ISSUES IN CLINICAL NURSING

Inducements for medical and health research: issues for the profession

of nursing

Linda Shields PhD, FRCNA, FRSA

Professor of Nursing, University of Hull, Hull, UK; Honorary Professor, University of Queensland, Brisbane, Qld, Australia;

University of Northumbria, Newcastle-upon-Tyne, UK; and Visiting Fellow, Orebro University, Orebro, Sweden

John Pearn MD, FRACP, FRCP

Chair, Ethics Committee, Royal Children’s Hospital and RCH Foundation, Royal Children’s Hospital & Health Service

District, Brisbane; and Department of Paediatrics and Child Health, Royal Children’s Hospital, Brisbane, Qld, Australia

Submitted for publication: 21 August 2006

Accepted for publication: 8 October 2006

Correspondence:

Linda Shields

Faculty of Health & Social Care

University of Hull

Cottingham Rd

Hull HU6 7RX

UK

Telephone: þ44 1482 463326

E-mail: L.Shields@hull.ac.uk

SHIELDS L & PEARN J (2007)SHIELDS L & PEARN J (2007) Journal of Clinical Nursing 16, 1196–1200

Inducements for medical and health research: issues for the profession of nursing

Aims and objectives. Inducements, incentives, reimbursements and payment to

subjects for participation in research projects raise many practical, professional and

philosophical issues for nurses. Nurses are enjoined, either formally as research

co-participants or informally as patients’ professional carers, in any research which

involves their patients. This role inescapably brings significant ethical obligations,

which include those of bioethical audit.

Background. A review of current international guidelines on reimbursement rec-

ommendations indicates that researchers select one of several paradigms which

range from the ‘commercial market model’ of supply and demand to that of pure

un-reimbursed altruism. In this latter, volunteers not only give their bodies and

emotional commitment, but also sacrifice their time and convenience. Inducement is

defined as the provision of resources or rewards which exceed the ‘resource neutral’

compensation for legitimate expense. If potential volunteers are truly free to make

an informed choice to participate in research, no ethical compromise exists if

inducements are offered; but by so doing both the research team and the volunteer

patients have shifted the ethos of their research from caritas and altruism to one of a

simple commercial relationship.

Conclusions. Inducements are inappropriate when offered to those who are

‘ethically captive’ in the sense that autonomy of choice may be compromised.

Relevance to clinical practice. In contemporary nursing practice, research involve-

ment is both frequent and desirable. A perspective of current debate about

inducements for volunteering, including legal and ethical issues, empowers nurses

to protect the patients or clients in their care.

Key words: ethics, history, nurses, nursing, research

1196 � 2007 The Authors. Journal compilation � 2007 Blackwell Publishing Ltd

doi: 10.1111/j.1365-2702.2007.01889.x

Introduction

Research in the health disciplines involves researchers and

their volunteer subjects and the professional staffs who are

enjoined in and who often monitor the research. Such staff –

nurses, doctors, therapists and medical scientists – can and do

act as ‘coal-face’ auditors of issues inherent in health-care

research. Nurses who care for those patients who are research

subjects may find themselves in purely service roles, as a co-

researcher within the project team, or as a combination of

both. Irrespective of their role, nurses are inescapably

engaged in the ethics of any research which involves their

patients. This involvement may be informal, but the ethical

responsibilities remain the same. Such professional involve-

ment and audit may be purely technical, more broadly

professional or may be explicitly focused on the ethical

domain.

In the UK in March 2006, eight young men were injected in

the study of a new drug in a phase 1 trial (Bhattacharya &

Coghlan 2006). Two received a placebo, and six the drug.

Those who received the drug had volunteered to be the first

humans to be so exposed. They collapsed and required life

support. It transpired that these healthy volunteers had been

offered a considerable sum to participate in the research.

Events have shown that nothing could compensate them for

the ordeal of fighting for their lives.

Nurses are today essential to all interventional health

research. Either they conduct their own studies, work as team

members on research projects, or provide clinical care for

patients or clients who are participating in studies as subjects.

It is obvious, therefore, that an understanding of the ethics of

offering inducements, incentives and capitation reimburse-

ments (the terminology changes) to subjects is a necessary

corpus of professional knowledge. The related issue of

compensation for injuries sustained in the research context

is equally important; but is not covered in this paper.

We explore here several concepts that relate to this topic,

focused within the perspective of the profession of nursing. A

discussion on offering inducements to volunteers as potential

subjects for health research involve: (i) a review of current

guidelines on research reimbursements; (ii) issues of altruism;

(iii) ethical issues particularly as these relate to those who are

‘captive subjects’ in the ethical sense; and (iv) several legal

issues as these impinge on the participating nurse.

Current models – reimbursements andinducements

By inducements we mean incentives, payments or gifts which

are offered to potential volunteers for their enrolment in

medical research. Sometimes, inducements are offered to

volunteer subjects who are already enrolled and participating

in research, to persuade them to continue. Even bioethicists

find the theme of inducements for medical research a

controversial issue. For example, following a Scottish study

in which healthy volunteers were paid £600 to drink orange

juice laced with pesticides (Cook et al. 1998), it was found

that ‘bioethicists cannot decide… whether we should be

worried that healthy people are being paid to enrol in (such)

research studies’ (Lemmens & Elliott 2001, p. 51).

In current practice, offers of ‘fair and reasonable compen-

sation’ for travel and incidental expenses are usually offered

to potential volunteers. Beyond this, there exists a baseline

framework, both regulatory and practical, which has a

profound effect on how the ethical theories behind decisions

surrounding inducements are made. The most common

models for inducements for involvement in research are

highlighted in guidance from the UK Central Office for

Research Ethics Committees (COREC) (Central Office for

Research Ethics Committees 2005), which oversees the

ethical evaluation of research carried out within the National

Health Service in the UK. COREC suggests that there are

three models which can be used, under which payment

remains ethical. Such guidelines are based on seminal work of

Dickert and Grady (1999). The first is the ‘market model’ in

which payment is controlled by supply and demand. The

second is the ‘wage payment model’ where an amount of

money is set at the level of wages of unskilled workers, but

where extra is given for burdensome procedures. The third

model, the ‘reimbursement model’ sees payment given

according to the financial loss incurred by subjects.

Some authors argue that the second model seems most

ethically acceptable (Dickert & Grady 1999); however, one

could question why this is so. Subjects are accepted as

potential volunteers for research if two criteria are met –

being of a certain health status (for example, a patient with

cancer; or a healthy person if controls are being sought) and

the ability to understand and interpret the research proposal

and its risks. In the context of Dickert and Grady’s (1999)

second model, the ‘wage payment model’, if such status or a

level of specific skill is required for participation, or partic-

ular preconditions for payment, is it not more ethical to pay

over and above a level paid for unskilled work?

In practice, many volunteer subjects receive no payment or

reimbursement for their participation in research. Such a

paradigm has pure altruism as its foundation. In this context,

it is the polar extreme of a spectrum of reimbursement –

inducement, at the opposite end of which sits major or

generous inducements which are offered in order to compete

in the ‘commercial marketplace’.

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The European Union (EU) has adopted an extensive

approach to this question (The European Parliament 2001).

As with many directives which are passed by the EU, there is

an imperative both to involve and cater for the plethora of

cultures, requirements and specific conditions of the 25

member nations. This has meant that any directives must, of

necessity, be very broad. Its directives about research ethics

could arguably be critiqued as being too wide for practical

use within nations. Such equivocation demonstrates that

rewarding or compensating both investigators and trial

subjects must be agreed upon between the sponsor of the

research and the research team at the site at which the

research is taking place. This has the potential to lead to

multi-site variability without making any real commitment

to enforcing positive ethical issues surrounding inducements

for research participation. Nurses are an essential part of all

such teams.

In the USA, there exists a profusion of guidelines, laws and

regulations about the use of incentives for participation in

research (Sears 2001, Rice & Broome 2004). As in all

countries, consensus on such an issue would be a good thing,

but has proved to be difficult to reach because of the

multiplicity of factors which affect different cultures, age

groups and vulnerable populations. Australia, too, has had

difficulty reaching a common directive. The National Health

and Medical Research Council of Australia (1999) has

produced guidelines for the ethical conduct of research.

Adherence to these is required before researchers can be

funded from government sources; but again, the directives on

recommendations relating to inducements remain general.

Nurses undertaking research or those who are involved as

professional team clinicians must read directives and avail-

able literature to remain knowledgeable about research

ethics. We feel that they need to make a balanced judgement

about when inducements may or may not be used ethically.

Only by examining the ethical themes governing such issues

can they hope to remain informed; and, by extension, can

their patients remain protected.

Altruism

Many research teams offer inducements, sometimes large

inducements exceeding thousands of pounds, as recruiting

stratagems. The fundamental question is whether health

research sits in the domain of altruism, or that of commerce.

If one takes such a binary, indeed polar, approach, the issues

are somewhat simpler. Some view any medical research as a

domain of altruism which binds both volunteer subjects and

those researchers and clinicians who are engaged in the

clinical care of such subjects. Others view any suggestion of

selling one’s body for research as an unhealthy negation or

belittlement of this altruism.

In the related but distinct field of organ donation for

transplantation, a similar polar difference of opinion exists.

Some see the selling of body organs – for the material benefit

of an impoverished donor and for the clinical benefit of the

recipient – as entirely ethical; whereas others do not (Nowak

2006). Some see any attempt to control this as denying

individuals, who are induced to sell body organs, or to

partake in medical research, the autonomy which all now

regard as one of the basic tenets of contemporary best-

practice bioethics.

When one speaks of inducements, we are not speaking of

reasonable recompense for expenses incurred in being a

volunteer research subject. Rather, we regard inducements as

anything which exceeds that which is ‘resource neutral’ with

respect to legitimate expenses incurred by potential volunteer

research subjects, and in the case of children, that of their

families as well. Reimbursement, recompense or inducements

may of course be cash, gifts or non-physical rewards. An

example of this latter might be the partial remission of a

prisoner’s sentence.

The health professions generally, and nursing specifically,

are built on a platform of altruism. Despite any salary or

payment for service, there is a fundamental ethos of the

primacy of alleviating suffering, of promoting dignity and the

fulfilment of palliative care; of the prevention of disease and

injury, and of curing disease. These things are perhaps best

embodied in the generic term, caritas. In the research context,

there is the added theme of scientific integrity, itself including

the ingredients of scientific honesty, objectivity and the

implementation of technical ‘best-practice’. The inappropri-

ate use of inducements has, we believe, the potential to

degrade the ethos of combined caritas and scientific integrity,

which doublet is fundamental to the contemporary profession

of nursing. We agree that:

societal trust in research [must] not [be] eroded, [and that] subjects

[being] enrolled in trials do not become merely a means to an end,

and medical research is sufficiently translated into clinical advances

that will benefit future patients. (Morin et al. 2002, p. 78)

Captive subjects

Most feel that inducements are inappropriate if approaches to

a ‘volunteer’ occur in the context of any modification of true

free choice of the potential research participant. A basic tenet

of autonomy established explicitly in the Nuremburg Code

(1946–1949), gives ‘free and informed consent’ as one of the

basic inviolate precepts of medical research (Annas & Grodin

L Shields and J Pearn

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1992). Nevertheless, many members of society and many

‘legitimate’ potential subjects for research cannot truly give

consent which is ‘free and informed’, because of their specific

vulnerability to influences beyond their control. People

exposed to such vulnerability are sometimes referred to by

ethicists as ‘captive subjects’. The term applies to fœtuses,

children, the mentally ill, prisoners, members of the armed

services, the intellectually disabled, the aged and the dead.

Three particularly vulnerable groups of ‘captive subjects’ are

(i) those who are members of institutions such as the armed

forces, or prisons; (ii) family members of the researchers

themselves; and (iii) those who are financially impoverished.

The degree of ‘ethical captivity’ is usually relative and

variable in several of these groups. Such applies particularly

to children where there is an increasing ability as the child

grows into adolescence and adult life, to interpret risk and

gain a sense of the independence and (hopefully) the

inviolability of their own body. The same applies to questions

of personal resources and wealth which obviously exist in

spectrum form along any concept of a sliding scale. This, in

turn, is modified by the wealth of one’s peers, or the general

wealth of the society or community in which such an

individual lives. This relativity of independence is currently

topical in ethical and societal debate about the sale of body

organs by members of otherwise impoverished societies to

potential donors for whom the cost may be relatively trivial.

From the point of view of the donor, such a sale (for example

a kidney) may lift the individual and his or her family from

lifelong penury into one where a better quality of life is

available for all. This issue remains controversial.

In the context of inducements for medical research, where

approaches are made to impecunious potential volunteers,

there is always a risk that the independence of such

individuals may be compromised. At one extreme, we have

experience of students who have felt that they were unable to

complete their university studies without extra money.

Although they may not otherwise have been interested or

bothered to volunteer to participate in a drug trial which may

involve being injected with a drug and subjected to serial

procedures over a weekend, they may do so for a modest

inducement of (say) £300 (or, say US$500). At the other

extreme, it is said, if the inducements are high enough, then

like a number of other issues and choices that confront any of

us as individuals, there is a point at which ‘everyone may

have their price’.

The nursing role here is to be aware that inducements may

render a potential research subject ‘captive’ in the ethical

sense; and that a nurse’s participation in the research

(albeit as a professional carer and not as an author or

‘acknowledged’ member of the specific research team itself),

inescapably involves them in what may be regarded as

unethical practice.

Legal issues

When a potential volunteer – for example, patient or normal

control – is considering participating in a research project, he

or she takes into account the risks of injury or death, the

nature of such injuries and their consequences, and the

potential advantages of participation. These latter may

include a belief, held rightly or wrongly, that they will

benefit personally from such participation either in monetary

terms or in the belief of a greater likelihood of cure. This

latter hope is commonly experienced, even when researchers

stress that there is little statistical probability of cure or even

of therapeutic benefit. This is sometimes called the ‘thera-

peutic misconception’ (Daugherty et al. 1995). Another

benefit is the subjective feeling of altruism that research

volunteers may, and often do, experience.

In the clinical management of patients outside the research

domain, at least in the UK and Australia, it is illegal to give a

patient an unreasonable inducement to participate in

a procedure through painting an unrealistic expectation

of a positive or beneficial outcome (Nisselle 1999). Whether

in primary clinical or in a specific research relationship, the

minimum legal obligation of clinical nurses is to be aware of

the risks inherent in any treatment, intervention or procedure

that they may be administering or monitoring; and if they

discover, often serendipitously or informally, that patients do

not understand the relevant risks, to bring this to the notice

of the researchers with whom the nurses are enjoined.

Conclusion

We feel that it is important that nurses involved either

clinically or in a co-participatory research role should be

aware of four issues relevant to the subject of inducements –

(i) capitation fees offered to the staff to recruit individuals; (ii)

the size of inducements that might be offered to research

subjects, whether patients or controls; (iii) the need to

monitor the explicit statements of risks, discomfort and

inconvenience which are explained to potential research

subjects prior to their final volunteering; and (iv) that nurses

have an understanding of whether or not individuals with

whom they are involved in professional care are in any way

ethically captive if inducements have been offered and

accepted.

We feel that there is nothing unethical about the general

use of modest inducements to individuals who can make free

and informed consent. Such, however, reduces altruism,

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� 2007 The Authors. Journal compilation � 2007 Blackwell Publishing Ltd 1199

which traditionally has been an underlying ethos of human

biomedical research. The question of what constitutes a

‘modest’ inducement is difficult and is not only culture-

specific but is relative to the degree of ethical captivity of the

potential volunteer.

If significant inducements are offered to research subjects,

and if subjects are truly ‘free and informed’ in the ethical

sense, there will inevitably be a reduction in the intangible

but important component of altruism in such research. We do

not go so far as to say that inducements should not be offered

simply because altruism is inevitably compromised. We feel,

however, that nurses participating either in clinical care or

directly in the research itself should be aware that such loss is

a price to be paid if excessive inducements are offered and

accepted for recruitment and continued participation.

Acknowledgment

We thank Ms Jan Pratt, Royal Children’s Hospital Health

Service District, Brisbane, for her suggestions.

Contributions

Study design: LS, JP; data analysis: LS, JP and manuscript

preparation: LS, JP.

References

Annas GJ & Grodin MA (1992) The Nazi Doctors and the

Nuremberg Code: Human Rights in Human Experimentation.

Oxford University Press, New York.

Bhattacharya S & Coghlan A (2006) The first human trials of a new

drug left six men fighting for their lives in the UK – what could

have caused such a catastrophic reaction? New Scientist 2544,

10–11.

Central Office for Research Ethics Committees (2005) Welcome.

Available at: http://www.corec.org.uk/recs/index.htm (accessed 4

June 2006).

Cook KA, Wiles R & Hopkins E (1998) The English patients: human

experiments and pesticide policy. Environmental Working Group,

Washington. Available at: http://www.ewg.org/reports_content/

english/English.pdf (accessed 9 February 2007).

Daugherty C, Ratain MJ, Grochowski E, Stocking C, Kodish E,

Mick R & Siegler M (1995) Perceptions of cancer patients and

their physicians involved in Phase 1 Clinical Trials. Journal of

Clinical Oncology 13, 1062–1072.

Dickert N & Grady C (1999) What’s the price of a research subject?

Approaches to payment for research participation. New England

Journal of Medicine 341, 198–203.

Lemmens T & Elliott C (2001) Justice for the professional guinea pig.

American Journal of Bioethics 1, 51–53.

Morin K, Rakatansky H, Riddick FA, Morse LJ, O’Bannon JM,

Goldrich MS, Ray P, Weiss M, Sade RM & Spillmand MA (2002)

Managing conflicts of interest in the conduct of clinical trials.

Journal of the American Medical Association 287, 78–84.

National Health and Medical Research Council of Australia (1999)

National Statement on Ethical Conduct in Research Involving

Humans. Canberra. Available at: http://www.nhmrc.gov.au/

publications/_files/e35.pdf (accessed 4 June 2006).

Nisselle P (1999) Competition law and the medical profession.

Modern Medicine Australia 42, 119–121.

Nowak R (2006) Not brain-dead, but right for transplant.

New Scientist 191, 6–7.

Rice R & Broome ME (2004) Incentives for children in research.

Journal of Nursing Scholarship 36, 167–172.

Sears JM (2001) The payment of research subjects: ethical concerns.

Oncology Nurses’ Forum 28, 657–663.

The European Parliament (2001) Directive 2001/20/Ec of the Euro-

pean Parliament and of the Council of 4 April 2001 on the

Approximation of the Laws, Regulations and Administrative

Provisions of the Member States Relating to the Implementation

of Good Clinical Practice in the Conduct of Clinical Trials on

Medicinal Products for Human Use. Brussels. 2001. Available at:

http://europa.eu.int/eur-lex/pri/en/oj/dat/2001/l_121/l_12120010501

en00340044.pdf (accessed 4 June 2006).

L Shields and J Pearn

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