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Clinical Nutrition (2006) 25, 196–202

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INTRODUCTION PART TO THE ESPEN GUIDELINES ON ENTERAL NUTRITION

Ethical and Legal Aspects of Enteral Nutrition

U. Kornera,�, A. Bondolfib, E. Buhlerc, J. MacFied, M.M. Meguide,B. Messingf, F. Oehmicheng, L. Valentinih, S.P. Allisoni

aCharite—Universitatsmedizin Berlin, Berlin, GermanybCentre lemanique d’ethique, Batiment de Provence, Lausanne, SwitzerlandcGeriatrischer Schwerpunkt, Stadtische Kliniken Esslingen, Esslingen, GermanydDepartment of Surgery, Scarborough Hospital, Scarborough, UKeDepartment of Surgery, Upstate Medical University, Syracuse, USAfService d‘hepatogastroenterology et d‘assistance nutritive, Hopital Lariboisiere, Paris, FrancegAbt. Intensivrehabilitation, Bavaria Klinik Kreischa, Kreischa, GermanyhDepartment Gastroenterology, Charite—Universitatsmedizin Berlin, Berlin, GermanyiClinical Nutrition Unit, University Hospital, Queens Medical Centre, Nottingham, UK

Received 21 January 2006; accepted 21 January 2006

KEYWORDSEnteral nutrition;Tube feeding;Oral nutritional sup-plements;Ethics;Law;Patient autonomy;Incompetence

ee front matter & 2006lnu.2006.01.024

ing author.ess: uwe.koerner@char

Summary European ethical and legal positions with regard to EN vary slightly fromcountry to country but are based on a common tradition derived from Graeco Romanideas, religious thought and events of the 20th century. The Hippocratic tradition isbased on ‘beneficience’ (do good) and ‘non-maleficience’ (do no harm). Religiousthinking is based upon the presumption of providing food and drink by whatevermeans unless burden outweighs benefit. The concept of ‘autonomy’ (the patientsright to decide) arose following in the decades after the Second World War and isenshrined in Human Rights law. The competent patient has the right to participate indecision making and to refuse treatment although the doctor is not obliged to givetreatment which he or she considers futile or against the patient’s interests. Theincompetent patient is protected by law. The fourth principle is that of ‘justice’ i.e.equal access to healthcare for all.

The law regards withholding and withdrawing treatment as the same. It alsodefines the provision of food and drink by mouth as basic care and feeding byartificial means as a medical treatment. It requires doctors to act in the bestinterests of the patient.

The full version of this article is available at www.espen.org.& 2006 European Society for Clinical Nutrition and Metabolism. All rights reserved.

European Society for Clinical Nutrition and Metabolism. All rights reserved.

ite.de (U. Korner).

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Introduction

These guidelines address some of the ethical andlegal issues which are increasingly part of theclinical decision-making process involved in provid-ing nutrition support. The European ethical tradi-tion is based on the Graeco–Roman ideas, refinedby religious considerations and further developedduring the 20th century.

Q: What is the basis for the European ethicaltradition in Medicine?

A: The Hippocratic ethical code is based on‘beneficience’ i.e. do good, and ‘non-maleficience’i.e. do no harm. This tradition was, however,paternalistic, and it was not until the 20th centurythat the notions of ‘autonomy’ i.e. the patient’sright to decide, and ‘justice’ i.e. equal rights forall, were introduced. Religious ideas have alsocontributed.

Comment: The Hippocratic tradition, refined byRoman physicians, was based on the ‘do good butdo no harm’ principles. It also embodied the notionof confidentiality but eschewed autonomy, and wasmotivated by ‘philanthropia’ i.e. do good in orderto preserve the physician’s reputation. Hippocrateswrote ‘Give necessary orders with cheerfulness andsincerity, turning his (the patient’s) attention awayfrom what is being done to himy revealing nothingof the patient’s future or present condition’ In the1st century AD, Scribonius Largus, physician to theEmperor Claudius, took a step nearer our modernattitude by encouraging physicians to base deci-sions on Humanitas, that is love of mankind, and onMisercordia, or mercy. Enteral feeding has a 500 yrhistory in Europe and its principles were defined byJohn Hunter in 1793, when he wrote concerning apatient with paralysis of the swallowing muscles. ‘Itbecomes our duty to adopt some artificial mode ofconveying food into the stomach, by which thepatient may be kept alive while the diseasecontinues’. The concept of ‘starve a fever andfeed a cold’, prevalent since Galen in the 4thcentury AD, was abandoned in the 19th century,when several authors emphasised the importanceof feeding in medical care.

As a new principle the respect for patient’sautonomy arose in the seventies of the 20thcentury. The competent patient now has the rightto participate in all the decision-making concerninghis treatment, and the law provides safeguards forthe patient who is ‘incompetent’ i.e. incapable ofunderstanding or making decision. The paternalis-tic approach of Hippocrates was therefore super-

seded by that of autonomy. On the other hand,despite a number of recent legal cases, the doctoris still not obliged to submit to pressure by thepatient, relatives or others, to give treatmentwhich he or she believes to be futile or against thepatients’ interests i.e. the burden or adverseeffects outweigh benefit. European religious tradi-tions, both Christian and Jewish, are sometimeserroneously supposed to favour preservation of lifeat all costs. In fact, Roman Catholic teaching isclear that there should be a presumption in favourof providing nutrition and hydration provided thatit is of sufficient benefit to outweigh the burdensto the patient. This involves judgements concern-ing the quality of life which has assumed increasingimportance in assessing the efficacy of treatment.One may contrast the use of tube feeding insituations where it may not prolong life, but whereit improves it’s quality, with treatments which mayprolong life at the expense of prolonged suffering.In most countries the physician may not end life,but on the other hand is not required officiously toprolong the process of dying. Orthodox Jewishthinkers regard the dying person in a special lightand argue against impediments to dying in the finalyear of life.

The growth of National Health Services in Europehas seen the increasing recognition of ‘justice’(equal access to healthcare for all) as an importantethical concept. On the other hand the growth indemand for healthcare and new technical develop-ments face all societies with the problem ofsatisfying infinite demand with finite resources.

Society and its political representatives have yetto face up to the problem of enormously expensiveand sometimes futile treatment of the few, whichmay so consume resources in staff, facilities andmoney as to deny proper treatment of those morelikely to benefit and survive. The doctor is there-fore faced with balancing ‘justice’ against ‘bene-ficence’ and ‘autonomy’, and trying to deploy thelimited resources available to achieve the max-imum benefit. Through legal and other conflicts(see below), there may be difficulties in the way ofwithdrawing expensive but ineffective treatment inorder to use the resources of the nutrition careteam to better effect. In cases of conflict, theadvice and support of local ethical committees maybe helpful.

Q: Is there a difference between ethicalprinciples and legal framework?

A: Yes, although the laws of European countries(which may differ in some details between

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countries) are based on the common ethicaltradition described above.

Comment: Ethical codes of caring professionsinclude not only minimal acceptable standards ofbehaviour, but also ideals, and have been describedas ‘the collective conscience of our profession’.The law, on the other hand, defends individualrights and liberties and sets minimum standardsbelow which professional conduct can be regardedas lacking in care, negligent or downright criminal.It also protects those who are unable or incompe-tent to make decisions on themselves. In addition,it provides some safeguards and protection fordoctors and other professions. It has embodied theprinciple, for example, that no doctor can beobliged to provide treatment which he/she be-lieves to be against the patients’ interests or futile.This delicate balance between patients’ legal rightsand professional judgement has, however, beenthreatened by recent unfortunate legal judgementsin the UK and USA, whose consequences have yet tobe defined. Unprincipled political interference,stimulated by extreme pressure groups, is also athreat that the professions will need to resist.Fortunately, Europe in general has continued tomaintain a liberal and humane approach to theseproblems.

In the judgement of risk versus benefit in themedico-legal context, it is clearly vital that theprofessional who wishes to avoid or to provide adefence against litigation should be fully conver-sant with the latest medical evidence and beappropriately trained and experienced.

Q: What are the implications of the law forthe organisation and conduct of nutritionalsupport?

A: As with other treatments, the best results areobtained by teams trained and organised to carry itout. This is of particular relevance to artificialmeans of nutritional support.

Comment: There is sufficient evidence, in thecase of parenteral nutrition, that specialisednutrition teams obtain the best results, with thefewest complications. There is some evidence also,in the case of enteral tube feeding, that experi-enced and properly organised groups, working toagreed protocols, have fewer complications andbetter outcomes than those who provide occasionalor ad hoc treatment. There is, therefore, a risk oflitigation if artificial nutrition, conducted by theinexpert, results in serious complications, beyondthe normal risks inevitably associated with anyform of intervention.

Q: How does the law regard enteral nutrition?Is it basic care or a medical treatment?

A: The law differentiates between oral intakeand enteral tube feeding. While tube feeding isclearly considered therapy, oral nutritional supple-ments can be basic care as well as therapy. Oralnutritional supplements are therapy under certainconditions e.g. if pharmacologic effects should beachieved by specific composition (BCAA, etc.) Theprovision of adequate fluid and nutrients by mouthincluding oral nutritional supplements in mostinstances as well as help with drinking and eatingwhere necessary is regarded by the law as basiccare.

Comment: Although paediatricians have argued,with good reason, that tube feeding of the neonateis part of basic care, in the older child and adult itis generally accepted that nutrition by artificialmeans is a medical treatment, involving profes-sional judgement and intervention, governed bythe laws related to medical practice. On the otherhand, oral intake is governed by the laws related toduty of care and to Human Rights, whereby anyperson, organisation or institution that undertakesto provide care is obliged to provide and ensure anadequate oral intake of food and fluid wherepossible and as acceptable to the patient. Acompetent patient is entitled to refuse food anddrink and, indeed, many dying patients do. It isunkind and improper to try to force unwillingpatients to eat or swallow.

Q: When is a patient competent to exerciseautonomy and who decides for the incompetentpatient?

A: The laws differ in detail and emphasis on thispoint between countries, although the principlesremain similar. For the definition of competence,see below. If by reason of psychiatric or braindisease the patient is not able to understand theissue or express a view, the doctor has a number ofoptions.

1.

Has the patient written a ‘living will’ expressinghis/her wishes concerning treatment underthese circumstances? Such written testamentsshould be respected and will increasingly beregarded as legally binding.

2.

Alternatively, has the patient ever expressedhis/her wishes verbally to family or friends? Suchexpressions should be considered and respected.

3.

In some countries the family has legal rights tomake decisions.

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4.

The patient may previously have appointed amember of the family, a friend, or lawyer to betheir legal guardian at a time when he/she wasincompetent to make decisions. Such personshave legal autonomy.

5.

In a few cases, (see below), reference to thecourts may be necessary. The court may appoint‘guardian ad litem’ (particularly in children) orempower the doctor to take a decision ‘in thebest interests of the patient’.

6.

Although it is not legally binding to do so, thedoctor should always consider and respect theviews of all the members of the team who shouldbe participants in any decision making whetherthe patient is competent or not.

Q: How is legal competence defined?

A: Competence under civil law is not to beequated with patient’s ability to give his/herconsent. Only the following conditions excludeindividuals from legal competence under civil law:

1.

Children under 14 resp. 18 yr: In children under14 yr (in some countries under 16 yr), theparents have the authority to make decisionsunless the courts specifically remove or takeover that authority. Adolescents between 14 and18 yr should be informed according to theirpsychosocial maturity and their consent shouldbe recognised and/or carried out.

2.

Severe psychiatric illness. Whenever a psychia-trist and other required people have certifiedthe patient, in a legally approved manner, asincapable of making rational decisions. Thisincludes those with anorexia nervosa and severedepression, but not those imprisoned for otherreasons. Indeed it is conceivable that doctorscould be sued for failing to give artificialnutrition in such cases where malnutrition is lifethreatening.

3.

Primary brain or other disease, which rendersthe patient temporarily or permanently incap-able of understanding or of expressing, wishesby any means.

Comment: Even patients without legal compe-tence under civil law should be informed about theplanned measures according to his/her mentalcapacity.

In general, a patient has the ability to consentwhen he/she is able to understand the benefits,risks and consequences of the respective interven-tion as well as the consequences of the omission ofthe measure, and is able to make a self-determined

decision. The patient may be temporarily orpermanently unable to consent to complex mea-sures, but may well be able to consent to simpleones. Intellectually, the decision concerning tubefeeding may be a simple one, yet emotionally it is acomplex issue. The attending physician must assessthe patient’s ability to consent separately for eachtherapeutic decision and must document theconversation carefully. For instance, underagedadolescents will obtain their ability to decide abouta nutritional therapy quite early, because normallythis is a rather simple and low-risk therapeuticmeasure.

In relation to (3) above, the British MedicalAssociation and the Law Society have publishedclear guidelines on the assessment of mentalcapacity:

A person should be able to:

�

Understand in simple language what the medicaltreatment (or research intervention) is, itspurpose and why it is proposed. � Understand its principle benefits, risks and

alternatives.

� Understand in broad terms what will be the

consequences of not receiving the proposedtreatment.

� Retain the information for long enough to make

an effective decision.

� Make a free choice without pressure.

The process of communicating verbally, bywritten word, or by signs, may sometimes bedifficult. However, the doctor should not betempted to underestimate the patient’s capacityto make a decision and should make every attemptto assist this process, including, in the case of afluctuating mental state, returning at a time whenthe patient is in a less confused phase.

Q: What should be done in case of doubtwhether enteral tube feeding will be beneficialor when the prognosis of the underlying condi-tion is uncertain?

A: If in doubt give a trial of treatment. Thisshould be for a defined period agreed among allmembers of the team and with the patient’s familyand/or representative. Goals and criteria forcontinuing or discontinuing the feed should beagreed in advance.

Comment: Acute stroke affecting swallowing is atypical example of this type of problem, in whichprognosis may be uncertain for the first 2–3 weeks,during which nutritional support should be given to

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prevent malnutrition developing and thereby im-pairing recovery in those whose neurological con-dition improves. The decision to start treatment isalso governed, of course, by the current orpreviously expressed wishes of the patient or bythe views of a legal guardian. In contrast, patientswith terminal brain disease e.g. tumour, Alzhei-mer’s etc may suffer more risk from tube feedingthat benefit, so that the ethical balance may beagainst treatment.

Q: How does the law regard withdrawing orwithholding tube feeding?

A: Withdrawal is regarded in the same way aswithholding treatment in the first place i.e. is it inthe best interests of the patient, and do the risksoutweigh the benefits? Also, it is concerned thatautonomy has been preserved and that the patientor legal guardian have been consulted and givenapproval.

Comment: There are certain situations e.g.persistent vegetative state or when there is conflictbetween professional judgement and the wishes oflegal guardian or family, when the courts need tobe involved before any action is taken.

The current attitude of the law is yummarized bya legal judgement as follows:

Medical science and technology has advanced fora fundamental purpose: the purpose of benefitingthe life and health of those who turn to medicineto be healed. It surely was never intended that itbe used to prolong biological life in patients bereftof the prospect of returning to an even limitedexercise of human life

One religious and ethical authority has arguedthat preventing doctors withdrawing treatmentwhere it is providing no benefit is unethical sinceit would discourage trials of treatment wherebenefit is initially in doubt. This view supports theconcept of planned and limited trials of treatmentundertaken after full discussion with all concerned,with agreed goals and grounds for withdrawalshould the treatment prove ineffective or burden-some to the patient.

Special situations

Persistent vegetative state

Q: In cases of severe brain damage where theprospect of recovery is extremely unlikely, how

does the law regard withdrawal of food and fluidadministration by tube?

A: The law was clarified by the Cuzan case in theUS and by the Tony Bland case in the UK. The courtswill not entertain an application to withdrawtreatment within 12 months of the onset of thecondition, by which time it becomes possible todetermine whether the patient has lost all featuresof personhood although brain stem function persistsi.e. a persistent vegetative state. The court maythen give permission for doctors to stop treatment,‘if it is in the best interests of the patient’.

Comment: The courts usually require that thepatient has been examined serially over a period oftime by an expert in the field of brain damage withspecial experience of such cases.

Dementia

Q: What is the role of enteral feeding indementia?

A: In early or mild dementia, memory loss affectspeople’s awareness or memory of meal times, sothat meals may be missed. The supervision of mealsand the provision of finger buffet snacks from whichthe demented person can help themselves betweenmeals have proved adequate to ensure propernutrition. As the condition worsens, oral supple-ments may be justified. With intercurrent rever-sible illness, the patient should be considered inthe same way as those without dementia. In thelate stages of disease, Alzheimer’s or cerebro-vascular dementia, the balance of evidence is thatartificial tube feeding has more risks than benefits,and should not be undertaken. Attention to comfortand dignity take precedence over nutritional orfluid therapy.

Comment: In recent studies of terminal demen-tia, it was shown that tube feeding does notprolong life and causes more complications thanbenefits. It reminds us that loss of appetite andthirst are terminal features in this fatal condition,as in other terminal illnesses at a late stage.

Malignant disease

Q: Does enteral feeding have a significant rolein terminal cancer?

A: The role of enteral feeding in oncologygenerally is summarised in chapter Oncology, interminal cancer, oral supplements may be useful,

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and tube feeding may be beneficial on obstructivelesions of the gastrointestinal tract. Treatmentshould be dominated by the need to providecomfort and symptom relief rather than by anyform of aggressive nutritional support.

The dying patient

Q: How does our ethical tradition guide us?

A: Even religions e.g. Roman Catholicism, Juda-ism, which may be supposed to be in favour of life,regard the process of dying in a special light andonly urge a presumption in favour of providingnutrition and hydration provided that this is ofsufficient benefit to outweigh the burdens involvedto the patient. It is one of the physician skills toknow when curative or aggressive treatment shouldbe abandoned in favour of the provision of care,comfort, symptom relief and the preservation ofdignity. It involves a recognition of the dyingprocess, which may be rapid or prolonged overmany months.

Q: What are the threats to medical ethics?

A: There are political, business, insurance,reimbursement and management issues, whichmay directly or subtly erode professional ethicalpractice. For the proper conduct of medical care, itis important that the professions resist any erosionof a firm and clear ethical stance, which is the markof a profession.

Comment: Doctors themselves should ensuretheir own ethical behaviour as well as resistingexternal pressures to weaken ethical rules. On theother hand, ethics must be made relevant tomodern conditions and the doctor has, increasingly,a responsibility to balance fair distribution ofresources (justice) against individual benefit (ben-eficence) and even autonomy where this becomesunreasonable in its demands on resources.

Further reading

1. Allison SP. Organization and legal aspects. In: Sobotka L,editor. Basics in clinical nutrition. 3rd ed. Prague: GalenPress; 2004. p. 139–47.

2. American Dietetic Association. Ethical and legal issues innutrition, hydration, and feeding (Guidelines). J Am DietAssoc 2002;102:716–26.

3. Angus F, Burakoff R. The percutaneous endoscopic gastro-stomy tube: medical and ethical issues in placement. Am JGastroenterol 2003;98/2:272–7.

4. Brett AS, Rosenberg JC. The adaequacy of informed consentfor placement of gastrostomy tubes. Arch Intern Med2001;161:745–8.

5. Buckley T, Crippen D, DeWitt AL, et al. Ethics roundtabledebate: withdrawal of tube feeding in a case with persi-stent vegetative state where the patients wishes areunclear und there is family dissension. Crit Care 2004;8/2:79–84.

6. Casarett D, Kapo J, Caplan A. Appropriate use of artificialnutrition and hydration—fundamental principles an recom-mendations. N Engl J Med 2005;353:2607–12.

7. CREST [Clinical Resource Efficiency Support Team] homeenteral tube feeding working groups (2004) Guidelines forthe management of enteral tube feeding in adults.www.crestni.org.uk.

8. Finucane TE, Christmas C, Travis K. Tube feeding in patientswith advanced dementia: a review of the evidence. JAMA1999;282:1365–70.

9. Gillick MR. Rethinking the role of tube feeding in patientswith advanced dementia. N Engl J Med 2000;342/3:206–10.

10. Gillick MR. Artificial nutrition and hydration in the patientwith advanced dementia: is withholding treatment compa-tible with traditional Juadism? J Med Ethics 2001;27:12–5.

11. Keown J. Medical murder by omission? The law and ethics ofwithholding and withdrawing treatment and tube feeding.Clin Med: J R Coll Phys London 2003;3/5:460–3.

12. Klose J, Heldwein W, Rafferzeder M, et al. Nutritional statusand quality of life in patients with percutaneous endoscopicgastrostomy (PEG) in practice: prospective one-year follow-up. Dig Dis Sci 2003;48/10:2057–63.

13. Kolb C. Nahrungsverweigerung bei Demenzkranken: PEG-Sonde—ja oder nein? (83 Seiten, graph. Darst.) Frankfurt amMain: Mabuse-Verlag; 2003.

14. Korner U, Biermann E, Buhler E, et al. Leitlinie EnteraleErnahrung der DGEM und DGG: Ethische und rechtlicheGesichtspunkte. Aktuelle Ernahrungsmedizin 2004;29/4:226–30.

15. Kunin J. Withholding artificial feeding from the severelydemented: merciful or immoral? Contrast between secularand Jewish perspectives. J Med Ethics 2003;29:208–12.

16. Lennard-Jones JE. Ethical and legal aspects of clinicalhydration and nutritional support. BJU Int 2000;85/4:398–403.

17. Lennard-Jones JE, working party A positive approach tonutrition as treatment. Report on the role of enteral andparenteral feeding in hospital and at home. London: KingsFund Centre; 1992.

18. Loewy EH. Ethics, nutrition and society: where do we standtoday? Wien Klin Wochenschr 1997;109/24:964–7.

19. MacFie J. Ethics and nutrition. Wien Klin Wochenschr1997;109/21:850–7.

20. Mitchell SL, Buchanan JL, Littlehale S, et al. Tube-feedingversus hand-feeding nursing home residents with advanceddementia: a cost comparison. J Am Med Directors Assoc2003;4/1:27–33.

21. Mitchell SL, Kiely DK, Gillick MR. Nursing home character-istics associated with tube feeding in advanced cognitiveimpairment. J Am Geriatr Soc 2003;51/1:75–9.

22. Murphy LM, Lipman TO. Percutaneous endoscopic gastro-stomy does not prolong survival in patients with dementia.Arch Intern Med 2003;163/11:1351–3.

23. Oehmichen F. Kunstliche Ernahrung am Lebensende. In:Korner U (Hrsg.) Berliner Medizinethische Schriften No.45,Dortmund: Humanitas Verlag; 2001.

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24. Rabeneck L, McCoullough LB, Wray NP. Ethically justified,clinically comprehensive guidelines for percutaneous endo-scopic gastrostomy tube placement. Lancet 1997;349:496–8.

25. Sherman FT. Nutrition in advanced dementia. Tube-feedingor hand-feeding until death. Geriatrics 2003;58/11(10):12.

26. Simon A. Ethische Aspekte der kunstlichen Ernahrung beinichteinwilligungsfahigen Patienten. Ethik Med 2004;16:211–6.

27. Slomka J. Withholding nutrition and the end of life: clinicaland ethical issues. Cleveland Clin J Med 2003;70/6:548–52.

28. Swaroop VS, Bergstrom LR. Percutaneous endoscopic gastro-stomy in patients with dementia. Am J Gastroenterol2003;98/8:1904 (Comment on Angus/Burakoff).

29. Truog RD, Cochrane TI. Refusal of hydration and nutrition.Irrelevance of the ‘‘artificial’’ vs ‘‘natural’’ distinction. ArchIntern Med 2005;165:2574–6.