The New England Journal of Medicine -- October 2, 1997 -- Volume 337,

Number 14

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SOUNDING BOARD

Ethical Complexities of Conducting Research in Developing Countries

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One of the great challenges in medical research is to conduct

clinical trials in developing countries that will lead to

therapies that benefit the citizens of these countries. Features

of many developing countries -- poverty, endemic diseases, and a

low level of investment in health care systems -- affect both the

ease of performing trials and the selection of trials that can

benefit the populations of the countries. Trials that make use of

impoverished populations to test drugs for use solely in

developed countries violate our most basic understanding of

ethical behavior. Trials that apply scientific knowledge to

interventions that can be used to benefit such populations are

appropriate but present their own ethical challenges. How do we

balance the ethical premises on which our work is based with the

calls for public health partnerships from our colleagues in

developing countries?

Some commentators have been critical of research performed in

developing countries that might not be found ethically acceptable

in developed countries. Specifically, questions have been raised

about trials of interventions to prevent maternal-infant

transmission of the human immunodeficiency virus (HIV) that have

been sponsored by the National Institutes of Health (NIH) and the

Centers for Disease Control and Prevention (CDC). (1,2) Although

these commentators raise important issues, they have not

adequately considered the purpose and complexity of such trials

and the needs of the countries involved. They also allude

inappropriately to the infamous Tuskegee study, which did not

test an intervention. The Tuskegee study ultimately deprived

people of a known, effective, affordable intervention. To claim

that countries seeking help in stemming the tide of

maternal-infant HIV transmission by seeking usable interventions

have followed that path trivializes the suffering of the men in

the Tuskegee study and shows a serious lack of understanding of

today's trials.

After the Tuskegee study was made public, in the 1970s, a

national commission was established to develop principles and

guidelines for the protection of research subjects. The new

system of protection was described in the Belmont report. (3)

Although largely compatible with the World Medical Association's

Declaration of Helsinki, (4) the Belmont report articulated three

principles: respect for persons (the recognition of the right of

persons to exercise autonomy), beneficence (the minimization of

risk incurred by research subjects and the maximization of

benefits to them and to others), and justice (the principle that

therapeutic investigations should not unduly involve persons from

groups unlikely to benefit from subsequent applications of the

research).

There is an inherent tension among these three principles. Over

the years, we have seen the focus of debate shift from concern

about the burdens of participation in research (beneficence) to

equitable access to clinical trials (justice). Furthermore, the

right to exercise autonomy was not always fully available to

women, who were excluded from participating in clinical trials

perceived as jeopardizing their safety; their exclusion clearly

limited their ability to benefit from the research. Similarly,

persons in developing countries deserve research that addresses

their needs.

How should these principles be applied to research conducted in

developing countries? How can we -- and they -- weigh the

benefits and risks? Such research must be developed in concert

with the developing countries in which it will be conducted. In

the case of the NIH and CDC trials, there has been strong and

consistent support and involvement of the scientific and public

health communities in the host countries, with local as well as

United States-based scientific and ethical reviews and the same

requirements for informed consent that would exist if the work

were performed in the United States. But there is more to this

partnership. Interventions that could be expected to be made

available in the United States might be well beyond the financial

resources of a developing country or exceed the capacity of its

health care infrastructure. Might we support a trial in another

country that would not be offered in the United States? Yes,

because the burden of disease might make such a study more

compelling in that country. Even if there were some risks

associated with intervention, such a trial might pass the test of

beneficence. Might we elect not to support a trial of an

intervention that was beyond the reach of the citizens of the

other country? Yes, because that trial would not pass the test of

justice.

Trials supported by the NIH and the CDC, which are designed to

reduce the transmission of HIV from mothers to infants in

developing countries, have been held up by some observers as

examples of trials that do not meet ethical standards. We

disagree. The debate does not hinge on informed consent, which

all the trials have obtained. It hinges instead on whether it is

ethical to test interventions against a placebo control when an

effective intervention is in use elsewhere in the world. A

background paper sets forth our views on this matter more fully.

(5) The paper is also available on the World Wide Web (at

http://www.nih.gov/news/mathiv/mathiv.htm).

One such effective intervention -- known as AIDS Clinical Trials

Group protocol 076 -- was a major breakthrough in the search for

a way to interrupt the transmission of HIV from mother to infant.

The regimen tested in the original study, however, was quite

intensive for pregnant women and the health care system. Although

this regimen has been proved effective, it requires that women

undergo HIV testing and receive counseling about their HIV status

early in pregnancy, comply with a lengthy oral regimen and with

intravenous administration of the relatively expensive

antiretroviral drug zidovudine, and refrain from breast-feeding.

In addition, the newborn infants must receive six weeks of oral

zidovudine, and both mothers and infants must be carefully

monitored for adverse effects of the drug. Unfortunately, the

burden of maternal-infant transmission of HIV is greatest in

countries where women present late for prenatal care, have

limited access to HIV testing and counseling, typically deliver

their infants in settings not conducive to intravenous drug

administration, and depend on breast-feeding to protect their

babies from many diseases, only one of which is HIV infection.

Furthermore, zidovudine is a powerful drug, and its safety in the

populations of developing countries, where the incidences of

other diseases, anemia, and malnutrition are higher than in

developed countries, is unknown. Therefore, even though the 076

protocol has been shown to be effective in some countries, it is

unlikely that it can be successfully exported to many others.

In addition to these hurdles, the wholesale cost of zidovudine in

the 076 protocol is estimated to be in excess of $800 per mother

and infant, an amount far greater than most developing countries

can afford to pay for standard care. For example, in Malawi, the

cost of zidovudine alone for the 076 regimen for one HIV-infected

woman and her child is more than 600 times the annual per capita

allocation for health care.

Various representatives of the ministries of health, communities,

and scientists in developing countries have joined with other

scientists to call for less complex and less expensive

interventions to counteract the staggering impact of

maternal-infant transmission of HIV in the developing world. The

World Health Organization moved promptly after the release of the

results of the 076 protocol, convening a panel of researchers and

public health practitioners from around the world. This panel

recommended the use of the 076 regimen throughout the

industrialized world, where it is feasible, but also called for

studies of alternative regimens that could be used in developing

countries, observing that the logistical issues and costs

precluded the widespread application of the 076 regimen. (6) To

this end, the World Health Organization asked UNAIDS, the Joint

United Nations Programme on HIV/AIDS, to coordinate international

research efforts to develop simpler, less costly interventions.

The scientific community is responding by carrying out trials of

several promising regimens that developing countries recognize as

candidates for widespread delivery. However, these trials are

being criticized by some people because of the use of placebo

controls. Why not test these new interventions against the 076

regimen? Why not test them against other interventions that might

offer some benefit? These questions were carefully considered in

the development of these research projects and in their

scientific and ethical review.

An obvious response to the ethical objection to

placebo-controlled trials in countries where there is no current

intervention is that the assignment to a placebo group does not

carry a risk beyond that associated with standard practice, but

this response is too simple. An additional response is that a

placebo-controlled study usually provides a faster answer with

fewer subjects, but the same result might be achieved with more

sites or more aggressive enrollment. The most compelling reason

to use a placebo-controlled study is that it provides definitive

answers to questions about the safety and value of an

intervention in the setting in which the study is performed, and

these answers are the point of the research. Without clear and

firm answers to whether and, if so, how well an intervention

works, it is impossible for a country to make a sound judgment

about the appropriateness and financial feasibility of providing

the intervention.

For example, testing two or more interventions of unknown benefit

(as some people have suggested) will not necessarily reveal

whether either is better than nothing. Even if one surpasses the

other, it may be difficult to judge the extent of the benefit

conferred, since the interventions may differ markedly in other

ways -- for example, cost or toxicity. A placebo-controlled study

would supply that answer. Similarly, comparing an intervention of

unknown benefit -- especially one that is affordable in a

developing country -- with the only intervention with a known

benefit (the 076 regimen) may provide information that is not

useful for patients. If the affordable intervention is less

effective than the 076 regimen -- not an unlikely outcome -- this

information will be of little use in a country where the more

effective regimen is unavailable. Equally important, it will

still be unclear whether the affordable intervention is better

than nothing and worth the investment of scarce health care

dollars. Such studies would fail to meet the goal of determining

whether a treatment that could be implemented is worth

implementing.

A placebo-controlled trial is not the only way to study a new

intervention, but as compared with other approaches, it offers

more definitive answers and a clearer view of side effects. This

is not a case of treating research subjects as a means to an end,

nor does it reflect "a callous disregard of their welfare." (2)

Instead, a placebo-controlled trial may be the only way to obtain

an answer that is ultimately useful to people in similar

circumstances. If we enroll subjects in a study that exposes them

to unknown risks and is designed in a way that is unlikely to

provide results that are useful to the subjects or others in the

population, we have failed the test of beneficence.

Finally, the NIH- and CDC-supported trials have undergone a

rigorous process of ethical review, including not only the

participation of the public health and scientific communities in

the developing countries where the trials are being performed but

also the application of the U.S. rules for the protection of

human research subjects by relevant institutional review boards

in the United States and in the developing countries. Support

from local governments has been obtained, and each active study

has been and will continue to be reviewed by an independent data

and safety monitoring board.

To restate our main points: these studies address an urgent need

in the countries in which they are being conducted and have been

developed with extensive in-country participation. The studies

are being conducted according to widely accepted principles and

guidelines in bioethics. And our decisions to support these

trials rest heavily on local support and approval. In a letter to

the NIH dated May 8, 1997, Edward K. Mbidde, chairman of the AIDS

Research Committee of the Uganda Cancer Institute, wrote:

These are Ugandan studies conducted by Ugandan investigators

on Ugandans. Due to lack of resources we have been sponsored

by organizations like yours. We are grateful that you have

been able to do so.... There is a mix up of issues here

which needs to be clarified. It is not NIH conducting the

studies in Uganda but Ugandans conducting their study on

their people for the good of their people.

The scientific and ethical issues concerning studies in

developing countries are complex. It is a healthy sign that we

are debating these issues so that we can continue to advance our

knowledge and our practice. However, it is essential that the

debate take place with a full understanding of the nature of the

science, the interventions in question, and the local factors

that impede or support research and its benefits.

Harold Varmus, M.D.

National Institutes of Health

Bethesda, MD 20892-0148

David Satcher, M.D., Ph.D.

Centers for Disease Control and Prevention

Atlanta, GA 30329-4018

Editor's note Letters on this subject will be published in a

subsequent issue of the Journal, along with the responses of Dr.

Angell and Drs. Lurie and Wolfe.

References

1. Lurie P, Wolfe SM. Unethical trials of interventions to reduce

perinatal transmission of the human immunodeficiency virus in

developing countries. N Engl J Med 1997;337:853-6.

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2. Angell M. The ethics of clinical research in the third world.

N Engl J Med 1997;337:847-9.

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3. National Commission for the Protection of Human Subjects of

Biomedical and Behavioral Research. Belmont report: ethical

principles and guidelines for the protection of human subjects of

research. Washington, D.C.: Government Printing Office, 1988.

(GPO 887-809.)

Return to: Text

4. World Medical Association Declaration of Helsinki. Adopted by

the 18th World Medical Assembly, Helsinki, 1964, as revised by

the 48th World Medical Assembly, Republic of South Africa, 1996.

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5. The conduct of clinical trials of maternal-infant transmission

of HIV supported by the United States Department of Health and

Human Services in developing countries. Washington, D.C.:

Department of Health and Human Services, July 1997.

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6. Recommendations from the meeting on mother-to-infant

transmission of HIV by use of antiretrovirals, Geneva, World

Health Organization, June 23-25, 1994.

 

Copyright © 1997 by the Massachusetts Medical Society