Classification of stillbirth by relevant condition at death (ReCoDe): population based cohort study
BMJ 2005; 331 doi: https://doi.org/10.1136/bmj.38629.587639.7C (Published 10 November 2005) Cite this as: BMJ 2005;331:1113All rapid responses
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Editor:
Our response to Erwich and colleagues is available on
http://bmj.bmjjournals.com/cgi/content/full/331/7527/1270
Wu and Spencer question the ability of customised charts to define
growth restriction in our study of stillbirths. In fact we used customised
birthweight percentiles (www.gestation.net/centiles) to calculate which
baby was growth restricted. In the majority of cases where a baby is small
for gestational age at birth, either alive or dead, the fact that it was
small was not recognised as such antenatally. If there was no suspicion,
it is likely that there were no ‘growth scans’, as in most units these are
not done routinely. However if they were done, and growth restriction was
recognised, then it is possible that delivery was expedited once the baby
was considered to be mature enough. Thus relying on serial growth scans to
explain growth restriction as a relevant condition for stillbirth is
likely to be of limited use.
Customised centiles are indeed based on coefficients from
heterogeneous populations, and adjust – within normal limits – for
physiological variables such as maternal height, weight, ethnic group and
parity as well as the sex of the baby. A low customised birth weight
percentile is a good indicator of pathological smallness [1]. A summary of
the evidence is available from www.perinatal.nhs.uk/growth/.
Wu and Spencer consider that the detail of primary and secondary
conditions in our paper makes ReCoDe too complicated. The analysis was
undertaken to test the coding in our new classification and to shed new
light on conditions associated with stillbirth. However we agree that
categories can be reported in a more simplified way. We have done this in
a recent regional report [2], where we summarised stillbirths in 9 major
ReCoDe groups: congenital anomaly; infection; fetal growth restriction;
umbilical cord; placenta; maternal conditions; intrapartum asphyxia;
miscellaneous; and unclassified/unknown.
1. Gardosi J. Customised Fetal Growth Standards: Rationale and
Clinical Application. Seminars in Perinatology 2004;28(1):33-40.
2. Gardosi J and Francis A. Perinatal Mortality and Social
Deprivation. In: Key Health Data for the West Midlands, University of
Birmingham, 2005 (Chapter 5),
www.perinatal.nhs.uk/pnm/Keyheathdatachapter5.pdf
Competing interests:
None declared
Competing interests: No competing interests
Editor -
The findings of Gardosi et al [1] relies heavily on their customised
antenatal growth charts as the ReCoDe system has reclassified most of the
unknown stillbirths as associated with fetal growth restriction.
It is questionable how these charts could account for the growth
velocity of fetuses from varying ethnicity, maternal weight and parity, as
population based studies would be required to obtain background data for
calculation. In addition, in order to determine that a fetus has not
achived its full growth potential, at least two serial assessments of
growth are needed. Furthermore, in Asian populations, where fetal size is
generally smaller than Caucasian counterparts, a reclassification of small
for dates babies would actually suggest that these babies are normally
small and are not associated with intrauterine growth restriction.
Consequently, this would increase the number of unexplained stillbirths.
Certain occult conditions, such as undiagnosed gestational diabetes could
also explain a significant number of stillbirths but is very difficult to
diagnose as glucose tolerance returns to normal so rapidly after placental
delivery.
In its attempt to be comprehensive, the ReCoDe system has become
overly complicated with confusing primary and secondary classifications.
In order for a classification system to be widely accepted, it should be
simple to understand with clearly defined categories that help reduce
interpersonal errors in classification. We look forward to a modified
version of ReCoDe in the future.
Pensee Wu,
Specialist Registrar in Obstetrics and Gynaecology,
St John's Hospital, Chelmsford, Essex, CM2 9BG
Chris P. Spencer,
Consultant Obstetrician and Gynaecologist,
St John's Hospital, Chelmsford, Essex, CM2 9BG
1. Gardosi J, Kady SM, McGeown P, Francis P, Tonks A. Classification
of stillbirth by relevant condition at death (ReCoDe): population based
cohort study. Br Med J 2005; 331: 1113-7.
Competing interests:
None declared
Competing interests: No competing interests
Editor - on behalf of my co-authors, I would like to thank your
correspondents for their interest in our paper.
Ms Robinson’s sad outcome of her first pregnancy reminds us that
often no cause of stillbirth is found, despite a postmortem. An overt
emphasis on ‘cause’, and the frequent inability to find one, is difficult
for bereaved parents who are seeking to understand what has happened. A
causal classification system often also fails to do justice to the
pathologist’s efforts, when an ‘unexplained’ category results despite a
high quality postmortem. We found that with ReCoDe, postmortem findings
could be fed very easily into the classification system. We therefore
agree with Dr Kirk on the need to emphasise the importance of postmortems,
and believe that they are more informative when coupled with a more
relevant classification system.
We were very careful in our paper not to present the ReCoDe
classification as a way to identify causes of death. Yet Dr Sebire's
letter still refers to ‘causes’ over half a dozen times. For example,
fetal growth restriction should not be seen as a cause of death, but a
relevant condition which is known to increase the risk of stillbirth 5
fold for fetuses below the 10th customised centile, and over 10 fold for
fetuses below the 3rd customised centile [1]. Of course not all growth
restricted fetuses die; but nor do most fetuses with conditions
representing any of the old perinatal mortality categories.
Dr Sebire also takes issue with the fact that no pathologist was
listed as co-author. This is explained by the BMJ’s strict rules on
authorship. The Perinatal Institute in fact enjoys a very active
collaboration with the regional perinatal pathology team led by Dr Phil
Cox. They have not only commented favourably on our new classification,
but already initiated studies on stillbirth and postmortem assessment of
fetal growth restriction. Theirs is a good indication that ReCoDe, which
deals with conditions, will stimulate further research into causes.
Clearly, identifying causes has been a formidable challenge over the
years. Using the conventional system, the proportion of stillbirths
classified as ‘unexplained’ has in fact been getting larger [2]. In
addition, overall stillbirth rates have been on the increase [3].
While everyone hopes that more of the underlying causes of
stillbirths will be determined one day, the main stakeholders require more
immediately to have a better insight into the relevant conditions. They
include the bereaved parents, who have to come to terms with the loss; the
clinicians who will want to focus on better methods to recognise fetal
growth problems as major risk factors of in-utero death; and those who are
tasked with planning health services, and who will need to allocate the
necessary resources for improved strategies for prevention.
Finally, Dr Sillender is correct to state that an RCT of antenatal
growth assessment would be welcome. For sufficient power to demontrate a
reduction in stillbirths, the size of such a trial would need to be
formidable, and attempts to obtain funding have not been successful in the
past. Perhaps this lack of interest was linked to the fact that most
stillbirths, to date, have been classified as ‘unexplained’…
1. Clausson B, Gardosi J, Francis A, Cnattingius S. Perinatal outcome
in SGA births defined by customised versus population-based birthweight
standards. Br J Obstet Gynaecol 2001;108:830-4.
2. Maternal and Child Health Consortium. CESDI 4th Annual Report:
Confidential Enquiry of Stillbirths and Deaths in Infancy, 1997
3. Confidential Enquiry into Maternal and Child Health. Stillbirth,
Neonatal
and Post-neonatal Mortality 2000–2003, England, Wales and Northern
Ireland. London:RCOG Press; 2005
Competing interests:
None declared
Competing interests: No competing interests
Editor- The paper of Gardosi et al1 is important to illustrate the
inadequacy of current classification systems and to stress the
preponderance of fetal growth restriction which, presumably, is not
diagnosed before the death occurs. Although definition of relevant
conditions at death may mute the debate about its cause, the distinction
between conditions, causes or mechanisms of death is still not clear in
this paper. Clear definitions or guidelines are not provided. Asphyxia is
a non-specific final common pathway of death not a cause nor a condition.
The authors intend to identify as many conditions as possible for a case.
This would be a powerful tool to stop debates about the cause where
conditions overlap or where several entities coexist, like fetal growth
restriction, pre-eclampsia, placental insufficiency and oligohydramnios.
However, the paper describes one condition as primary (cause?) and one as
secondary. Interestingly, in the primary group of fetal growth restriction
only 53/1129 (4.7%) have placental insufficiency as a secondary condition.
This unexpected low number illustrates the loss of insight into the
pathway to death.
The issue of using a hierarchy is motivated to “reflect clinical
relevance”. Although it seems preferable, a classification system for
perinatal mortality cannot be strictly hierarchical because of the
cognitive process of how doctors make a diagnosis2.
Any system restricted to stillbirths neglects the issue of iatrogenous
preterm delivery with neonatal death in cases with the same relevant
conditions. We welcome any suggestion for better classification of
perinatal mortality, since this is essential for both patient care and
prevention. The value of ReCoDe needs to be proven.
1. Gardosi J, Kady SM, McGeown P, Francis A, Tonks A. Classification
of stillbirth by relevant condition at death (ReCoDe): population based
cohort study. BMJ, doi:10.1136/bmj.38629.587639.7C (19 October 2005).
2. Elstein AS, Schwarz A. Clinical problem solving and diagnostic decision
making: selective review of the cognitive literature. BMJ 2002;
324(7339):729-732.
Competing interests:
No competing financial interests. Authors are developing a classification system themselves.
Competing interests: No competing interests
Gardosi et al's (1) recent report seems to lack focus on the main
issue. Definition of a new classification for stillbirth may be slightly
useful, but shouldn't be used retrospectively to justify the utility of
individually customised fetal growth charts.
The authors' method of using customised charts to improve detection
of pathologically small babies seems logical, and may prove to be a
significant advance in antenatal care. However, it may also expose women
& babies to iatrogenic harm if delivery is brought forward for no or
little benefit. I look forward to the authors producing a prospective
randomised controlled trial which would hopefully validate their charts.
Hopefully this trial will have a cute acronym too.
References
1. Gardosi J, Kady SM, McGeown P, Francis P, Tonks A. Classification
of stillbirth by relevant condition at death (ReCoDe): population based
cohort study. Br Med J 2005; ,331: 1113-7.
Competing interests:
None declared
Competing interests: No competing interests
The recent publication by Gardozi et al1 raises several issues
requiring further discussion. First, it is somewhat surprising that in a
study based on classification of stillbirth using previous pathological
classifications, no perinatal pathologist was involved in this study.
Second, and most importantly, many might take issue with the underlying
premise of this study. The authors state that any classification system
that results in a high proportion of cases being defined as unexplained is
not fulfilling its purpose. Surely the purpose of a classification system
is to the accurate so as to improve understanding of the underlying
disease processes. If it is true that the mechanism or cause leading to
death in an individual case cannot be determined with more than
speculative certainty, it is entirely correct to classify the case as
unexplained rather than to assign a potentially erroneous or artificial
cause of death in order to create the impression of knowledge. It is
unclear why the term ‘relevant condition at death’ was introduced, rather
than ‘cause of death’, which is used in all other settings of death
investigation, since the term ‘relevant’ presumably means ‘relevant to the
cause of death’ as opposed to any other possible relevance.
In particular, the main finding of this study is the reclassification
of numerous apparently previously unexplained cases, as fetal growth
restriction (FGR), such classification being on the basis of an estimated
customised weight for gestation below the 10th percentile. The clinical
relevance of growth restriction according to these criteria remain
controversial in ongoing pregnancies, and to therefore attribute the cause
of death to FGR in the absence of other specific findings may well be
incorrect. It is, of course, entirely possible that growth restriction is
an important contributory factor to stillbirth. However, the issue in
these cases is primarily to try to understand why a minority of fetuses
with mild growth restriction should die in-utero, whilst 10% of the entire
obstetric population will demonstrate a similar degree of FGR but will
result in livebirth.
It is agreed that current antenatal management only detects a small
proportion of intrauterine FGR, and that improved detection methods may be
associated with improved outcomes. Nevertheless, the suggestions of this
study have the potential to lead to both misleading interpretations of the
cause of death in future cases of stillbirth, and to a falsely inflated
sense of understanding of the underlying mechanisms leading to such
intrauterine death in the absence of an apparent pathophysiological basis.
Although it is entirely appropriate to highlight that severe FGR can lead
to intrauterine death, to suggest that the mere presence of biometric
markers suggesting a mild degree of growth restriction similar to that of
a large proportion of the population of living fetuses ‘causes’ death,
does not in anyway improve our understanding or certainty of underlying
disease processes in these cases and is inappropriate for introduction
into clinical practice on the basis of currently available evidence.
Yours Sincerely
Dr NJ Sebire
Consultant in Paediatric Pathology
Great Ormond Street Hospital,
Great Ormond Street,
London
1. Gardosi J, Kady SM, McGeown P, Francis P, Tonks A. Classification
of stillbirth by relevant condition at death (ReCoDe): population based
cohort study. Br Med J 2005; ,331: 1113-7.
Competing interests:
None declared
Competing interests: No competing interests
Gardosi et al congratulate themselves that under the ReCoDe
classification "only 15.2% of stillbirths remained unexplained". But if
the most common "condition" was fetal growth restriction, and 43% fell
into this category, then at least 58% are still unexplained under this
system. To classify something falls well short of explaining its cause.
There are many different known causes for fetal growth restriction, and
doubtless many unknown or at least unidentifiable ones. Some of these may
not even contribute to a risk of stillbirth when present. The goal should
be a clear understanding of the UNDERLYING cause of every stillbirth. The
fetal postmortem examination, despite its lack of effect on classification
in this study, remains a vital part of this effort, and has repeatedly
been shown to have an important impact on counselling to parents about
recurrence risks.
Competing interests:
None declared
Competing interests: No competing interests
Interesting report. My first child was stillborn at 37 weeks. He
weighed 6lbs 2 oz. Despite a full post-mortem, no cause was found. I was
assured that subsequent pregnancies would be normal as "lightning never
strikes twice".
My second son was born this year, weighing 7lbs 15 oz. He seemed OK,
but had some blistering on his skin. We were devastated to learn that he
had a fatal genetic condition called Herlitz junctional epidermolysis
bullosa. He died aged 4 months. What angers me the most is that the skin
blistering was noticed at the post mortem but not investigated further;
all that was needed was a biopsy. I was mis-informed and my poor baby son
had to suffer unimaginable pain. I'm not the only one.
More needs to be done to investigate "unexplained" stillbirths.
Yours sincerely
A grieving mum.
Competing interests:
None declared
Competing interests: No competing interests
Classification and Growth Restriction in Stillbirths
We were very interested to read the paper on the Classification of
Stillbirth by
Gardosi et al (1) and agree that current UK classification systems require
reassessment.
The Confidential Enquiry into Maternal and Child Health (CEMACH) is
concerned that the decline in infant mortality rate has distracted
attention
from an apparent deterioration in the stillbirth rate. Confidential
enquiry data
(to be published) show a small but significant increase in the stillbirth
rate
over the last ten years from 5.37 per 1000 livebirths in 1994 to 5.69 in
2004,
a trend also suggested by Office of National Statistics data. Over 60% of
stillbirths reported to CEMACH are classified as ‘unexplained’. This is
unacceptable if it is therefore inferred that no relevant factors exist or
that
these deaths are inevitable.
We agree that many ‘unexplained’ stillbirths show evidence of growth
restriction. A CESDI study of antepartum term stillbirths showed a simple
reclassification reduced the proportion of ‘unexplained’ deaths from
approximately 77% to 31% (2). In Liverpool, a review of 177 stillbirths
found
that only 27% of deaths remained unexplained following full clinico-
pathological correlation which took into account growth restriction (3).
Clearly, growth restriction is not, in itself, a cause of death: although
its
presence implies impaired fetal nutrition probably from reduced utero-
placental blood flow in many cases. Although there is a shortage of
pathologists with appropriate expertise, autopsy remains helpful in
diagnosing growth restriction by providing evidence of nutritional
deprivation
not available to the obstetrician.
CEMACH believes that a national programme should be developed with
the
ultimate aim of reducing the stillbirth rate and is in a position to
assist in this
process. Whether ReCoDe is the optimal solution is as yet unclear, but
with
the current limitations in knowledge, a better and informative
classification
system would be a major step forward.
References
1 Gardosi J, Kady, SM, McGeown P, Francis A, Tonks A. Classification
of
stillbirth by relevant condition at death (ReCoDe): population based
cohort
study. BMJ 2005; 331: 1113 - 1117
2 Study of Antepartum Term Stillbirths. Confidential Enquiry into
Stillbirths
and Deaths in Infancy. 5th Annual Report. pp 41 – 50, 1998.
3 Weindling AM, Shukla R, Ashworth M, Kokai G, Fleming K. Perinatal
deaths in the UK: A better classification system needed? Archives of
Disease
in Childhood 2005; 90, supplement II, A64.
Competing interests:
None declared
Competing interests: No competing interests