obtained
Martinez Japan, Australia, Hong Kong, To determine what factors influence 618 neonatologists in the participating Questionnaire included demographic Approval of the Research Ethics
et al43 Singapore, Taiwan, and resuscitation practices and countries. RR: 51% (n = 318) data and questions on preferred Committee of the University of
Malaysia neonatologists’ attitudes toward EPIs treatment and counseling California and at each site was
(GA 22–25 wk) obtained before the study.
McAdams Mongolia To identify factors that influence health 210 health care providers randomly Questionnaire included demographic Approval of the Institutional Review
et al44 care professionals’ practices and selected. RR: 100% (n = 210) data, vignettes, and close-ended and Board of the University of
attitudes toward parental multiple-choice questions Washington was obtained, and
involvement in neonatal resuscitation anonymity of participants and
decisions voluntary participation was

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ensured
Mills et al16 Australia To explore physicians’ attitudes toward 140 neonatologists. RR: 78% (n = 109) Questionnaire included demographic —
resuscitation of critically ill data, 8 resuscitation scenarios of
incompetent patients and toward the incompetent critically ill patients, and
best-interest standard (age of questions about resuscitation
patients: GA 24 wk–80 y) preferences

7
8
TABLE 3 Continued
Study Country Aim Sample Size and RR Data Collection Ethical Considerations
Mulvey Australia To determine obstetricians’ attitudes 187 obstetricians. RR: 48% (n = 89) Questionnaire included demographic —
et al45 toward resuscitation of EPIs and data and questions on antenatal
infants with extremely low birth wt counseling and resuscitation
Munro et al46 Australia To investigate neonatologists’ attitudes 100 neonatologists. RR: 70% (n = 70) Questionnaire included demographic —
toward antenatal counseling and data and attitudinal questions on
resuscitation for EPIs (,GA 26 wk) resuscitation and counseling
Norup47 Denmark To describe pediatricians’ attitudes 954 physicians. RR: 69% (n = 664) Questionnaire included demographic The regional Research Ethics
toward treatment of EPIs (.GA 24 data, fictional cases, and attitudinal Committee stated participant
wk) questions; 2 different versions were approval was unnecessary, and
used anonymity of participants was
ensured
Oei et al48 Australia To explore physicians’ and nurses’ 76 neonatologists and 57 nurses. Questionnaire included graded Anonymity of participants was
attitudes toward resuscitation of EPIs Neonatologists’ RR: 93% (n = 71); questions, open-ended questions, and ensured
(,GA 28 wk) nurses’ RR: 72% (n = 41) numeric responses
Partridge United States To determine factors that influence 445 neonatologists practicing in Survey included demographic data, Approval of the Committee on Human
et al49 delivery room resuscitation decisions California. RR: 61% (n = 270) multiple-choice and open-ended Research of the University of
for EPIs (,GA 26 wk) questions on resuscitation of EPIs, California was obtained, and
counseling, and threshold of viability anonymity of participants was
ensured
Partridge South Africa To explore physicians’ attitudes toward 394 practicing pediatricians and Questionnaire included demographic Approval of the Research Ethics
et al50 life support and counseling for EPIs neonatologists. RR: 24% (n = 93) data and attitudinal questions on Committee and the University of
(GA 23–30 wk) counseling, management of delivery, Witwatersrand Institutional Review
and resuscitation Board was obtained, and anonymity
of participants was ensured
Partridge United States To describe neonatologists’ perceptions 376 neonatologists in California. RR: Questionnaire included a copy of the Approval of the Research Ethics
et al51 of the Born-Alive Infants Protection 44% (n = 156) Born-Alive Infants Protection Act, Review Board of the University of
Act for EPIs (GA 20–24 wk) demographic data, and questions on California was obtained, and
current and future practices anonymity of participants and
regarding counseling and voluntary participation was
resuscitation ensured
Peerzada United States To explore neonatologists’ attitudes 175 practicing level II and III Cross-sectional survey contained close- Approval of the Committee on Clinical
et al52 toward parental wishes regarding neonatologists. RR: 85% (n = 149) ended questions on threshold for Investigation at Children’s Hospital
resuscitation of EPIs (GA 22–26 wk) intervention, vignettes, and attitudinal Boston was obtained, and
questions anonymity of participants was
ensured
Peerzada Sweden To explore neonatologists’ attitudes 124 neonatologists. RR: 71% (n = 88) Cross-sectional survey contained close- Approval from the Research Ethics
et al53 toward parental wishes regarding ended questions on threshold for Committee of Umeå University was
resuscitation of EPIs (GA 22–26 wk) intervention, vignettes, and attitudinal obtained, and anonymity of
questions participants was ensured
Ramsay and United States To understand physicians’ definition of 73 neonatologists and obstetricians. Phone survey; 2 different versions were Approval of Columbia University

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Santella54
Singh et al55 United States
live birth/fetal death and their
attitudes toward resuscitation of EPIs
(,GA 24 wk)
RR: 79% (n = 58) used
Questionnaire included 4 different
scenarios and attitudinal questions
Medical Center’s Institutional
Review Board was obtained, and
anonymity of participants was
ensured

CAVOLO et al
 which a young married couple mean threshold between GA 22 and

Hospital Institutional Review Board

Board of the University of Chicago 24 weeks35,43,45,51 with few

Approval of the Children’s Memorial

Approval of the Institutional Review
struggled over the resuscitation
decision of their 25-week-old infant. exceptions. In the international
Ethical Considerations

Only 63% of pediatricians and 65% of study of Martinez et al,43 physicians

obstetricians would resuscitate in in Japan set a lower threshold

—
this case. (GA 21–22 weeks), whereas
physicians in Malaysia43 and South
was obtained

was obtained

GA 26 and 27 Weeks Africa50 set a higher threshold (GA

Between 95% to 100% and 100%, 25 weeks).
respectively, would resuscitate EPIs
at GA 26 weeks38,41,48,55 and GA 27 Physicians’ Attitudes Toward
weeks.38,48 Few (0%–1% and 0%)
Semistructured interviews (20–60 min)

Parents’ Requests for Resuscitation

27-item survey included demographic

would not resuscitate at GA 2638,41,48 or Nonresuscitation

data and attitudinal questions

or 27 weeks.38,48 In 13 studies, researchers

Data Collection

Attitudes According to Threshold for investigated physicians’ attitudes

Resuscitation
In 6 studies, researchers investigated
what physicians considered to be the
lower GA threshold for resuscitation.
None of the physicians surveyed
would set the threshold below GA
and/or gynecologist registrars and
toward parents’ requests to
resuscitate or to not resuscitate their
EPI. Some investigators examined
attitudes according to GA, whereas
others examined attitudes according
to thresholds for accepting or
refusing the parents’ requests

22 weeks, and only rarely would

500 neonatologists in 2003; RR: 63%

16 neonatal pediatric and obstetric

(n = 304); 550 neonatologists in

(Table 7).
they set the threshold above GA
129 neonatologists practicing in
Sample Size and RR

24 weeks.
Illinois. RR: 66% (n = 85)
1996; RR: 66% (n = 362)

Attitudes Toward Parental Requests

Most of the physicians surveyed set According to GA
the resuscitation threshold between In 3 studies,27,31,42 physicians were
GA 22 weeks and GA 24 weeks. It
consultants

asked whether they would refuse the

ranged from 0% to 55% at 22
weeks,29,34,48,49,56 11% to 40% at 23
weeks,34,48,49,56 and 2% to 78% at 24
weeks.34,48,49,56 Whereas these
resuscitation decisions for EPIs (,GA
preferences for EPIs born in the gray
parents’ request to resuscitate or not
resuscitate their EPI, whereas in 6
studies, physicians were asked whether
they would accept a nonresuscitation

studies varied greatly, in 1 study, 97%

reasoning in decisions concerning

request.16,25,32,36,40,42 Regardless of the

treatments for EPIs and abortion
To determine physicians’ treatment

of physicians set the resuscitation

To explore factors that influence

To investigate physicians’ ethical

form of the question, the data clearly

threshold at GA 23 weeks.54 The reveal that physicians were less
authors of this study sampled opinions willing to accept a nonresuscitation
zone (GA 23–26 wk)

of 58 obstetricians and neonatologists

Aim

request as GA increased. Likewise,

practicing in 34 hospitals with NICUs in they were less likely to refuse
New York City.54 a resuscitation request as GA
28 wk)

Few physicians set the threshold increased. Similarly, as GA increased,

above GA 24 weeks: 0% to 10% set physicians were more willing to
the threshold at 25 weeks,34,49,56 0% deny a nonresuscitation request
to 1% at 26 weeks,34,49,56 and 0% at (Fig 3).
27 weeks.49,56 Bell et al,29 analyzing
the attitudes of 95 Romanian GA 22 Weeks
Country

neonatologists, found that 27% of At GA 22 weeks, only 1% of

RR, response rate; —, not applicable.
Weiss et al56 United States

New Zealand

physicians set the resuscitation physicians would refuse parents’

threshold at GA 26 weeks, below which nonresuscitation request, whereas
they would refuse to resuscitate. 42% would refuse a resuscitation
TABLE 3 Continued

In 5 studies, researchers request.31 By contrast, the Arzuaga

determined which week was et al27 study on the attitudes of
et al57
Qualitative

Collyns

selected on average as the threshold Muslim physicians found that 44% of

study
Study

for resuscitation. In the majority of physicians would refuse parents’

those studies, researchers set the nonresuscitation requests.

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PEDIATRICS Volume 143, number 6, June 2019 9
TABLE 4 Assessment of Quantitative Studies Using Specific Appraisal Criteria
Study (n = 33) Hawker et al23 Criteriaa
1 2 3 4 5 6 7 8 9 Overall Assessment (Out
Abstract Introduction Method Sampling Data Ethics Results Transferability Implications of 36 Possible Points)
and Title and Aims and Analysis and Bias or and
Data Generalizability Usefulness
Armstrong Good Fair Good Fair Poor Poor Good Good Fair Moderate
et al25
Arzuaga and Good Good Good Good Fair Fair Good Good Fair High
Meadow26
Arzuaga et al27 Fair Good Good Good Good Poor Good Good Good High
Ballard et al28 Good Good Good Fair Good Fair Good Good Good High
Bell et al29 Fair Fair Poor Fair Very Poor Good Fair Good Moderate
poor
Charafeddine Good Good Good Good Fair Fair Good Good Fair High
et al30
Cummings et al31 Good Good Good Fair Very Poor Fair Fair Fair Moderate
poor
De Leeuw et al32 Good Good Good Good Good Poor Good Good Poor High
Duffy and Fair Fair Good Good Fair Fair Good Fair Fair High
Reynolds33
Geurtzen et al34 Fair Good Good Good Fair Fair Good Fair Fair High
Gooi et al35 Good Poor Good Good Fair Poor Good Fair Good High
Hansen et al36 Good Good Good Good Poor Very poor Good Good Good High
Kariholu et al37 Fair Good Fair Fair Very Poor Good Poor Fair Moderate
poor
Khan et al38 Good Good Fair Fair Fair Poor Good Fair Poor Moderate
Kunkel et al39 Good Good Good Good Good Fair Good Good Fair High
Laventhal et al40 Good Fair Good Fair Fair Fair Good Fair Fair High
Lavin et al41 Good Fair Fair Fair Poor Very poor Good Fair Fair Moderate
Lavoie et al42 Good Fair Fair Good Good Poor Good Fair Fair High
Martinez et al43 Good Good Good Fair Fair Fair Fair Fair Poor Moderate
McAdams et al44 Good Good Good Fair Fair Fair Good Fair Fair High
Mills et al16 Fair Good Good Poor Very Very poor Fair Fair Poor Low
poor
Mulvey et al45 Fair Fair Poor Fair Very Very poor Good Poor Poor Low
poor
Munro et al46 Poor Good Poor Poor Very Very poor Good Poor Fair Low
poor
Norup, 199847 Fair Fair Fair Good Fair Fair Good Fair Fair Moderate
Oei et al48 Good Fair Fair Poor Poor Poor Fair Poor Poor Low
Partridge et al49 Good Fair Fair Good Very Good Good Fair Good High
poor
Partridge et al50 Fair Poor Fair Fair Fair Fair Good Poor Good Moderate
Partridge et al51 Good Good Fair Fair Good Good Good Fair Fair High
Peerzada et al52 Good Good Good Good Good Fair Good Good Fair High
Peerzada et al53 Fair Fair Good Good Good Fair Good Fair Fair High
Ramsey and Fair Poor Fair Good Very Good Fair Fair Fair Moderate
Santella54 poor
Singh et al55 Good Good Good Good Good Fair Fair Good Fair High
Weiss et al56 Fair Fair Fair Fair Fair Fair Good Fair Poor Moderate
The specific appraisal criteria are from Hawker et al.23 Scoring: good = 4; fair = 3; poor = 2; very poor = 1.
a Hawker et al23 appraisal questions: (1) Did they provide a clear description of the study? (2) Was there a clear background and a clear statement of the aims of the research? (3) Is the

method appropriate and clearly explained? (4) Was the sampling strategy appropriate to address the aims? (5) Was the description of the data analysis sufficiently rigorous? (6) Have
ethical issues been addressed, and what has necessary ethical approval gained? (7) Is there a clear statement of the findings? (8) Are the findings of this study transferable
(generalizable) to a wider population? (9) How important are these findings for policies and practice?

GA 23 Weeks a resuscitation request at GA Again, the Arzuaga et al27

Seven percent to 43% of physicians 23 weeks. 31 In 1 study, researchers report was an exception,
would refuse a nonresuscitation reported that 98% of physicians with 46% of physicians
request for EPIs, 31,33 and 7% would accept a parental refusing a nonresuscitation
of physicians would refuse nonresuscitation request. 42 request.

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10 CAVOLO et al
 TABLE 6 Summary of Physicians’ Attitudes Toward Resuscitation and Nonresuscitation of EPIs

appropriate to the aims? (5) Were the data collected in a way that addressed the research issue? (6) Was the relationship between researcher and participants adequately considered? (7) Were ethical issues taken into consideration? (8) Was the
a CASP24 appraisal questions: (1) Was there a clear statement of the aims of the research? (2) Was a qualitative methodology appropriate? (3) Was the research design appropriate to address the aims? (4) Was the recruitment strategy
According to GA
Assessment
(Out of 30
Possible)
Overall

High
GA, wka Resuscitation, % Nonresuscitation, % Threshold for Resuscitation, %b
22
Range 0–4.437,38,41,48 85–10033,37,38,41,46,48 0–5529,34,48,49,56
Exception 5127 4927 —
Research
Valuable
Was the

23
Yes
10

Range 4–4728,38,41,48,55 57–81.938,41,48,55 11–4034,48,49,56

Exception 8527 1527 9754
24
38–9916,25,32,33,36–38,40,41,48,55 2–27.232,38,41,46,48,55 2–7834,48,49,56
of Findings
Statement

Range
Clear

Exception — 6332 —
Yes
9

25
Range 85.4–10038,41,48,55 0–4.238,41,48,55 0–1034,49,56
Exception 63 and 6547 — —
Data Analysis
Sufficiently

26
Rigorous

95–10038,41,48,55 0–138,41,48 0–134,49,56

Yes

Range
8

Exception — — 2729
27 100 yes38,48 0 no38,48 049,56
—, not applicable.
Considered

a GA refers to the number of complete wk of gestation. For example, a GA of 22 wk spans from 220 to 226.
Ethical
Issues

No
7

b Threshold for resuscitation refers to the lowest GA below which physicians would not resuscitate.
data analysis sufficiently rigorous? (9) Was there a clear statement of findings? (10) How valuable was the research? Scoring: yes = 3; unclear = 2; no = 1.

GA 24 Weeks countries, only physicians who stated

Relationship Between Researcher

they would resuscitate EPIs were also

Adequate Consideration of the

In 1 study, 53% of physicians would

refuse a parental nonresuscitation asked whether they would accept
and Participants

request, but only 1% would refuse a nonresuscitation request; 6% to

a resuscitation request at GA 24 40% indicated that they would.32
No
6

weeks.31 In other studies,

CASP Criteriaa

researchers report that 65% to 94% GA 25 Weeks

of physicians would accept More physicians would refuse
a nonresuscitation request.16,25,36,40, a nonresuscitation request
42
In the study of 11 European (41%–61%) at GA 25 weeks.31,42
Appropriate

Collection
Data

Yes
5
TABLE 5 Assessment of Qualitative Study Using the Appraisal Criteria of CASP

Recruitment
Appropriate

Strategy

Unclear
4
Clear Statement Appropriate Appropriate
Design

Yes
3

Methodology

Yes
2

of Aims

Yes
1

et al57

FIGURE 2
Collyns

Physicians’ attitudes toward resuscitation and nonresuscitation of EPIs. Some researchers report
n=1
Study

data on physicians’ attitudes toward both resuscitation and nonresuscitation. Such studies are
represented by multiple dots.

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PEDIATRICS Volume 143, number 6, June 2019 11
TABLE 7 Physicians’ Attitudes Toward Parents’ Resuscitation or Nonresuscitation Requests
GA, General Attitudes Toward Parents’ Requests Threshold for Accepting or Refusing Parents’ Requests
wk Refused Parents’ Refused Parents’ Accepted Parents’ Youngest GA for Oldest GA for Youngest GA for Oldest GA for
Nonresuscitation Resuscitation Nonresuscitation Refusing Parents’ Accepting Parents’ Accepting Parents’ Refusing Parents’
Request, % Request, % Request, % Nonresuscitation Nonresuscitation Resuscitation Resuscitation
Request, % Request, % Request, % Request, %
22 131; exception: 4427 4231 — Range: 0–126,56 052,53 Range: 12–2126,52, 4056
53

23 Range: 7–4331,33; 731 9842 Range: 5–1526,56 Range: 37–6152,53 Range: 60–8426,52, 3056
exception: 4627 53

24 5331 131 Range: 65–9416,25,36, Range: 27–2926,56 Range: 30–5052,53 Range: 3–1526,52,53 956
40,42
; exception:
6–4032
25 Range: 41–6131,42 031 2442 Range: 30–5026,56 Range: 6–1352,53 Range: 0–226,52,53 256
26 Range: 64–8231,42 031 — Range: 15–2326,56 Range: 0–352,53 026,52,53 256
27 6431 031 — Range: 1–226,56 — — 056
—, not tested.

None of the physicians would refuse
parents’ resuscitation requests,31 and
only 24% of physicians would accept
a nonresuscitation request.42
GA 26 to 27 Weeks
The majority of physicians would
refuse a nonresuscitation request for
infants as old as GA 26 and 27 weeks;
this ranged from 64% to 82%31,42
and 64%,31 respectively. None of the
physicians would refuse parents’
resuscitation request in this range
of GA.31
61%.52,53 From GA 24 weeks, the
percentage declines until reaching
0% again at 26 weeks.52,53
In 3 studies,26,52,53 researchers
sought to determine the lowest GA at
which physicians would accept
parents’ resuscitation requests. In
those studies, 12% to 84% of the
physicians set the minimum age for
resuscitation between GA 22 and 23
weeks, with more physicians leaning
toward 23 weeks as the lower limit
for resuscitation. The percentage
dropped as the GA of the infant
increased, going from 3% to 15% for
GA 24 weeks to 0% for GA 26 weeks.
Among the neonatologists surveyed
in Weiss et al,56 40% would refuse to
resuscitate EPIs with a GA of 22
weeks, but 0% would refuse to
resuscitate infants born at GA 27
weeks. The results of these studies
indicate that the physicians surveyed

Attitudes According to Threshold for

Accepting or Refusing Parents’ Requests
for Resuscitation or Nonresuscitation
This threshold was defined as the
lowest GA at or below which
resuscitation should be consistently
withheld.56 For parental
nonresuscitation requests of infants
at GA 22 weeks, virtually no physician
(0%–1%) considered this GA to be
a threshold for refusing
nonresuscitation requests.26,56 The
percentage sharply increased to 30%
to 50% of physicians setting the
threshold at GA 25 weeks; the
percentage decreased for those
setting the threshold at 26 weeks.26,56
No physician considered GA 22 weeks
as the oldest age for accepting
nonresuscitation requests. The
majority of physicians placed such FIGURE 3
Physicians’ attitudes toward parents’ resuscitation or nonresuscitation requests. Some researchers
a GA threshold at 23 weeks, with the report data on physicians’ attitudes toward both parents’ request for resuscitation and parents’
percentage ranging from 37% to request for nonresuscitation. Such studies are represented by multiple dots.

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12 CAVOLO et al
seem to set the lower limit for
resuscitation at GA 22 to 23 weeks
and the upper limit for refusing to
resuscitate between 24 and 25 weeks.
Influence of Physicians’
Demographic Characteristics
In 10 studies, researchers
investigated possible correlations
between physicians’ demographic
characteristics and their attitudes
toward resuscitation, nonresuscitation
(n = 8),26,30,32,34,38,41,49,51 and parents’
requests for resuscitation and
nonresuscitation (n = 2).27,42
Demographic Characteristics and
Attitudes Toward Resuscitation
In 2 studies, researchers found
a statistically significant correlation
between physicians’ specialty and
their attitudes. Obstetricians were
more likely to recommend
resuscitation for very young EPIs
than neonatologists34 and
pediatricians.41 Only De Leeuw et al32
found a statistically significant
correlation between attitudes and
physicians’ parental status and
religiosity. Physicians with children
and physicians who were religious
were more willing to resuscitate EPIs.
Partridge et al51 found a significant
correlation with physicians’ age and
work setting. Older physicians and
those working in private hospitals set
higher GA thresholds for
resuscitation. Finally, Arzuaga and
Meadow26 found a statistically
significant correlation between
physicians’ attitudes and different
abortion legislations. US physicians
working in states prohibiting
abortion after GA 23 weeks were less
likely to think that resuscitation
should be mandatory at GA 24 weeks
(Table 8).
In several studies, researchers found
that physicians’ years of
experience,30,32,34,49 sex,30,49
identification as pro-choice or pro-
life,26,51 and level of NICU30,49 did not
have a significant impact on
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PEDIATRICS Volume 143, number 6, June 2019
physicians’ attitude toward
resuscitating EPIs (Table 8).
Impact of Physicians’ Characteristics on
Attitudes Toward Parental Requests
Arzuaga et al27 analyzed whether
different measures of religiosity
influenced Muslim physicians’
decision to accept nonresuscitation
requests from parents. A higher
frequency of Quran reading was
associated with a higher likelihood of
resuscitating an EPI against parents’
requests for infants at GA 22 weeks
(odds ratio [OR]: 7.6; P , .001) and
23 weeks (OR: 4.55; P = .003).27 In
addition, a higher attendance at
congregational worship services was
associated with a higher probability
of resuscitating an EPI against
parents’ request for infants at GA
23 weeks (OR: 5.3; P = .006). Lavoie
et al42 observed a statistically
significant correlation between
physicians’ willingness to accept
a parental request and physicians’
personal experience with disability.
Physicians having personal
experience with disabled persons
were more likely to accept parents’
request to not resuscitate (90% vs
71%; P = .01). No significant
correlations were found with age, sex,
country, years of practice, and
parental status.42
Influence of Case-Related Factors on
Physicians’ Attitudes
In 19 studies, researchers
investigated the influence of case-
related factors on physicians’
attitudes toward resuscitation and
nonresuscitation (n = 17)* and
parents’ requests for resuscitation
and nonresuscitation (n = 6).30,33,46,52,
53,57
Impact of Case-Related Factors on
Attitudes Toward Resuscitation
Singh et al55 classified case-related
factors as 2 categories: patient-
related factors (eg, condition at birth)
and non–patient-related factors
* Refs 26,28,30,34,39,42–44,46–49,52,53,55,57.
(eg, resource allocation). Using the
same classification, we identified
a trend: although physicians
considered patient-related factors to
be important contributors in the
decision to resuscitate, non–patient-
related factors were rarely
considered important contributors to
the decision-making.
The main factors influencing
physicians’ attitudes toward
resuscitation or nonresuscitation
were EPIs’ medical condition at
birth,26,42,48,52,53,55 presence of
congenital anomalies,34,42,43,45,49
probability of death or survival,30,43,
45,46,52,53,55
probability of future
disability,30,52,53 parents’ wishes,26,30,
43,45,48,49
and quality of life.43,49,57
The factors that were deemed less
relevant in the decision-making
process were emotional or financial
burden to the family,43,45,46,52,53
health care resource allocation,43,45,46,
49,55,57
and fear of litigation.43,45,46,49,
55
Only in the study of Lebanese
neonatologists’ attitudes30 did
researchers find that health care
resource allocation was ranked
second as an influencing factor.
Authors of another study found
that fear of litigation was an
important, although subtle, factor that
influenced physicians’ decision to
resusciate.28
Finally, in 3 studies, researchers
found that maternal characteristics
can also influence physicians’
attitudes toward resuscitation. In
Kunkel et al,39 parity, planned
pregnancy, and race had a statistically
significant impact on physicians’
willingness to resuscitate an EPI.
Similarly, in 2 studies in which
physicians were asked to give
opinions on 2 scenarios in which
EPIs’ characteristics remained
constant but maternal characteristics
(eg, age, marital status, parity) varied,
maternal characteristics were found
to significantly affect physicians’
willingness to resuscitate.44,47
13
TABLE 8 Correlations Between Physician Demographics, Non–Case-Related Variables, and Physicians’ Attitudes Toward Resuscitation and
Nonresuscitation
Age Sex Has Religiosity Pro-choice Years of Health Care Specialty Level of Public Abortion
Children Versus Pro- Experience NICU Versus Law
life Private
Hospital
Arzuaga and — — — NS NS — — — — P , .05
Meadow26
Charafeddine NS NS NS NS — NS — NS — —
et al30
De Leeuw et al32 — — P = .05 P = .008 — NS — — — —
Geurtzen et al34 NS — — — — NS P = .028 — — —
Khan et al38 — — — — — — NS — — —
Lavin et al41 — — — — — — 22 wk: P = .0003; 23 wk: — — —
P = .0008a
Partridge et al49 NS NS — — — NS — NS NS —
Partridge et al51 P= — NS NS NS — — — P = .01 —
.02
NS, no significant correlation found or no numerical data reported; —, not tested.
a Statistical correlations between specialty and attitudes have been tested and reported according to the different GAs.

Impact of Case-Related Factors on
Attitudes Toward Parental Requests
A number of studies observed that
physicians were willing to resuscitate
an EPI, even against parents’
requests, in cases in which
resuscitation would be clearly
beneficial or when parents were
unsure about resuscitation.30,33,52,53
In 2 studies, researchers reported
that parental influence is limited
when there is a high likelihood of bad
or good outcomes, especially at GA 22
and 25 weeks.46,57
DISCUSSION
Physicians’ Attitudes Toward
Resuscitation and Nonresuscitation
The results of this systematic review
reveal that the GA at birth of EPIs
greatly influences physicians’
attitudes toward resuscitation and
nonresuscitation and accepting or
refusing parents’ requests for or
against resuscitation. Physicians’
willingness to resuscitate, to accept
parents’ resuscitation requests, and
to refuse parents’ nonresuscitation
requests increases with increasing
GA. This trend is consistent with the
majority of clinical practice
guidelines, which advise comfort care
at GA 22 weeks and active treatment
at GA 24 to 26 weeks.18,59,60
Our results confirm other research18
that physicians’ views on
resuscitation and on parents’
requests to resuscitate or not vary
greatly when analyzing the 23-to-24-
week GA period, constituting a “gray
zone” of uncertainty. This uncertainty
reflects a lack of consensus among
physicians. Guidelines vary widely for
infants born in the GA 23-to-24-week
range compared with other GAs.18,59
Guidelines also tend to endorse
a more individualized approach to
treatment rather than advising strict
resuscitation or nonresuscitation
efforts.18,59–61 The existence of the
gray zone is also supported by our
finding that individual physicians’ GA
threshold for initiating resuscitation
is typically placed between GA 22 and
24 weeks.
We found 2 exceptions to these
trends.27,32 First, De Leeuw et al32
reported that Dutch physicians are
less willing to resuscitate an EPI of
GA 24 weeks than physicians from
other European countries. This is
consistent with 1992 Dutch
guidelines stating that the
resuscitation threshold is a GA of 26
weeks.62 In 2010, the Netherlands
developed new guidelines advising
active treatment from GA 24 weeks.63
This recommendation may have
contributed to a greater willingness
to resuscitate at this GA. Indeed,
according to Geurtzen et al,34 78% of
the physicians surveyed set the
resuscitation threshold at GA 24
weeks. Second, Arzuaga et al27
reported that Muslim physicians had
a greater willingness to resuscitate
EPIs at GA 22 and 23 weeks, even
against parental requests for
nonresuscitation. Physicians’ greater
religiosity was associated with
a greater willingness to resuscitate.
De Leeuw et al32 also confirmed these
results.
Influencing Factors
Our results revealed that physicians
deem non–patient-related factors less
relevant than patient-related factors
in helping them decide whether to
resuscitate EPIs. However, these
non–patient-related factors were
studied only superficially.
Complicating the picture is that self-
reported attitudes may be subject to
social desirability bias28; thus,
physicians’ attitudes summarized
here may not correspond to their
actual behavior in practice.
Researchers investigating the

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14 CAVOLO et al
variability of physicians’ attitudes
influenced by non–patient-related
factors found that maternal
characteristics39,44,47 and fear of
litigation28 greatly affected
physicians’ attitudes. We also
found that certain physicians’
demographic characteristics also
have an impact, suggesting that an
interplay of various factors, rather
than GA alone, influences
physicians’ attitudes. Therefore,
physicians’ attitudes in this area
should be viewed as a multifaceted
phenomenon. This is in accordance
with a subset of the ethical
literature affirming that
consideration of GA alone is not
sufficient in deciding whether to
resuscitate EPIs.64–68 In fact, GA is
just 1 of the many factors that can
influence the prognosis.65 Moreover,
GA estimates are imprecise, having
a margin of error of 2 weeks; thus,
basing a decision solely on GA
carries the risk of not resuscitating
viable infants.66–68
The majority of included studies
(n = 23) included questionnaires
structured around GA as the variable
of interest. Doing so implies that GA is
the primary factor directing the
decision-making process. This leads
to a reductionist approach in
determining physicians’ attitudes
toward resuscitation or
nonresuscitation decisions. The
majority of questionnaires used in the
included studies were composed of
yes or no and multiple-choice
questions. Choosing from a set of
predetermined answers also
contributed to an oversimplified
description of reality. Physicians’
attitudes were described as being
either for or against resuscitation at
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2019 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
FUNDING: Funded by a grant from the Research Foundation (Flanders).
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.
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PEDIATRICS Volume 143, number 6, June 2019
the given GAs without investigating
the reasoning behind the attitudes
further.
Quantitative methodologies are well
suited to reveal general attitudinal
tendencies, but the rigid structure of
quantitative assessment instruments
also blurs a full description of the
complexities behind such attitudes.
Therefore, they are best
complemented with qualitative
research to gain in-depth insight into
the multifaceted reality,69 such the
reasons behind physicians’ attitudes
toward resuscitation. Only 1
qualitative study57 emerged from our
literature search, confirming the
urgency for more qualitative research
in the field.
Limitations and Strengths
Some limitations must be noted. First,
the inclusion of solely English-
language articles may mean that
results of some relevant studies may
have been overlooked, potentially
limiting the generalizability of our
results. Second, only 1 study set in
a low-income country44 (Mongolia)
was included, which may have
further limited the generalizability of
the results and introduced cultural
bias. Third, because only 1
qualitative study emerged in our
search, the nuanced reality behind
physicians’ attitudes remains
obscure.
The main strength of our review
resides in the large number of eligible
studies originating from 27 countries
spread across the globe. Thus, our
review is based on data extracted
from a wide variety of cultures and
legislative systems. In addition,
a significant number of studies
provided direct information on the
main themes of the review: attitudes
toward resuscitation and
nonresuscitation (n = 19), attitudes
toward parents’ resuscitation and
nonresuscitation requests (n = 13),
and demographic (n = 11) and case-
related (n = 20) influencing factors.
Finally, physicians’ attitudes on
resuscitation of EPIs were examined
from different perspectives, leading
to a focused description of physicians’
attitudes.
CONCLUSIONS
Our results reveal that a diverse
group of physicians believe that
EPIs should not be resuscitated at
GA 22 weeks, whereas they should
always be resuscitated from GA 25
weeks. Our results confirm that the
gray zone of uncertainty is 23 to
24 weeks for resuscitation attitudes.
Although the included studies are
focused on GA, we suggest that an
interplay of factors, rather than
the GA alone, influences physicians’
attitudes, highlighting the lack
of understanding of the complex
and nuanced reality behind the
attitudes toward resuscitation
of EPIs.
ABBREVIATIONS
CASP: Critical Appraisal Skills
Programme
EPI: extremely premature infant
GA: gestational age
OR: odds ratio
PRISMA: Preferred Reporting
Items for Systematic
Reviews and Meta-
Analyses
15
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 Physicians' Attitudes on Resuscitation of Extremely Premature Infants: A
Systematic Review
Alice Cavolo, Bernadette Dierckx de Casterlé, Gunnar Naulaers and Chris Gastmans
Pediatrics 2019;143;
DOI: 10.1542/peds.2018-3972 originally published online May 10, 2019;

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 Physicians' Attitudes on Resuscitation of Extremely Premature Infants: A
Systematic Review
Alice Cavolo, Bernadette Dierckx de Casterlé, Gunnar Naulaers and Chris Gastmans
Pediatrics 2019;143;
DOI: 10.1542/peds.2018-3972 originally published online May 10, 2019;

The online version of this article, along with updated information and services, is
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