Virchows Archiv

https://doi.org/10.1007/s00428-020-03002-4

ORIGINAL ARTICLE

Diagnostic discrepancies between antemortem clinical diagnosis

and autopsy findings in pediatric cancer patients
Nikhil Raghuram 1 & Khalid Alodan 2 & Ute Bartels 1 & Sarah Alexander 1 & Jason D. Pole 3 & Paul Gibson 4 &
Donna L. Johnston 5 & Carol Portwine 6 & Mariana Silva 7 & Lillian Sung 1,8

Received: 26 September 2020 / Revised: 12 December 2020 / Accepted: 18 December 2020

# Crown 2021

Abstract
Prevalence of discrepancies between antemortem clinical diagnoses and postmortem autopsy findings is uncertain in pediatric oncology
given improving diagnostic capabilities over time. Primary objective was to describe discrepancies between antemortem and postmortem
diagnosis of pediatric cancer deaths. Secondary objective was to compare clinical characteristics of deaths with and without major
diagnostic discrepancies. This was a retrospective study that included pediatric cancer patients diagnosed and treated in Ontario and who
died from 2003 to 2012. Antemortem clinical diagnoses associated with mortality were determined by reviewing the patient’s health
records 2 weeks prior to death while the postmortem diagnoses were determined by the autopsy report. Discrepancies among these
diagnoses were classified using the Goldman criteria where major discrepancies were directly related to the cause of death in contrast to
minor discrepancies. Among the 821 patients who died, 118 (14%) had an autopsy and were included. Of these autopsies, 12 (10%) had
a major diagnostic discrepancy between antemortem and postmortem diagnoses. Major discrepancies consisted of opportunistic infec-
tions (n = 5), missed cancer diagnosis (n = 3), and organ complications (n = 4). Death in a high acuity setting (12/12, 100% vs. 60/106,
57%; P = 0.003) and treatment-related mortality (12/12, 100% vs. 60/106, 57%; P = 0.003) were significantly associated with major
discrepancy. Major diagnostic discrepancy was found in 10% of pediatric oncology autopsies. Missed infections and organ complica-
tions were predominant etiologies. Death in a high acuity setting and treatment-related mortality were associated with major diagnostic
discrepancies. Autopsies continue to be important for improving diagnostic insight and may improve future clinical care.

Keywords Autopsy . Diagnostic discrepancy . Pediatric oncology . Cancer . Clinical decisions

* Lillian Sung Background

lillian.sung@sickkids.ca
Pediatric cancer survival has improved significantly over the
1
Division of Haematology/Oncology, The Hospital for Sick Children, past several decades, with 5-year overall survival rates ex-
555 University Avenue, Toronto, ON M5G 1X8, Canada
ceeding 80% in high-income countries [1]. Despite the suc-
2
Division of Pediatric Medicine, The Hospital for Sick Children, cesses, approximately 20% of children diagnosed with cancer
University of Toronto, Toronto, Ontario, Canada
will not survive due to progressive cancer or treatment-related
3
Centre for Health Services Research, The University of Queensland, mortality [2]. In addition, during the most recent 10 years,
Brisbane, Australia
improvement in survival has started to plateau [3]. This find-
4
Division of Haematology/Oncology, McMaster Children’s Hospital, ing has prompted the need for innovative therapeutic strate-
1280 Main St West, Hamilton, Ontario L8N 3Z5, Canada
gies as well as an urgent need to understand the causes of
5
Division of Hematology/Oncology, Children’s Hospital of Eastern death in an effort to improve survival rates.
Ontario, 401 Smyth Rd, Ottawa, Ontario K1H 8L1, Canada
Medical autopsy remains an important procedure to estab-
6
Department of Pediatrics, McMaster Children’s Hospital, 1280 Main lish postmortem diagnosis and detect clinically missed diag-
St West, Hamilton, Ontario L8N 3Z5, Canada
nosis, thus supporting quality assurance [4–6]. While some
7
Department of Pediatrics, Kingston General Hospital, 76 Stuart St, studies have evaluated the prevalence of diagnostic discrep-
Kingston, Ontario K7L 2V7, Canada
ancies identified by autopsy in general and among adults with
8
Child Health Evaluative Sciences, The Hospital for Sick Children, cancer, there are a limited number of studies that have
Peter Gilgan Centre for Research and Learning, Toronto, Ontario,
Canada
assessed diagnostic discrepancies in pediatric oncology

patients [4, 7, 8]. Evaluating diagnostic discrepancies between
antemortem and postmortem cause of death in pediatric on-
cology is important as in this setting, treatment-related mor-
tality can be prevalent [9, 10], and identifying patterns of
diagnostic discrepancies may impact diagnostic testing in crit-
ically ill patients. Better identification of underlying processes
that could contribute to mortality may improve care and out-
comes, potentially increasing survival rates.
Consequently, our primary objective was to describe dis-
crepancies between the antemortem and postmortem diagno-
sis of pediatric cancer deaths. Secondary objective was to
compare clinical characteristics of deaths with and without
major diagnostic discrepancies.
Methods
This study was approved by the Research Ethics Board at The
Hospital for Sick Children (SickKids) and all participating
centers. Given the retrospective nature of the study, the re-
quirement for informed consent was waived by the SickKids
Research Ethics Board.
Setting and patients There are five centers that treat children
with cancer in Ontario, namely London Health Sciences
Centre (London), Hamilton Health Sciences Centre
(Hamilton), SickKids (Toronto), Cancer Centre of
Southeastern Ontario at Kingston (Kingston), and Children’s
Hospital of Eastern Ontario (Ottawa). These centers report
cancer incidence, treatment, and outcome data to a provincial
population-based cancer registry named the Pediatric
Oncology Group of Ontario (POGO) Networked
Information System (POGONIS). For this study, we included
all deaths reported to POGONIS from January 1, 2003, to
December 31, 2012, for patients who were ≤ 18 years of age
at the diagnosis of cancer. Patients who were not seen within
1 year or no longer cared for by a POGO center and who died
in a non-POGO center were excluded (as antemortem diagno-
sis could not be retrieved). Evaluable autopsies were defined
as eligible deaths in which an autopsy was performed and in
which the report was available in the medical records.
Research only autopsies and coroner cases in which results
were withheld were excluded.
Design This analysis was a component of a study aimed at
defining and describing treatment-related mortality in pediat-
ric cancer patients [10, 11]. For this study, occurrence of an
autopsy and the autopsy report itself was collected. We first
described the percentage of deaths in which an autopsy was
performed, both overall and by year of death. Next, we fo-
cused on cases in which an autopsy was performed to deter-
mine whether there was a discrepancy between the antemor-
tem diagnosis and postmortem diagnosis.
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A discrepancy in diagnosis was defined as when the autopsy
identified a diagnosis that was not suspected prior to the patient’s
death. Diagnostic discrepancies were graded based on the
Goldman criteria for autopsy discrepancies [6, 12]. With this
system, discrepancies are graded I to V where I and II are clas-
sified as “major” findings, and III and IV are classified as “mi-
nor” findings. Class V represents the lack of diagnostic discrep-
ancy, or diagnostic congruence between antemortem and post-
mortem diagnoses. Major diagnostic discrepancies were those
that were directly related to the cause of death and consisted of
class I and II discrepancies. Class I or critical diagnostic discrep-
ancies were defined as missed diagnoses that were directly relat-
ed to the cause of death, would likely have changed clinical
management, and likely would have prolonged survival if they
had been known prior to death. Class II or serious diagnostic
discrepancies were defined as missed diagnoses that were direct-
ly related to the cause of death but would not have prolonged
survival if they had been known prior to death. Correct antemor-
tem diagnosis may fail to prolong survival if there was a lack of
effective therapy available at the time, or because the patient was
already receiving appropriate therapy (for example, receiving
empiric treatment for invasive fungal disease). Minor diagnostic
discrepancies were those that were not directly related to the
cause of death and consisted of class III and IV discrepancies.
Class III diagnostic discrepancy was defined as a missed diagno-
sis that was not directly related to the cause of death but was
either symptomatic and should have been treated, or would even-
tually have affected survival. Class IV diagnostic discrepancy
was defined as a missed diagnosis that was not directly related
to the cause of death and did not meet class III criteria.
The antemortem diagnoses were determined by reviewing
the patient’s health records up to 2 weeks prior to the date of
death and included admission and discharge notes, progress
notes, clinic letters, laboratory and microbiology results, radi-
ology reports, death certificates, and notes from allied
healthcare professionals. The postmortem diagnoses were de-
termined by the autopsy report.
For classification, two investigators (NR and KA) indepen-
dently assigned the antemortem and postmortem diagnoses.
These were compared and a single set of antemortem and
postmortem diagnoses were arrived at by consensus. The
same two investigators then categorized diagnostic discrepan-
cies (classes I to V) and resolved differences by consensus.
For class I and II diagnostic discrepancies, these were present-
ed to a panel comprised of three pediatric oncologists (SA,
UB, and LS) where the overall final categorization was made
by consensus.
Statistics Descriptive statistics were used to describe the study
population, antemortem diagnosis, and postmortem diagnosis.
The Fisher’s exact test was used to compare the clinical char-
acteristics of those with major diagnostic discrepancies (clas-
ses I or II) vs. those without major diagnostic discrepancies
Virchows Arch
(classes III, IV, or V). Factors evaluated were autopsy type
(unrestricted vs. restricted), sex, age at death, year of death,
underlying cancer diagnosis, relapse status, hematopoietic
stem cell transplantation receipt, location of death (high acuity
setting defined as the emergency department, intensive care
unit or operating room vs. low acuity setting defined as ward,
home, or hospice), withdrawal of supportive care, and study-
adjudicated treatment-related mortality (defined as absence of
progressive cancer) [10]. A P value less than 0.05 was con-
sidered statistically significant. Statistical analysis was per-
formed using Graphpad Prism (version 8.4.1 for Mac,
GraphPad Software, San Diego, CA, USA, www.graphpad.
com).
Results
Between January 1, 2003, and December 31, 2012, there were
a total of 821 eligible deaths registered in POGONIS and
included in our study (Fig. 1). Among these deaths, 141 pa-
tients underwent an autopsy of which 118 patients were
evaluable and included in the final analysis. Table 1 and
Supplemental Table 1 describe the characteristics of these
patients; unrestricted autopsies comprised 67 (57%) of all au-
topsies. The most common underlying cancer diagnosis was
Fig. 1 Flow diagram of Deaths identified in POGONIS during the study period
identification and selection of
patients included in the study
Number of patients included in study
Number of eligible deaths that underwent an autopsy
Number of autopsies included in final analysis
leukemia or lymphoma in 51 (43%) patients. Overall, the pro-
portion of patients who had an autopsy was 118/821(14%),
with a range of 9–19% among the five participating centers
(Fig. 2). Between 2007 and 2012, the proportion ranged be-
tween 5/74 (7%) to 19/90 (21%) by calendar year (Fig. 3).
Among the 118 autopsies, there were 887 postmortem di-
agnoses (median 6, interquartile range 2–10 diagnoses per
death). Table 2 shows major diagnostic discrepancies
consisting of class 1 (critical) (n = 8) and class 2 (serious)
(n = 4) diagnostic discrepancies occurred in 12 patients,
resulting in a major diagnostic discrepancy prevalence of
10%. Among the 8 patients with class I (critical) diagnostic
discrepancies, 5 patients had missed infectious causes of mor-
tality. Among the 5 patients with missed infectious causes, 4
of these patients had a primary diagnosis of leukemia or lym-
phoma. The other 3 patients with class I (critical) diagnostic
discrepancies had missed diagnosis of malignancy. Table 2
also shows class II or serious diagnostic discrepancies, which
all consisted of unrecognized organ complications (n = 4).
Table 1 shows the comparison of clinical characteristics be-
tween the presence vs. the absence of a major diagnostic discrep-
ancy. Two factors were significantly associated with major diag-
nostic discrepancy, namely death in a high acuity setting (12/12,
100% among major discrepancies vs. 60/106, 57% among no
major discrepancy; P = 0.003) and study-adjudicated treatment-
(n=964)
Did not meet eligibility criteria (n=143)
>18 years at the time of diagnosis (n=1)
Died outside the study period (n=1)
Inaccurate identification of patient outcome (n=2)
Uncertain or unconfirmed cancer diagnosis (n=3)
Not seen within 1 year or no longer cared for by
POGO center and died in a non-POGO center
(n=136)
(n=821)
Number of deaths without an autopsy (n=680)
(n=141)
Excluded from analysis (n=23)
Missing/incomplete autopsy results (n=15)
Coroner case (documents withheld) (n=5)
Non-diagnostic autopsy (n=1)
Autopsy done for research purposes only (n=2)
(n=118)
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Table 1 Characteristics of pediatric cancer patients who underwent autopsy and comparison of presence vs. absence of major diagnostic discrepancy

Characteristic Total, n = 118 Number with major Number without major P value*
diagnostic discrepancy, n = 12 diagnostic discrepancy, n = 106

Autopsy type 0.550**

Unrestricted 67 (57%) 8 (67%) 59 (56%)
Restricted, all organs excluding head/neck 7 (6%) 2 (17%) 5 (5%)
Restricted, CNS only 28 (24%) 1 (8%) 27 (25%)
Restricted, specific organ systems only 16 (14%) 1 (8%) 15 (14%)
Male sex 57 (48%) 7 (58%) 50 (47%) 0.550
Age at death in years 0.743
0–5 years 46 (39%) 6 (50%) 40 (38%)
> 5–10 years 30 (25%) 2 (17%) 28 (26%)
> 10–18 years 42 (36%) 4 (33%) 38 (36%)
Year of death
2003–2007 66 (56%) 7 (58%) 59 (56%) 1.000
2008–2012 52 (44%) 5 (42%) 47 (44%)
Underlying diagnosis 0.089
Leukemia or lymphoma 51 (43%) 9 (75%) 42 (40%)
Solid tumor 29 (25%) 1 (8%) 28 (26%)
Brain tumor 38 (32%) 2 (17%) 36 (34%)
Relapse status 36 (31%) 4 (33%) 32 (30%) 1.000
Received hematopoietic stem cell transplant 32 (27%) 4 (33%) 28 (26%) 0.733
Allogeneic 24 (20%) 4 (33%) 20 (19%)
Autologous 8 (7%) 0 (0%) 8 (8%)
Location of death 0.003#
Emergency department 3 (3%) 2 (17%) 1 (1%)
Intensive care unit 68 (58%) 10 (83%) 58 (55%)
Operating room 1 (1%) 0 (0%) 1 (1%)
Ward 24 (20%) 0 (0%) 24 (23%)
Home 17 (14%) 0 (0%) 17 (16%)
Hospice 5 (4%) 0 (0%) 5 (5%)
Withdrawal of supportive care 40 (34%) 4 (33%) 36 (34%) 1.000
Study-adjudicated treatment-related mortality 72 (61%) 12 (100%) 60 (57%) 0.003
*
Groups compared using Fisher’s exact test
**
Compared unrestricted vs. restricted combined
#
Compared high acuity settings (intensive care unit, emergency room, and operating room) vs. low acuity settings (ward, home, and hospice)
CNS, central nervous system

related mortality (12/12, 100% among major discrepancy vs. 60/
106, 57% among no major discrepancy; P = 0.003).
Discussion
In this study, we found an overall autopsy prevalence of 14%
and an overall major diagnostic discrepancy prevalence of
10% among pediatric cancer patients who underwent an au-
topsy. Unrecognized infection and organ complication were
the predominant etiologies of these major diagnostic discrep-
ancies. Deaths in a high acuity setting (emergency department,
intensive care unit, or operating room) and adjudicated as
treatment-related mortality were significantly more likely to
be associated with a major diagnostic discrepancy.
Our study underscores the importance of autopsies in pro-
viding important information to clinicians caring for pediatric
oncology patients [4–6]. Our finding that missed infection was
an important contributor to diagnostic discrepancy is consis-
tent with other studies of pediatric oncology patients in which
undetected opportunistic infections, especially invasive fungal
disease, were a common contributor to major diagnostic dis-
crepancies [4, 7, 8]. We also found that undetected organ
complication is an additional key contributor to diagnostic
discrepancy. This finding is consistent with contemporary
adult oncology studies [13].
Virchows Arch

Fig. 2 Percentage of deaths

Percentage of autopsies performed per

25%
associated with autopsy among % of patients with a restricted autopsy
the five participating centers
% of patients with an unrestricted autopsy
20%

number of deaths
15%

10%

5%

0%
Site A Site B Site C Site D Site E Aggregate
Participating sites

The prevalence of major diagnostic discrepancies (10%) was
lower in our study when compared to other studies that de-
scribed estimates of 23.5% among all autopsies performed
[6], and 25% among autopsies in adult and pediatric oncology
[8, 13]. Our lower prevalence could be a reflection of improved
diagnostic tests and better antifungal and antibacterial prophy-
laxis in the past decades [14–16]. However, our study also
found a relatively low prevalence of autopsies (14%) performed
in our select patient population, with just over-half the total
number of autopsies (57%) being unrestricted. This low rate
is consistent with a single North American institution where
the autopsy rate for pediatric oncology patients was 18% [8].
Consequently, our lower prevalence of diagnostic discrepancy
may also be related to the lower rate of autopsy. Nonetheless, if
the autopsy rate were increased, it may provide more opportu-
nity to better understand the causes of death and could lead to
improved processes that impact on patient outcomes.
Despite the prevalence of diagnostic discrepancies, previ-
ous studies have failed to identify factors associated with ma-
jor diagnostic discrepancies [5, 12, 13, 17–20]. This finding
may have been related to the small number of patients
undergoing autopsy [6]. In contrast, we identified two factors
associated with major diagnostic discrepancy, namely loca-
tion of death in a high acuity setting and treatment-related
mortality. Death in high acuity settings has been studied be-
fore and no correlations with major diagnostic discrepancies
were found among pediatric patients [21]. The difference be-
tween that study and ours may be related to our focus on
pediatric oncology patients, and differences in characteristics
of diagnostic discrepancy in our population compared to a
general pediatric population. Our finding that both high acuity
settings and treatment-related mortality were associated with
diagnostic discrepancy is not surprising since we would ex-
pect them to be correlated with each other.
The strengths of this study include its multi-center na-
ture, use of two reviewers, and further adjudication of
diagnostic discrepancies by a panel of clinical oncolo-
gists. However, the retrospective nature of the study poses
some limitations. There may have been selection bias with
autopsies more likely being performed in patients with
uncertain antemortem diagnosis or with treatment-related
mortality. Furthermore, we relied on the accuracy of

Fig. 3 Percentage of deaths

Percentage of autopsies performed per

25% % of patients with a restricted autopsy

during the study period (2003–
2012) % of patients with an unrestricted autopsy
20%
number of deaths

15%

10%

5%

0%
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
Year
 Virchows Arch

Table 2 Major diagnostic

discrepancies identified from Diagnostic discrepancy Antemortem diagnosis Postmortem diagnosis n
autopsy class* and type

Class I: Critical diagnostic 8

discrepancy
Infection 5
Multi-organ failure of unknown Systemic herpes simplex virus type 1
etiology 1 infection including pneumonitis
Hepatic encephalopathy Disseminated varicella zoster 1
infection with hepatic necrosis
Hemorrhagic shock Pseudomembranous colitis 1
secondary to Clostridium difficile
Respiratory failure secondary Escherichia coli sepsis 1
to large abdominal tumor
Multi-organ failure of unknown Multi-organ candidiasis 1
etiology
Cancer diagnosis 3
Multi-organ failure of unknown Primary hemophagocytic 1
etiology lymphohistiocytosis
Pneumonia and Epstein-Barr virus Multi-organ post-transplant 1
infection lymphoproliferative disease,
diffuse large B cell lymphoma
Cerebral edema, query metabolic Diffuse neuroglial tumor 1
disorder
Class II: Serious 4
diagnostic
discrepancy
Organ complication 4
Septic shock Cardiomyopathy 1
Presumed cerebral vascular Ruptured brain aneurysm 1
thrombotic event
Infection, pneumonic process Pulmonary occlusive vasculopathy 2
*
See methods for definitions of class I and class II diagnostic discrepancies

medical records, which may not necessarily reflect the
team’s understanding and interpretation of symptoms
and signs. Finally, our rate of unrestricted autopsies was
low and thus, we may have underestimated the rate of
diagnostic discrepancies.
evaluated the manuscript. SA, UB, and LS analyzed the data. LS wrote
the manuscript. All authors read and approved the final manuscript.
Funding This study was funded by an operating grant from the Pediatric
Oncology Group of Ontario. LS is the Canada Research Chair in Pediatric
Oncology Supportive Care.

Data availability The datasets used and/or analyzed during the current
study are available from the corresponding author on reasonable request.
Conclusions

In conclusion, major diagnostic discrepancy was found in
10% of pediatric oncology autopsies. Missed infections and
organ complications were predominant etiologies. Death in a
high acuity setting and treatment-related mortality were asso-
ciated with major diagnostic discrepancies. Autopsies contin-
ue to be important for improving diagnostic insight and may
improve future clinical care.
Supplementary Information The online version contains supplementary
material available at https://doi.org/10.1007/s00428-020-03002-4.
Author’s contributions NR and KA collected and analyzed the data and
wrote the manuscript. CP, MS, PG, and DJ contributed data. JP critically
Compliance with ethical standards
Ethics approval and consent to participate This study received research
ethics board approval from the Hospital for Sick Children Research
Ethics Board (#1000041703). Given the retrospective nature of the study,
the requirement for informed consent was waived by the SickKids
Research Ethics Board.
Consent for publication Not applicable.
Competing interests The authors declare that they have no competing
interests.
Code availability Not applicable.
Virchows Arch
Abbreviations POGO, Pediatric Oncology Group of Ontario;
POGONIS, Pediatric Oncology Group of Ontario Networked
Information System
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