Brain death in early pregnancy: A legal and ethical challenge coming to your intensive care unit?

Abstract

Increasingly, reports are emerging of maternal physiological support after brain death in pregnant women declared brain dead long before the gestational age of foetal viability. While these ‘miracle babies’ often receive significant media attention – such as the recent case of Catarina Sequeira – it is difficult to estimate the probability of a live birth in such circumstances given a clear publication bias in favour of reporting good outcomes. In a number of highly publicised cases, continuation of maternal physiological support after brain death has been attempted against the express wishes of the patient's family in jurisdictions where a foetal right to life is given weight in law. The legal issues around discontinuation of maternal physiological support after brain death have not yet been assessed by a UK court. The scenario is easily envisioned, however, where conflict emerges as to the appropriateness of such support. While there is no statutory definition of death in the UK, the courts have accepted brain-dead patients as legally dead upon completion of brainstem testing. However, as UK law grants few explicit legal rights to a foetus, it is unclear as to how conflicts are to be resolved. This article is not intended as a systematic review of the medical or legal academic literature, nor as a review of the clinical management of the pregnant brain-dead patient; rather, it aims to summarise the evidence base for maternal physiological support after brain death and the relevant case law. Using a recent case as an example, this article will outline the legal approach to death in the UK, contrast the status in law of a brain-dead mother and her foetus, and advance an argument of the circumstances in which maternal physiological support after brain death may be ethically justifiable. The authors hope this will assist the UK intensivist in the complex decision-making such cases demand.

Introduction

Increasingly, reports are emerging of maternal physiological support after brain death (MPS-BD) in pregnant women declared brain dead long before the gestational age of foetal viability. While these ‘miracle babies’ often receive significant media attention – such as the recent case of Catarina Sequeira – it is difficult to estimate the probability of a live birth in such circumstances given a clear publication bias in favour of reporting good outcomes. In a number of highly publicised cases, continuation of MPS-BD has been attempted against the express wishes of the patient's family in jurisdictions where a foetal right to life is given weight in law.

The legal issues around discontinuation of MPS-BD have not yet been assessed by a UK court. The scenario is easily envisioned, however, where conflict emerges as to the appropriateness of such support. While there is no statutory definition of death in the UK, the courts have accepted brain-dead patients as legally dead upon completion of brainstem testing. However, as UK law grants few explicit legal rights to a foetus, it is unclear as to how conflicts are to be resolved.

This article is not intended as a systematic review of the medical or legal academic literature, nor as a review of the clinical management of the pregnant brain-dead patient; rather, it aims to summarise the evidence base for MPS-BD and the relevant case law. Using a recent case as an example, this article will outline the legal approach to death in the UK, contrast the status in law of a brain-dead mother and her foetus, and advance an argument of the circumstances in which MPS-BD may be ethically justifiable. The authors hope this will assist the UK intensivist in the complex decision-making such cases demand.

The case of Catarina Sequeira

Catarina Sequeira, a 26-year-old former international athlete, was admitted to the intensive care unit at the São João Hospital in Porto, Portugal in December 2018 following an asthma attack. She was declared brain-dead several days later. At the time of admission, Sequeira was 19 weeks' pregnant. The hospital's ethics committee decided to continue artificial organ support with the goal of elective caesarean section delivery at 32 weeks' gestation. This was brought forward following worsening maternal respiratory compromise, and the foetus was delivered by caesarean section at 31 + 6 weeks, weighing 1.7 kg. A day later, Catarina Sequeira was disconnected from the ventilator and circulatory death occurred. ¹

The hospital ethics committee stated that the evidence to support the decision to continue artificial ventilation was twofold: the strong agreement of her family and the father that this would be her wish, and that Sequeira had not opted out of Portugal's presumed consent law for organ donation. They argued this suggested she would not object to ongoing treatment in a brain-dead state in order to preserve life. ² This is the second reported case in Portugal of the successful delivery of a woman declared brain-dead before the age of foetal viability. In 2016, a Lisbon woman was supported with MPS-BD for 15 weeks after brain death, leading to a successful delivery at 32 weeks' gestation. ³ In that case, the baby left hospital after three weeks in neonatal intensive care. To the best of the authors' knowledge, no further follow-up is available.

The potential need for the provision of MPS-BD

Brain-dead patients experience a multitude of physiological insults resulting in a loss of essential homeostatic brain functions. These abnormalities can be successfully managed in the short term with routine intensive care to normalise physiology and will allow for brain stem death testing if appropriate.^4–6 The original description of brain death, or coma dépassé, was based on the observations of 23 brain-dead patients who had continued circulatory activity for between 2 and 26 days. ⁷ Physiological support after brain death is frequently undertaken in ICU for a short period to facilitate organ donation. However, while the average circulatory survival of BSD patients who receive maximal physiological support over extended times following declaration of BSD in the current era remains unknown, even historical case series show that rapid progression to circulatory death is by no means inevitable.^8,9 Where prolonged physiological support is undertaken after breath death, circulatory survival can persist for months, or even years, as in the well-known case of Jahi McMath. ¹⁰

The most comprehensive study of foetal delivery following MPS-BD was published in 2010. A team from Heidelberg, Germany, analysed 30 cases, reporting successful foetal delivery and neonatal survival in 63%. ⁶ Subsequent case reports are found in both the medical literature^11–13 and the news media,^2,3,14–16 including one case with a live birth after 123 days of MPS-BD following brain death at only nine weeks' gestation. ¹⁵ The only reported case from the UK, included in the Heidelberg study, occurred in 2006. In this case, brain-death occurred at 26 weeks' gestation, when the foetus was physically and legally viable. In this case, MPS-BD was continued to facilitate successful delivery at 30 weeks. ¹⁷

The incidence of brain death in pregnant women in the UK is unknown; such data are not routinely collected by intensive care units, or NHS Blood and Transplant (NHSBT). A recent case series estimated the prevalence of pregnancy among brain dead patients at 2.5%. ¹⁸ There are two cases recorded by NHSBT in the last three years (Gardiner D, NHSBT – personal communications) but this is likely to be an underestimate of the total number.

However, given the tendency of predominantly successful MPS-BD cases to be reported either in the media or literature, it is likely that the majority of brain-dead pregnant women either do not receive MPS-BD or do so unsuccessfully, at least in the UK. The reported ‘success rate’ in the Heidelberg study of 63% arguably overestimates the probability of a live birth in this population. In summary, while the reported number of successful cases of MPS-BD appears to be increasing, there is insufficient evidence to provide meaningful predictive data to clinicians and families considering this treatment, albeit to say that a successful outcome is feasible but by no means certain.

The key legal questions and answers in the UK

The legal definition of death

The diagnosis of death by neurological criteria, known commonly as ‘brain death’, has been incorporated into UK clinical practice since the Conference of Medical Royal Colleges in 1976. ¹⁹ The current edition of the Code of Practice for the Diagnosis and Confirmation of Death, issued by the Academy of Medical Royal Colleges (AoMRC) in 2008, provides guidance for declaring a person dead on the basis of irreversible loss of brainstem functioning. ²⁰ While there is no statutory definition of death in the UK, the AoMRC's Code of Practice states that

the courts in England and Northern Ireland have adopted these criteria as part of the law for the diagnosis of death. There is no reason to think that courts in other parts of the UK would not follow this approach. ²⁰

The legal status of the brain-dead mother

Under the principles of the AoMRC Code of Practice, the legal status of a mother would be that of a dead body once both sets of brain-stem death tests have been completed, with the legal time of death the time of completion of the first set. ²⁰ The jurisdiction over a dead body is traditionally assumed by the Coroner in England, Wales and Northern Ireland, and the Procurator Fiscal in Scotland. However, this jurisdiction was challenged in the recent case of Re: A (A Child), in which the father of a brain-dead child sought permission to transfer him to another country where artificial ventilation would be continued. ²¹ Passing judgement, Hayden J highlighted that no coroner appears to have asserted such authority in circumstances where life support is ongoing following brain stem death. ²¹ He further clarified that the coroner is likely not an appropriate adjudicator of how the body ought to be handled in the diagnosis and confirmation of death using neurological criteria: ‘should a difference of view arise between treating clinicians and family members in circumstances where assisted ventilation is continuing, any dispute, if it cannot be resolved otherwise, should be determined in the High Court, not under coronial powers’. ²¹

A number of offences exist regarding the abuse of dead bodies, including detaining a body and conspiring to prevent a lawful and decent burial. ²² As these offences are grounded in common law, there are no statutes for reference, and their application relies on precedent. While such prosecutions are uncommon, however, it is legally possible that should ongoing treatment of a brain-dead patient be felt to constitute an offence, a prosecution could be brought under these precedents.

It is common practice for brain-dead patients to receive physiological support in ICUs to facilitate organ donation. Legally, this practice is covered in England, Wales and Northern Ireland by the section 43 of the Human Tissue Act 2004 ²³ and in Scotland by the Human Tissue (Scotland) Act 2006, ²⁴ all of which provide a legal framework for the treatment of ‘dead bodies’ for the purposes of organ donation. However, this legislation does not apply to the situation where prolonged MPS-BD would be instituted for the explicit purpose of foetal support.

The legal status of the foetus

It is generally accepted that a foetus in utero does not have explicit legal rights in any UK jurisdiction. This is outlined by the Attorney General's Reference (No. 3 of 1994), which found that a defendant who attacked a pregnant woman, resulting in the postpartum death of a live-born foetus, could not be found guilty of murder as the victim – a foetus – was not a legal person at the time of the incident. ²⁵ In the case of Re F (in utero), a court in England and Wales refused a father's request to make a foetus a ward of court, citing that it is not a person in a legal sense. ²⁶

Each UK jurisdiction does however afford a foetus some degree of legal protection. Abortion is a common law offence in Scotland and a statutory offence in England, Wales and Northern Ireland. ²⁷ In addition, in England and Wales the Infant Life (Preservation) Act 1929 sets out the offence of ‘child destruction’, the act of ‘destroying the life of a child capable of being born alive’. ²⁸ A similar offence exists in Northern Ireland under section 25 (1) of the Criminal Justice Act (Northern Ireland) 1945. ²⁹ Though the protections of the Abortion Act 1967 now allow a defence to abortion in all UK jurisdictions, ³⁰ having been extended to Northern Ireland from October 2019, the underlying legislation remains in place. It is therefore possible that in England, Wales and Northern Ireland an act leading to the death of a viable foetus might be subject to prosecution for an offence of child destruction under the relevant legislation.

While not commenting on MPS-BD specifically, NHSBT guidance does advise that cross-clamping the aorta (an act) in a pregnant organ donor could be prosecuted in England and Wales as the offence of child destruction under the Infant Life (Preservation) Act 1929. ³¹ However, UK case law makes clear distinction between omissions and acts with respect to legal liability of doctors treating patients on life support. The decision of the House of Lords in Airedale vs. Bland indicated that it is legally permissible to withdraw life supporting treatment from a patient if it is not in his best interests. ³² It might reasonably be expected that the courts would apply the precedent of Bland to foetuses, as well as living legal entities. If so, it is likely that withdrawal of MPS-BD would be viewed as an omission, not an act, and thus would not be subject to prosecution. We stress however that this has not been tested legally in any UK jurisdiction.

Summary of the UK legal position

In summary, while there would appear to be no legal impediment to withdrawal of MPS-BD in any UK jurisdiction, this is a presumption that has yet to be tested in the courts, especially in Northern Ireland, where it could be considered that a foetus does have a legal status (though this is similarly untested). Should the courts apply the precedent of Bland as they have previously, the withdrawal of MPS-BD would likely constitute an omission, not an act, and doctors would be unlikely to be subject to prosecution.

The legal status of the mother is even less clear. Under the terms of the AoMRC Code of Practice, the legal standing of a brain-dead pregnant woman is that of a dead body. It is possible that should ongoing treatment of the mother's ‘dead body’ be found to be objectionable, a common-law charge of ‘conspiracy to prevent a decent and lawful burial’ could be pursued. However, in the recent case of Re: A (A Child), the court asserted that the High Court, rather than the coroner, should have authority to make final decisions while a patient is still receiving artificial life support, even when brain dead. ²¹ It could be argued that with regard to a dispute over continuation of artificial life support, the court treated a ventilated brain-dead patient effectively in the same way as they would a living person with irreversible loss of capacity.

An argument in favour of the provision of MPS-BD

As in many ethical scenarios regarding pregnancy, decisions regarding MPS-BD require consideration of the respective rights of both mother and foetus. In the context of MPS-BD, the mother, by definition, has irreversibly lost her ability to express her autonomy (which in other contexts is often determinative). While the official legal status may be that of a dead body, brain-dead patients in clinical practice are often treated, and thought of, as patients who have irreversibly lost capacity, and indeed the courts have on occasion followed this approach as in the above case of Re: A (A Child). ²¹ It may therefore be more appropriate to deploy a model of decision-making similar to the ‘best interests’ model used where patients lose capacity. In such a model, patients’ relatives are consulted to ascertain information about the patient's previously stated wishes, values and beliefs. Clinicians use this information – in conjunction with their understanding of the clinical context – to determine the most appropriate course of action in a particular case.

While this decision-making standard is distinct from substituted judgment and patients’ wishes, values and beliefs are not legally binding in and of themselves, they often hold significant influence when considering a patient's interests. The Supreme Court ruling in Aintree vs. James was clear that ‘interests’ must not be limited to the physical state of a patient and must be a broad view which would certainly include a wish to bring about the healthy birth of a child. ³³ This implies that if there were clear evidence that a brain-dead mother would have wanted MPS-BD to continue, it could ethically be attempted under the aforementioned paradigm of treating the brain-dead patient as a living patient without capacity. However, the Supreme Court were clear that they could not compel a doctor to provide a treatment they felt was ‘without indication’. ³³

Conversely, several cases of MPS-BD against the stated wishes of a brain-dead mother have been documented, typically in jurisdictions where legislation grants a foetus an explicit or effective right to life. In the case of Miss P, an Irish woman was supported with MPS-BD against the wishes of both her family and treating clinicians (prior to the repeal of the Eighth Amendment to the Irish constitution). ³⁴ In the case of Marlise Muñoz, a Texas woman was treated with MPS-BD in direct contravention of an advance directive. ³⁵ In both cases, courts eventually ruled to order the cessation of MPS. Where MPS-BD is not in keeping with the previously stated wishes of a patient, it would be difficult to ethically justify a decision to continue treatment given the clear infringement on a woman's dignity associated with invasive treatment.

As well as a significant emotional burden on the patient's family and ICU staff, MPS-BD is a significant use of resources. The UK has one of the lowest numbers of ICU beds per capita in Europe, ³⁶ and the admission of a Level 3 patient who is mechanically ventilated for 13–15 weeks would have significant implications for bed capacity of most ICUs. The strict utilitarian might argue that this would represent prioritisation of a foetus – a potential life – over other living patients in the hospital who might suffer as a result of critical care bed shortages. However, as these cases are so rare, the resource implication to the NHS on a wider scale is likely to be small.

The literature clearly reflects that in many cases, clinicians feel an impetus to offer MPS-BD. Even in a jurisdiction where a foetus may be without significant legal status, it is clear that society in general regards a foetus to have a degree of moral value, and that where it is within the capabilities of medical professionals to facilitate foetal delivery, many wish to do so. The motivations for this may be multiple: to fulfil the presumed dying wish of a patient, to allow ‘some good to come’ of the tragic death of a young woman or to use available medical technology to allow a potentially viable pregnancy to come to term.

The question therefore is – under what circumstances is MPS-BD ethical? We would suggest the following prerequisites:

a reasonable expectation of the possibility of successful foetal delivery;

a reasonable belief that it would be in the interests of the brain-dead mother to undergo prolonged MPS in order to bring about the delivery of the foetus.

In terms of the first prerequisite, the current evidence base does not allow even a weak recommendation in terms of a likely success rate, save to say that successful MPS-BD is feasible but by no means certain. If, as in the sole reported UK case, brain death has occurred at, past, or very close to the age of foetal viability, ¹⁵ the first prerequisite is likely to be met, as the required duration of MPS-BD is short. In a case similar to that of Catarina Sequeira, where many months of MPS-BD would be required to reach the age of foetal viability, logic dictates that the probability of successful delivery would be lower, although there is no evidence to support this. Should there be clear manifestations of multi-organ failure refractory to medical treatment even at an early stage – as was reported in the case of Miss P, who had developed necrotic tissue secondary to extra-ventricular drain insertion ³⁴ – the likelihood of success would be far lower, the balance would likely be in favour of discontinuing MPS-BD.

In terms of the second point, discussion with the family would be key to determining the patients' previously stated values, wishes and beliefs in order to inform what would be in the patient's interests. In the absence of evidence to the contrary, it would be reasonable to assume that a pregnant woman would wish to successfully deliver the child. In terms of determining a patient's interests, it would also be reasonable to assume that a patient would not wish her family members to go through undue distress or suffering, nor to suffer indignity herself (even if they were not capable of suffering in a conscious fashion).

In the case study, the fact that Catarina Sequeira had not opted out of Portugal's presumed consent law for organ donation was used by the hospital's ethics committee to justify continuing MPS-BD. ² Presumed consent for organ donation exists in Wales and is planned to be introduced in England and Scotland in the near future.^37–39 It could be argued that MPS-BD to facilitate organ donation and to facilitate foetal delivery are similar ethical paradigms: in both cases, the brain-dead person is treated as a temporary ‘container’ of items (foetus and organs) which society deems valuable, that medical professionals determine to retrieve at the time they deem best. While a prior stated wish in favour of organ donation could be used to support a decision to MPS-BD, implying that a patient would not object to continued artificial ventilation in a brain-dead state in order to preserve life, the duration of MPS-BD, and hence the ‘burden’ of the treatment, differs significantly between these two objectives. In the absence of other evidence of a patient's wishes or values, we would argue that support for organ donation alone is unlikely to ethically justify MPS-BD.

Perhaps the most difficult scenario would be one where the family state a strong wish for MPS-BD to continue, but clinicians feel that it is not indicated, either for clinical or ethical reasons (either or both of the above-suggested prerequisites not being met). This could be the case in very early pregnancy, where complications of brain-death or the primary injury are already manifesting, as were reported in the case of Miss P, ³⁴ or where other evidence exists that MPS-BD would not be in the mother's best interests. With increased media awareness of such cases, however, and increasing public expectations of what medicine, and particularly critical care, can achieve, there exists the possibility of conflict between clinicians and family members. Resolution of such conflict should involve the early input of specialist teams, as well as discussions with families as to what defines ‘success’ for them. Given the extensive legal ambiguities listed above, clinicians should seek early legal advice and, if necessary, recourse to the courts.

Conclusions

Cases of brain-death in early pregnancy are inevitably difficult for all involved. While the literature is scant and undoubtedly skewed by publication bias, studies indicate that MPS-BD following brain-death in early pregnancy may be a feasible strategy to deliver a viable foetus, though the exact chance of success at any given gestational age is unclear. There is a real possibility for this situation to arise in UK intensive care units, particularly with the increasing frequency of BSD testing in the UK. The legal situation in the UK is complex and untested. Under common law, the legal status of a brain-dead person is that of a dead body, but in the recent case of Re: A (A Child), the High Court treated a ventilated brain-dead patient as they would a living person with loss of capacity for the specific issue of ongoing artificial ventilation. Paradoxically, there exists potential for prosecution both in the case of institution or continuation of MPS-BD (under common law) and withdrawal of MPS-BD (under the offence of child destruction in England, Wales and Northern Ireland and/or common law in Scotland), though the latter is less likely assuming the courts continue to apply the principles of Bland, under which it would represent an ‘omission’. Given this situation, we recommend early legal advice, especially given the courts’ willingness to supersede coronial jurisdiction with regard to such patients.

An ethical paradigm of shared decision-making with respect to the brain-dead mother, similar to that used with patients who have irretrievably lost capacity, may allow clinicians to identify cases in which prolonged MPS-BD would be ethically justifiable. The precedent of Aintree vs. James is clear that any such assessment of ‘interests’ must be broad and not limited to a patient's physical status. We suggest that this is likely to be the case if the clinical team have a reasonable expectation of the possibility of successful foetal delivery, and a reasonable belief that it would be in the interests of the brain-dead mother to undergo prolonged MPS in order to bring about the delivery of the foetus.