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DOI: 10.1111/tog.

12554 2019;21:127–34
The Obstetrician & Gynaecologist
Review
http://onlinetog.org

Autopsy in the event of maternal death –


a UK perspective
Sebastian Lucas FRCP FRCPath

Emeritus Professor of Pathology, St Thomas’ Hospital, London SE1 7EH, UK


Correspondence: Sebastian Lucas. Email: sebastian.lucas@kcl.ac.uk

Accepted on 1 December 2018. Published online 18 March 2019.

Key content  To understand the variety of clinical pathologies that cause


• The UK has one of the lowest maternal mortality rates in the world maternal death.
and the highest autopsy rate of maternal deaths.  To better understand what takes place before, during and after a

• Autopsy data contribute to the national confidential enquiries into maternal autopsy and learn how obstetricians can assist
maternal deaths and help to identify remediable factors to reduce the investigation.
future mortality. Keywords: autopsy / pregnancy / maternal death / SADS
Learning objectives
 To understand the law and practices surrounding maternal
autopsies, which are mostly medico-legal.

Please cite this paper as: Lucas S. Autopsy in the event of maternal death – a UK perspective. The Obstetrician & Gynaecologist. 2019;21:127–34. https://doi.org/10.
1111/tog.12554

obstetricians and midwives that may help them to better deal


Introduction
with a maternal fatality under their care.
The UK has one of the lowest maternal mortality rates
(MMRs) among high-income countries and the highest
Why so many maternal autopsies?
autopsy rate after such deaths. A confidential enquiry
published in 2017,1 covering deaths in 2013–2015, found There are two non-contingent reasons as to why the UK
the MMR from direct and indirect maternal deaths to be investigates these deaths assiduously. First, there is the legal
8.76 per 100 000 maternities. Currently, there are an average requirement for a medical certificate of cause of death
of 60–70 such deaths per annum. Of these, 84% have an (MCCD) to be written and recorded centrally through the
autopsy. The autopsy report is scrutinised for the enquiry, as Registrars of Births and Deaths. This certificate is written by
well as clinical information. Two-thirds of coincidental the attending doctor if they are able to state the cause ‘to the
maternal deaths are autopsied. The glossary provides best of their knowledge and belief ’.2 If not possible, a coroner
definitions of the types of maternal death. (or procurator fiscal in Scotland) investigates the case,
The MBRRACE (Mothers and Babies: Reducing Risk usually by way of an autopsy, and writes the MCCD. This
through Audits and Confidential Enquiries across the UK)1 requirement is why, in the UK, one in six of all deaths
review process of notified maternal deaths starts with a (men, women and children) results in a medico-legal
review of the autopsy report by expert pathologists to (coronial) autopsy.3
confirm the declared cause of death, or otherwise suggest a Secondly, since 1952, UK obstetricians have regularly
more accurate pathology. Thereafter, clinical review reviewed all deaths to seek their causes and ways of reducing
panels evaluate the clinical care and consider remedial them, through confidential enquiries, published reports and
factors to reduce, if possible, the likelihood of deaths in recommendations. At the time of writing, the centre for these
the future. activities is MBRRACE-UK in Oxford. Because these
This review summarises the processes of the maternal enquiries have been so useful and have changed practice
autopsy in the UK, its relation to the law and what happens over the years, the belief has grown that most or all deaths in
after the autopsy. It also considers the more important and pregnancy and delivery should be investigated with autopsy;
interesting clinical pathologies involving pregnancy, delivery thus most maternal deaths are reported to a coroner. The
and the postpartum period. There are also suggestions for high maternal autopsy rate almost entirely comprises

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medico-legal autopsies, with few consented instances in the next day, since post-mortem decomposition and
which clinicians, although they know the cause of death, wish deterioration of the fine structure of internal organs is
to determine the clinical pathology with greater accuracy inevitable, no matter how well refrigerated the body was in a
than they could in life. A related factor is a belief among the mortuary. Certainly in cases of sepsis, autopsy should take
relatives of a dead mother that, since maternal deaths are place sooner rather than later so that samples from the body
genuinely uncommon, something must have gone wrong and can be cultured for bacterial infection with as little
that medical error may have played a role in the death; this contamination from the normal body/gut flora as possible.
reinforces the reporting of such cases to a coroner. Usually, maternal autopsies take place within the working
week following death.
The law in the UK Autopsies in the UK take place in both hospital mortuaries and
in local authority public mortuaries (free-standing buildings, not
The primary role of a coroner is to investigate known or associated with the National Health Service). The critical issues
suspected unnatural deaths. Under the current legislation for are whether the mortuary is sufficiently equipped to undertake
England and Wales,4 deaths within the coroner’s jurisdiction maternal autopsies (specifically, having microbiology culture
area are reported to them if it is suspected that: sample bottles available, as well as access to histopathology
1. the deceased died a violent or unnatural death laboratories for subsequent microscopic examination of the
2. the cause of death is unknown tissues) and whether the pathologist is sufficiently skilled to
3. the deceased died while in custody or otherwise in state perform the autopsy dissection and undertake any further
detention (including psychiatric hospitals). investigations such as histology. In addition, the quality of
In the realm of maternal deaths, the first criterion includes assistance from the mortuary’s anatomical pathology
the deaths of mothers in road traffic collisions, accidents, technologists can be critical – they help with dissection as well
homicide, suicide and drug overdoses. While suicide is now as reconstructing the body afterwards.
considered a direct maternal death, the others are As noted in the confidential enquiry reports, in previous
coincidental. The possibility of a medical, surgical or decades, the standard of maternal autopsies and their reports
pharmacological mishap is another aspect of this criterion varied from ‘excellent’ to ‘appalling’.5 The latter lack of
that involves the coroner (i.e. was this an unnatural and quality followed after autopsies and reports were carried out
preventable death?). by forensic pathologists who, generally, have no interest in
The second criterion is the reason why most maternal maternal death, but were presented with the cases by
autopsies are authorised by a coroner. If the death occurred coroners. This message has passed to the UK pathology
in hospital, the doctors involved often do not know what community, such that many pathologists (including forensic
happened, particularly if the death happened around the time pathologists) now decline to perform maternal autopsies
of delivery; if it occurred in the community (e.g. at home), because of having insufficient experience. It should be noted
then the coroner must investigate because its medical cause that, because of their rarity, many pathologists will never
will rarely be evident (or it may be traumatic, coming under encounter a case during their career. Learning on the job in
criterion 1). The very occasional deaths following home births their first, often difficult, case is not good practice.
will always be investigated, as will deaths following abortion. Consequently, coroners – and their officers who are active in
Maternal deaths not resulting in an autopsy, in which a treating organising coronial autopsies – increasingly seek out experienced
doctor can write an accurate MCCD, occur particularly in cases of pathologists to perform maternal autopsies. Such experts may
known fatal cancers – hence the lower autopsy rate for these work outside the geographical area of the coroner’s jurisdiction.
coincidental deaths. In the MBRRACE system, expert Coroners realise that in difficult and contentious cases, it is worth
pathologists also review these cases to provide their opinion on a delay and additional expense to have the case transferred to a
whether or not the death should have had an autopsy distant mortuary because they can then be more confident in the
investigation. In most cases, the answer is ‘not necessary’. results of an autopsy that is carried out by an experienced
pathologist. Eventually, we should arrive at an arrangement
whereby a small number of regional mortuaries, staffed by at least
Autopsy: when, where and by whom?
two pathologists with an interest in maternal death, perform all
An advantage of the UK coronial system is that when a maternal autopsies. See Suggestion 1.
coroner determines, from the information presented by
doctors, relatives and other informed parties, that an autopsy
is required to determine the cause of death, then it is virtually
The autopsy process and timing of results
impossible to prevent the autopsy from taking place through In most cases, the actual autopsy dissection involves a
a legal challenge. Therefore, autopsies can follow as soon complete autopsy: the head and brain might be omitted if the
as this decision is made. Ideally, autopsies should take place cause of death is obviously below the neck, but otherwise all

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internal organs are removed. The dissection is generally questions of the witnesses and thereby assist the coroner in
straightforward; in cases of peripartum haemorrhage, coming to a conclusion. The outcome will be the cause of
complete removal of the entire genital tract is a non- death and often a narrative commentary on how the death
standard procedure. In most instances, organ samples will be came about. It is important to realise that the coroner’s
retained for histology, and sometimes a whole organ is fixed inquiry does not apportion any blame for a death – such
in formalin before it is cut and blocked for histology. Blood, considerations take place elsewhere – but any subsequent civil
urine, cerebrospinal fluid (CSF) and any septic focus may be or criminal litigation will usually take a transcript of the
sampled for microbiology culture. Blood, urine and vitreous inquest as evidence.
samples may be needed for toxicological analysis: these are In a maternal autopsy, the pathologist will usually meet the
mandatory in cases of suspected drug overdose and frequent family when there is an inquest. Ideally, by the end of the
in cases of sudden and unexpected maternal death in inquiry, all of the issues will have been explored, but further
the community. questions can be addressed. This in turn raises the question:
It is always helpful to examine the placenta in cases of should the pathologist communicate with the family whenever
maternal death, but many deaths occur after a normal or a maternal autopsy occurs? Arguably, if the family do not
otherwise unremarkable delivery and placentas are routinely understand what has happened, despite having the autopsy
discarded. If there has been a hysterectomy following report, they should be given the opportunity for further
peripartum haemorrhage, it is essential to examine the clarification through talking to the pathologist.
uterus specimen. See Suggestion 2. In all cases of maternal death in a UK hospital, there
Depending on the cause of death, the time taken for the should be – at least – an internal inquiry into the death.
final autopsy result varies: if no histology or toxicological Autopsy reports contribute significantly to these
studies are needed, i.e. if the diagnosis is made on naked-eye considerations. If there is unusual pathology, or the death
appearances only, then a week is reasonable. However, most demonstrates an important lesson for future practice, a
cases involve histological analysis, and if the clinical hospital grand round or departmental clinico-pathological
pathology is complex and consultation with colleagues is conference (attended by the pathologist) is most instructive.
required, then it may take up to 3 months for the final report If the autopsy report and its conclusions seem incorrect
and diagnosis to emerge. For this reason, those undertaking according to the clinical story known to the attending
serious untoward incident inquiries, which regularly follow doctors, then the report should be queried as soon as
hospital-based maternal deaths, must be made aware of these possible. Most pathologists have little experience in this area
unavoidable delays and be careful about reaching conclusions and can produce wrong diagnoses. See Suggestion 4.
about past and future practice before the autopsy diagnosis is
declared. See Suggestion 3.
The clinical pathology of maternal death
The reasons why mothers die depend almost entirely on
Inquests and after
where they live and their access to medical and obstetric care.
Formal inquests are inquiries held in the coroner’s court. In low-income countries, where the MMR may be 10–100 times
They feature witnesses and are open to the public. In England that seen in the UK, the major causes of death are: haemorrhage,
and Wales, inquests follow 44% of all deaths that have an sepsis, unsafe abortion, complications of delivery and
autopsy.3 In the remaining autopsy cases, the coroner takes hypertensive diseases of pregnancy. However, these causes
the pathologists’ cause of death and completes the MCCD so of death are estimated based on clinical opinion and
that the relatives can present this to the Registrar of Birth and retrospective verbal autopsy:6 autopsy morbid anatomical
Deaths. There are no fixed rules on whether a particular information is rarely available. The picture in the UK is
maternal death should have an inquest, only that all evidently completely different; for example, out of more than 700 000
unnatural deaths do result in an inquest. An inquest is likely maternities, there is now fewer than one death a year from
if the cause of death is particularly complicated, if there are eclampsia,1 and unsafe (criminal) abortion is extremely rare
concerns over the mother’s care, or if the relatives are making thanks to 1960s legislation. In contrast with poorer countries,
complaints against a hospital or particular doctors. These where most maternal deaths are of direct obstetric cause,
usually take place months after the death, but in complex indirect deaths predominate in the UK (56% versus 44%).
cases can sometimes (regrettably) take place years later. This indication of the overall high quality of obstetric care is
Outside expert witnesses may be called to give evidence, both further boosted if venous thromboembolism is removed
in written reports and at the inquest. from the direct category; clinico-pathologically, it should be
Hospitals are always represented by lawyers; often, included in the indirect group.
individual healthcare staff have attending lawyers, and the Since 2014, reviews of the pathology of maternal death,
family may also be so represented. The role of lawyers is to ask made by expert pathologists, have been presented in annual

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MBRRACE reports, either alongside clinical category reviews better medical care during the last trimester and delivery.
or in separate sections of the report. Here, I focus on specific Often, these conditions are only diagnosed at autopsy (see
clinical pathologies and discuss how the autopsy contributes Autopsy Case 1). The mysterious peripartum cardiomyopathy
to their diagnosis and knowledge of their pathogenesis. (PPCM) continues to cause progressive heart failure in the
Table 1 indicates the causes of sudden death around the third trimester and after delivery.
time of term delivery; it includes the most difficult challenges A major change in the UK (and this probably applies to other
that pathologists face in determining the cause of death. The high-income countries, although it has not yet been formally
scenarios listed derive from personal experience as well as documented) is the increased incidence of diagnosed ‘sudden
the literature. arrhythmic cardiac death syndrome with a morphologically
normal heart’ (SADS/MNH). This occurs in someone who
Cardiac deaths suffers acute cardiac arrhythmia and dies, usually in the
In the UK, deaths from cardiovascular disease are the single community. It is a diagnosis of exclusion, made when all other
most common group of disorders causing maternal death.1 possible causes of death (including toxicological and
Ischaemic coronary heart disease is associated with increasing anaphylactic) are excluded. Many cases are suspected to
maternal age; valvular heart disease is a particular issue in result from inherited abnormalities of the heart rhythm
people who had rheumatic fever in their youth; structural (channelopathies), although this has been confirmed in only
cardiomyopathies, splenic artery aneurysm rupture and a few cases.7 SADS/MNH has always occurred, but the reasons it
dissection of the aorta continue to present as rapid collapse is now reported more frequently are that pathologists had been
and death; congenital heart disease is more frequently seen in reluctant to make the diagnosis and/or there had been no
pregnant women, but, thanks to improved surgical pathological examination, and/or any pathological
management, the fatality rate appears to be declining with examination had not been robust enough to exclude other
possible diagnoses. See Autopsy Case 2.
It is important that apparent cardiac deaths in young,
Table 1. Causes of sudden maternal death around the time of delivery pregnant women are properly examined, because there is
Organs and inevitable discrepancy between the imaging and
systems Clinical pathologies physiological information in life and what is actually
found at autopsy.
Lung Thromboembolism
Amniotic fluid embolism*
Venous thromboembolism to the lungs
Fat embolism
Air embolism** Pregnancy enhances the risk of venous thromboembolism
Acute asthma (VTE) in women by a factor of about 10; hence, pulmonary
Sickle cell crisis embolism is a major cause of maternal death. It occurs from
Pulmonary hypertension
the second trimester through to several weeks after delivery.
Pneumothorax
Polyvinyl alcohol (PVA) particle embolisation Obesity and caesarean section are well-known risk factors,
following uterine artery embolisation*** and the most common site of embolus origin is the left iliac
Heart Structural disease vein. Antithrombotic prophylaxis reduces the risk of
Diastolic dysfunction syndrome and post-delivery embolism and death but does not eliminate the risk.
fluid overload When a death does occur and the diagnosis is made – as it
Sudden arrhythmic cardiac death syndrome with a
morphologically normal heart usually is – at autopsy, questions may be asked as to whether
Pre-eclampsia-related cardiac arrest prophylaxis could have prevented the death. Here, the critical
Brain Acute haemorrhage (eclampsia or other issues can be addressed at autopsy: when did the deep vein
pathogenesis) thrombosis start (months, weeks, days or immediately before
Venous sinus thrombosis the fatal embolism)? Was the fatal embolism the first and last
Epileptic seizure
occasion, or were there previous episodes? Histological
Systemic Severe sepsis examination of the likely sites of the deep vein thrombosis
Thrombotic thrombocytopenic purpura (TTP)
Acute anaphylaxis and of the thrombus in the lung arteries can inform on
Drug toxicity (e.g. cocaine) chronology. Histology of the lung tissue may also reveal
Anaesthesia Spinal – high spinal block previous subclinical emboli. If no histology is done, then it is
General – respiratory failure usually impossible to narrow down the chronology of VTE.8
Haemorrhage Genital tract haemorrhage
Artery rupture Anaesthetic deaths
*See Autopsy case 2; **See Autopsy case 3; ***See Autopsy case 4 These deaths are complications of both spinal and
general anaesthesia.

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Spinal anaesthesia artefact and, in this instance, does not indicate AFES
Infection of the spinal cord and meninges is a rare (see Autopsy Case 2). In the former scenario, my view is
complication. Postdural puncture headache is common that a negative autopsy does not negate a positive clinical history
and, with severe CSF leakage, can lead to subdural when all other clinicopathological possibilities are excluded.
haemorrhage and even death. Obviously an autopsy is
critical for evaluating these scenarios. Sepsis
The uncommon cardiopulmonary complications of high- Reviews of sepsis in pregnancy and delivery have tended to
spinal block from spinal anaesthesia are more difficult to group all the scenarios into a single category, with emphasis on
diagnose.9 These will be diagnoses of exclusion (i.e. there is infection acquired during delivery – the ‘Semmelweis
no other pathologically evident cause of death) made after a syndrome’. However, different patterns of severe and fatal
critical review of the medical records done in conjunction infection have completely different pathogeneses and,
with anaesthetist colleagues. implicitly, different approaches to reduce their occurrence.11
There are six separate categories to consider, and the autopsy is
General anaesthesia critical for determining the appropriate one.
Deaths caused by general anaesthesia are very difficult for
pathologists to determine because there is no residual morbid 1. Sepsis following unsafe termination of pregnancy: non-
anatomical evidence, and measuring levels of anaesthetic aseptic techniques can introduce numerous virulent
agents in body fluids is unhelpful. Cardiac arrhythmia from infections. This scenario is rare in high-income countries
anaesthetic drugs is not diagnosable from autopsy. The most but is a major cause of maternal death in poor countries,
common scenario of post-delivery death following general particularly in those where safe termination is illegal.
anaesthesia is respiratory failure after removal of an 2. Ascending genital tract infection associated with miscarriage,
endotracheal tube because of premature removal and/or usually in the second trimester: the most common infection
blockage of the tube. However, an autopsy cannot provide agent is Escherichia coli; however, it is not usually possible to
positive proof. determine from an autopsy whether it is the cause of the
On a practical note, while levels of anaesthetic drugs in the miscarriage and rupture of membranes, or infects the tract
blood are not informative, it is always worth measuring following rupture of membranes. The bacteria come from the
blood mast cell tryptase levels after anaesthetic death. High mother’s perineum, pass up into the uterus and initiate
mast cell tryptase levels indicate an acute anaphylaxis endometritis. Then, in susceptible mothers, systemic sepsis
reaction, often to drugs. syndrome occurs. Pathologically, it is striking that nearly all
deaths in this scenario occur rapidly once the mother feels ill
Amniotic fluid embolism syndrome and show DIC in capillaries of the kidney. It is likely that the
Amniotic fluid embolism (AFE) syndrome (AFES) occurs as triggering of DIC, which probably has a genetic predisposition,
a clinically diagnosed event in about 2 per 100 000 deliveries is the critical factor in determining the outcome.
in the UK.10 In about 20% of cases, death results from 3. Genital tract infection and subsequent systemic sepsis:
cardiopulmonary collapse followed by a coagulopathy with occurring within hours or days of delivery, whether the
haemorrhage from the uterus and other sites. delivery was vaginal (assisted or not), by caesarean section,
The clinical story is critical for diagnosing this syndrome, or a medical or surgical termination at any gestation.
in conjunction with autopsy pathology. Amniotic and fetal Semmelweis syndrome, in which midwives and doctors
skin squamous cells should be found in the lungs, along with introduce bacteria such as Group A Streptococcus pyogenes
amniotic mucin forming a plug of the distal pulmonary (GAS) into the mother’s genital tract, is now very
arterioles and capillaries. If the patient has survived long uncommon in high-income countries. However, mothers
enough, coagulopathy with local haemorrhage is present, are still able to spread nasal bacteria from their own nose,
particularly from the genital tract, but there is no or their children’s noses, to their lower genital tract.
disseminated intravascular coagulation (DIC) in the kidney Perinatally acquired herpes simplex infection can
glomeruli. The squames and mucin may also be visible in the disseminate to cause devastating abdominal and systemic
uterine and cervical veins. infection, exacerbated by the lowered cell mediated
Diagnostic problems with autopsy are two-fold: there are immunity typical of late trimester pregnancy.
cases with a typical clinical story, with or without a 4. Systemic sepsis: typically arising from GAS infection,
coagulopathy, where no AFE material is seen in the lungs; usually a fulminant infection in mothers who are not in
and those with an atypical or ambiguous clinical story that labour and whose membranes have not ruptured. This
still have AFE material in the lungs. In the latter scenario, scenario is probably unrelated to pregnancy per se; rather,
note that vigorous cardiopulmonary resuscitation can readily it may reflect the community load of GAS and the host
force AFE material into the pulmonary circulation as an woman’s immune status.

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5. Severe infection related to pregnancy and delivery, but


outside the genital tract: include infected spinal Special cases
anaesthesia sites, infected caesarean section suture lines Mothers who are Jehovah’s Witnesses and have sickle cell
and perforation of a viscus during obstetric surgery. anaemia may present particular problems if and when blood
6. Other infections such as HIV, bacterial meningitis, loss occurs, since they do not accept blood products. In such
tuberculosis, pneumonia and influenza: during the cases, deaths will usually have a coronial autopsy in which the
recent H1N1 influenza pandemic, pregnancy was the relevant morbidities in addition to anaemia must be carefully
most significant risk factor for severe respiratory illness evaluated so that the refusal to accept blood products can be
and death.12 It is notable that in the UK, where virtually all placed in context regarding the cause of death.
mothers are tested for HIV and can be treated with anti- Other special cases include the very uncommon deaths
retrovirals, HIV/AIDS is rarely a contributory cause of around the time of delivery where, despite autopsy
maternal death. investigations and available clinical physiology data, a
definite cause of death is not found (i.e. the pathologies
A final note on sepsis in pregnancy: pregnant women with
listed in Table 1, with the exception of SADS/MNH, are
sickle cell diseases (both HbSS and HbSC genotypes) are
excluded). Families, coroners, hospitals and litigation lawyers
particularly liable to severe infection (commonly
do not like this and neither do pathologists. Whether such
Streptococcus pneumoniae) because their disease renders
deaths, which occur in full view of many experienced clinical
them relatively immunocompromised.
staff, are labelled as ‘unascertained’ or ‘SADS/MNH’ varies.
The quality of the autopsy is critical to making the distinction
Pre-eclamptic toxaemia/eclampsia and detailed clinical and anaesthetic input is essential (see
Death from severe hypertensive disease in pregnancy can Autopsy Case 3).
occur in the second and third trimesters and also after
delivery (postnatal eclampsia). If there was any doubt before
the death, autopsy pathology is critical for identifying these Conclusion
deaths. Most fatal cases of eclampsia involve intracerebral Unlike many countries, the UK has accurate information about
haemorrhage (through arterial hypertension); in HELLP the causes of death through regular peer review and the high
(haemolysis, elevated liver enzymes and low platelet count) autopsy rate following maternal deaths. A key factor is the
syndrome, liver failure through periportal necrosis and availability of pathological expertise in this area. Results
haemorrhage is important. Pathologically, it is likely that monitor the changes in the epidemiology of maternal mortality
pre-eclamptic toxaemia (PET) can also cause death via and enable realistic recommendations for reducing mortality.
cardiac arrest, as a cerebral–vagal–cardiac arrhythmia, Inevitably, a very small number of deaths that occur during
although this scenario is not yet generally accepted. delivery and sudden deaths in the community will never be
Positive autopsy histology evidence for PET/eclampsia resolved through autopsy pathology, but review systems
includes: abnormal spiral arteries (atherosis) in the uterine should be in place to ensure that these are kept to a minimum.
decidua, abnormal placental histology and glomerular
endotheliosis in the kidney; and liver periportal
haemorrhage in HELLP. Glossary
 Maternal death: the universal definition of maternal death
Peripartum haemorrhage is death occurring in women from conception through to
The major causes of peripartum haemorrhage include atonic delivery and up to 6 weeks postpartum. In the UK, all
uterus, retained placenta, traumatic tears to the genital tract, deaths up to 1 year postpartum are notified, though not all
rupture of the uterus, placenta praevia and accreta and AFES. will be centrally reviewed. The deaths are categorised as
The autopsy is essential to evaluate these possible direct, indirect or coincidental.
pathologies, and consideration is given as to whether the  Direct maternal death: caused by a disease process specific
whole genital tract should be removed en bloc, fixed and to pregnancy and delivery; e.g. pregnancy-related
examined in detail. Histology is useful in all of these possible infection, hypertensive diseases of pregnancy, peripartum
scenarios, except that an atonic uterus generally has no haemorrhage, death from anaesthesia, amniotic fluid
specific features that are visible under the microscope. Where embolism, deaths in early pregnancy, peripartum
there has been a hysterectomy, it is vital to examine the cardiomyopathy (PPCM), gestational trophoblastic
removed organ alongside the rest of the body. If still diseases and postpartum psychotic suicide. For historical
available, the placenta must also be examined. See Suggestion reasons, deaths resulting from VTE are also counted as
2 and Autopsy Case 4. direct causes. However, since these also occur in non-

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pregnant people, it would be better to classify them At autopsy, the expected pathology was a massive
as indirect. pulmonary thromboembolism, which is associated with risk
 Indirect maternal death: caused by diseases that also occur in factors of pregnancy, caesarean section and obesity. However,
women who are not pregnant, but which are exacerbated by there was no pulmonary thromboembolism and the iliac
pregnancy, critically affect the pregnancy, or where the veins were clear. Instead, acute staphylococcal infective
treatment is complicated by pregnancy; e.g. cardiac diseases endocarditis was found, affecting the aortic valve and the
other than PPCM; indirect sepsis (e.g. influenza); neurological anterior cusp of the mitral valve. One aortic valve cusp had
diseases other than VTE; immunological disorders; perforated, causing acute heart failure. Underlying the
gastrointestinal, renal, endocrine and pulmonary diseases; endocarditis, the aortic valve was bicuspid. Congenital
liver disease (other than acute fatty liver of pregnancy and bicuspid aortic valves have a 10–30% lifetime risk of
HELLP syndrome); primary pulmonary hypertension; and developing endocarditis. The causative organism is most
diseases involving bone marrow or solid organ commonly Staphylococcus aureus.
transplantation. None of the standard non-trophoblastic
cancers are really affected by pregnancy, apart from the Case 2
undoubted fact that treatment options for the mother are A 27-year-old primip reached 39 weeks of gestation with no
compromised by the presence of the fetus in utero. antenatal medical problems. She had not started labour and
 Coincidental maternal death: death resulting from diseases her membranes were not ruptured. She was witnessed to
unrelated to pregnancy; e.g. accidents, homicide, drug collapse, stop breathing and become pulseless. A bystander
overdose and alcoholism. commenced CPR and this was continued by members of the
 HELLP: hepatic elevated enzymes and low platelets; a ambulance staff. They found no pulse, and the ECG trace
variant of PET/eclampsia. showed the woman was in ventricular fibrillation. A
defibrillator was used to deliver one shock, but this did not
restore the heart rhythm and she was asystolic thereafter. The
Suggestions for obstetricians who deal woman was declared dead after more than 1 hour of intensive
with a maternal death resuscitation and a perimortem caesarean section.
Lung histology taken at autopsy found that the only
1. When communicating with the coroner (or fiscal) about a
morphological abnormality was massive quantities of
mother’s death that requires investigation, discuss whether
amniotic fluid material in the pulmonary arteries.
a specialist pathologist can perform the autopsy, even if it
In this scenario, there was clear evidence of acute cardiac
means having the body transferred out of district.
arrhythmia; absence of labour, rupture of membranes or
2. In cases of maternal death, it is helpful to be able to present
interference with the uterus prior to her collapse; and no
the placenta to the pathologist. If there are problems during
evident prodromal symptoms indicative of AFES. Therefore,
delivery, ensure that the placenta is retained and fixed in
it was decided that the death was caused not by AFES but
formalin. If there has been a hysterectomy before death, it is
sudden cardiac death. Previous reports have documented the
essential that the pathologist performing the autopsy can
presence of AFE material forced into the maternal circulation
examine the removed organ.
by resuscitation efforts.
3. When a post-death inquiry is initiated, be aware that the
final cause of death may not be available for weeks to
Case 3
months afterwards. Do not make final conclusions until
A woman had a caesarean section under spinal anaesthesia at
this information is presented.
38 weeks of gestation. While the uterus was being closed, she
4. If an autopsy report appears wrong according to your view
became breathless, with a respiratory arrest, followed by
of the clinical problems and their management, or omits
cardiac arrest. She survived for some days with hypoxic-
consideration of important factors, approach the coroner
ischaemic encephalopathy before eventually dying. Apart
and request a review.
from brain damage, the autopsy was entirely negative.
The diagnoses listed in Table 1 were considered in a
multidisciplinary consultation, and all but air embolism and
Autopsy cases: how the autopsy can alter
fluid overload syndrome were discarded. Further
the apparent diagnosis
examination of fluid balance and drug charts indicated no
Case 1 fluid overload. Although no air embolism was seen at
A 35-year-old woman had a caesarean section at 36 weeks of autopsy – and would not be expected, given that any air
gestation for slow fetal growth. Medically, she appeared well. would have been absorbed during the 3-day delay between
Once discharged, she collapsed at home on the third day post- collapse and death – the final diagnosis, on balance of
delivery and could not be resuscitated by the ambulance crew. probabilities, was air embolism.

ª 2019 Royal College of Obstetricians and Gynaecologists 133


Maternal autopsy in the UK

Case 4 uk/downloads/files/mbrrace-uk/reports/MBRRACE-UK%20Maternal%20Re
port%202017%20-%20Web.pdf].
A 40-year-old woman with two previous caesarean section 2 National Archives. Birth and Deaths Registration Act, 1953. London: UK
deliveries had a third such delivery at 40 weeks of gestation. As Government; 1953 [http://www.legislation.gov.uk/ukpga/Eliz2/1-2/20].
placenta accreta had already been diagnosed, she had uterine 3 UK Ministry of Justice. Coroners statistics 2017. London: UK
Government; 2017 [https://www.gov.uk/government/statistics/coroners-
artery embolisation (UAE) with polyvinyl alcohol (PVA) statistics-2017].
particles at delivery to reduce the placental blood flow. Two 4 National Archives. Coroners and Justice Act, 2009. London: UK Government;
weeks later there was still blood flow through the placenta, so 2009 [https://www.legislation.gov.uk/ukpga/2009/25/contents].
5 Millward-Sadler H. Chapter 15: Pathology. In: Lewis G, Clutton-Brock T,
UAE was repeated. Soon after, she deteriorated with Cooper G, Drife J, Edwards G, Harper A, et al. Saving Mothers’ Lives:
hypotension. Internal bleeding was suspected but a reviewing maternal deaths to make motherhood safer – 2003–2005.
laparotomy found none, and a subtotal hysterectomy was London: Confidential Enquiry into Maternal and Child Health; 2007 [http://
www.publichealth.hscni.net/sites/default/files/Saving%20Mothers%27%
performed. She died shortly afterwards. 20Lives%202003-05%20.pdf].
At autopsy, all of the pulmonary arterioles were found 6 World Health Organization (WHO). Maternal mortality. Geneva: WHO;
blocked by chains of PVA particles, with proximal thrombosis 2018 [http://www.who.int/news-room/fact-sheets/detail/maternal-morta
lity].
causing acute cor pulmonale. The uteroplacental resection 7 Lucas SB, Chapter 3.5.4: SADS/MNH. In: Knight M, Nair M, Tuffnell D,
contained similar particles, with partial infarction of the Kenyon S, Shakespeare J, Brocklehurst P, et al (Eds.). Saving Lives, Improving
placenta (which was percreta rather than accreta). Mothers’ Care. Surveillance of maternal deaths in the UK 2012–14 and
lessons learned to inform maternity care from the UK and Ireland
Somehow, the UAE procedure pushed the PVA particles Confidential Enquiries into Maternal Deaths and Morbidity 2009–14.
through the uterus circulation into the iliac veins and then into Oxford: MBRRACE; 2016 [https://www.npeu.ox.ac.uk/downloads/files/mb
the lung circulation, to cause pulmonary artery obstruction. rrace-uk/reports/MBRRACE-UK%20Maternal%20Report%202016%20-%
20website.pdf].
This has not been described before in pregnancy. Histology of 8 Lucas SB. Appendix A1: Venous thromboembolism – pathological aspects.
the uterus found no obvious arteriovenous fistula channel. In: Knight M, Tuffnell D, Kenyon S, Shakespeare J, Gray R, Kurinczuk JJ
(Eds.). Saving Lives, Improving Mothers’ Care. Surveillance of maternal
deaths in the UK 2011–13 and lessons learned to inform maternity care
Disclosure of interests from the UK and Ireland Confidential Enquiries into Maternal Deaths and
SL is the lead Pathology Assessor for MBRRACE-UK and Morbidity 2009–13. Oxford: MBRRACE; 2015 [https://www.npeu.ox.ac.
contributes to their annual reports. uk/downloads/files/mbrrace-uk/reports/MBRRACE-UK%20Maternal%20Re
port%202015.pdf].
9 Hawkins JL, Chang J, Palmer SK, Gibbs CP, Callaghan WM. Anesthesia-
Acknowledgements related mortality in the United States: 1979–2012. Obstet Gynecol
The MBRRACE-UK epidemiologist, Kathryn Bunch, 2011;117:69–74.
10 Knight M, Tuffnell D, Brocklehurst P, Spark P, Kurinczuk JJ, UK Obstetric
provided the autopsy rate data. Professor Marian Knight Surveillance System. Incidence and risk factors for amniotic fluid embolism.
(MBRRACE-UK) provided helpful suggestions. Obstet Gynecol 2010;115:910–7.
11 Lucas SB. Annex 7.1. Maternal sepsis, a possible future approach to case
definitions. In: Lewis G, Cantwell R, Clutton-Brock T, Cooper G, Dawson A,
References Drife J, et al. Saving Mothers’ Lives: reviewing maternal deaths to make
motherhood safer – 2006–08. Centre for Maternal and Child Enquiries,
1 Knight M, Tuffnell D, Shakespeare J, Kenyon S, Kurinczuk J (Eds) on behalf BJOG, March 2011, vol 118 (Suppl 1): pp97–101.
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inform maternity care from the UK and Ireland Confidential Enquiries into systematic autopsy examination of patients who died with A/H1N1
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134 ª 2019 Royal College of Obstetricians and Gynaecologists

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