Environmental tobacco smoke and tobacco related mortality in a prospective study of Californians, 1960-98

BMJ 2003; 326 doi: (Published 15 May 2003) Cite this as: BMJ 2003;326:1057

The Case of the Footnote Wagging the Article

The Case of the Footnote Wagging the Article

A Footnote with Legs

James E. Enstrom and Geoffrey C. Kabat’s recent paper in the British
Medical Journal, “Environmental tobacco smoke and tobacco related
mortality in a prospective study of Californians, 1960-98 (1),” has
generated much discussion and debate, in the United States and around the
world (2, 3). These authors’ assertion that “The association between
exposure to environmental tobacco smoke and coronary heart disease and
lung cancer may be considerably weaker than generally believed” has led a
broad spectrum of tobacco researchers, scientific societies and voluntary
health groups to challenge the authors’ findings (4), question their
methodology (4), refuse to publish earlier attempts (5), question the
viability of their data set (6), criticize the authors’ ties to the
tobacco industry (7, 8), and voice concern for the British Medical
Journal’s review policies and practices (9). In the midst of this
controversy, another debate has arisen about a footnote in which Enstrom
and Kabat acknowledged funding for their research:

“Funding: The American Cancer Society initiated CPS I in 1959,
conducted follow up until 1972, and has maintained the original database.
Extended follow up until 1997 was conducted at the University of
California at Los Angeles with initial support from the Tobacco-Related
Disease Research Program, a University of California research organization
funded by the Proposition 99 cigarette surtax
( After continuing support from the Tobacco-
Related Disease Research Program was denied, follow up through 1999 and
data analysis were conducted at University of California at Los Angeles
with support from the Center for Indoor Air Research, a 1988-99 research
organization that received funding primarily from US tobacco companies.
In recent years JEE has received funds originating from the tobacco
industry for his tobacco related epidemiological research because it has
been impossible for him to obtain equivalent funds from other sources”

This footnote has taken on a life of its own. In what may be a first
for a medical journal footnote, it was picked up by newspapers and wire
services around the world, including the London Times, the Irish
Independent, the Melbourne Australia Nationwide News Service, the Hindu,
and the Jerusalem Post. Some reports inferred from the footnote that the
Tobacco-Related Disease Research Program’s (TRDRP) action forced Dr.
Enstrom, “in recent years” to consort with the tobacco industry (3).
Jaffe et al., in a letter to the editor of the Jerusalem Post, wondered:
“Could it be that Enstrom’s non-tobacco funding sources dried up because
of the questionable validity of the research?” (10). Dr. Enstrom’s
statement that TRDRP denied him continuing funding is accurate as far as
it goes but omits the key fact that it was not funded because it had
inadequate scientific merit as determined by peer review. As a result,
many readers read more into this action than is warranted. It is
particularly important to TRDRP that the record be corrected because some
publicly reported interpretations are inconsistent with the facts and
impugned the program’s motives in not funding the proposal.

In Northern California, the Sacramento Bee and San Francisco
Chronicle both reported that TRDRP denied or dropped funding for Dr.
Enstrom’s research, striking the same tone as the Jerusalem Post letter
(11, 12). Sabin Russell, the Chronicle medical writer said:

“Enstrom vigorously defends his work, noting that it began with the
approval of the American Cancer Society and $250,000 in funding from
California's Tobacco Related Disease Research Program, which is paid for
by the state's cigarette tax. But the state dropped its support of
Enstrom in 1998, and the American Cancer Society withdrew its
collaboration after questioning the scientific value of his approach”

Intended or not, the implication is clear that TRDRP discontinued
funding because the conclusions Dr. Enstrom drew from his previously-
funded TRDRP research did not support the prevailing medical and public
health belief that exposure to environmental tobacco smoke is a serious
health risk. This implication could not be further from the truth,
however, as explained below.

Newspaper columnists are not the only ones who were led to an
incorrect conclusion by the authors’ choice of words. The American Cancer
Society’s press release about the article, “Study Inaccurately Uses ACS
Data to Suggest No Link Between Secondhand Smoke & Lung Cancer,”
included a similar take on the footnote:

“The study was performed by Dr. James Enstrom at UCLA, and was funded
originally by California Proposition 99 cigarette tax. When continued
support from that agency was denied, the researcher sought and received
significant funding from the tobacco industry's Center for Indoor Air
Research” (6).

Even at the British Medical Journal’s on-line Rapid Responses to the
Enstrom and Kabat article, commentators have raised questions about
TRDRP’s motives:

“Why was the grant from the Tobacco-Related Disease Research Program
terminated? Was it because the finding of no excess tobacco related
diseases in non smoking spouses was accepted, and hence further support
would be superfluous? Or was it because these findings were contrary to
the dogma of the anti-smoking lobby?” (13).

When these news articles and electronic postings appeared, TRDRP
received numerous written and telephone inquiries regarding this footnote.
The question that all asked was: Did the Tobacco Related Disease Research
Program deny continuing funding to Dr. Enstrom because their findings did
not strongly implicate environmental tobacco smoke in the etiology of lung
cancer and coronary heart disease?

In order to provide an accurate interpretation of Drs. Enstrom and
Kabat’s footnote and TRDRP’s funding practices, the facts surrounding the
ending of this project’s funding are reviewed below. Additionally, the
TRDRP funding process, the position of the University of California on
funding investigators with ties to the tobacco industry, and Enstrom’s
claim that he only became affiliated with the tobacco industry in recent
years because research funds were not available from other sources, will
be discussed.

The Facts

In 1991 TRDRP awarded Dr. Enstrom a three-year grant for a research
project titled “Tobacco-Related Disease Trends among 118,000
Californians.” When that grant was about to end in 1994, Dr. Enstrom
applied for a continuation grant – this is the proposal referred to in
Enstrom’s and Kabat’s footnote. In short, the proposal was not funded
because it had inadequate scientific merit and TRDRP had insufficient
funds. To gain a clear understanding of how this decision was made, it is
necessary to know TRDRP’s procedure for evaluating research proposals is
modeled on the open competition and peer review process used by the
National Institutes of Health. Proposals for continuing projects compete
with proposals for new projects; both are evaluated for scientific merit
by peer reviewers, scientists with expertise in the areas of proposed
research who have no conflicts of interest with the applicants. TRDRP’s
Scientific Advisory Committee did not recommend Dr. Enstrom’s proposal for
funding because peer reviewers did not assign it a sufficiently high score
for scientific merit given the very limited funds available. Very little
money was available for new grants in 1994 because the state government
tried to divert approximately 85% of TRDRP funds to meet other state needs
during a recessionary period.

It should be clear that TRDRP did not cancel a Dr. Enstrom’s ongoing
project midstream; Dr. Enstrom received full funding for a three-year
project in 1991. Nor did TRDRP deny continuing funding because of a
judgment about the “political correctness” of the results Dr. Enstrom
reported from his first project. TRDRP did not fund the continuation
proposal because it was judged by peer reviewers not to be among the very
best proposals that year.

It must be noted that, as a rule, TRDRP treats unfunded applications
as confidential. In fact, the program does not even reveal whether an
application was submitted, much less the outcome of the peer review and
funding process. However, since Dr. Enstrom reported in print that he
submitted an application that was denied funding, we are not violating a
confidence by clarifying the history.

TRDRP History: Policies and Procedures Concerning Grant Reviews

In TRDRP’s 12 annual grant funding cycles, it has awarded 1,020
grants totaling $325,530,000 to investigators at 81 California
institutions (15). Each application is rigorously evaluated by a peer
review panel of scientific experts for the significance of the research
plan, the soundness of the scientific approach, and the feasibility of
accomplishing the aims. Reviewers also assess the qualifications of the
investigators to conduct the proposed research and the adequacy of the
resources and environment in which the research would be conducted. For
competing continuation proposals such as Dr. Enstrom’s, they also judge
the progress achieved during the previous grant.

The footnote that describes TRDRP’s decision not to fund Dr.
Enstrom’s competing continuation proposal (“After continuing support from
the Tobacco-Related Disease Research Program was denied,…”) had the effect
of questioning the integrity of TRDRP’s procedures. While the authors may
not have intended to convey a derogatory message, many readers nonetheless
took their footnote to mean that TRDRP had refused to continue funding Dr.
Enstrom’s research because his results did not support the conclusion that
exposure to secondhand smoke causes disease. This interpretation led one
person who called the TRDRP office to state: “Isn’t it the policy of the
TRDRP to deny funding to investigators that have accepted money from the
tobacco industry?”

TRDRP’s Policy on Funding Investigators Who Have Received Funding
from the Tobacco Industry

TRDRP never has had and does not now have a policy excluding
researchers from receiving funding who have received funding from the
tobacco industry. However, TRDRP has been an active participant in the
nationwide debate, along with other tobacco research funders, on the role
of the tobacco industry in tobacco-use research. Earlier this year, the
TRDRP co-sponsored a national conference on “Tobacco Funding and
Scientific Research,” with the American Legacy Foundation and the National
Cancer Institute in New Orleans following the annual meeting of the
Society for Research in Nicotine and Tobacco (17). It should be noted
that representatives of the tobacco industry attended this conference. A
goal of TRDRP is to inform investigators of the potential pitfalls of
accepting funding from the tobacco industry because many are unaware of
the implications of this choice.

TRDRP’s interest in this topic arose with the creation in 2000 of the
Philip Morris External Research Program (PMERP). A statewide oversight
body, the Tobacco Education and Research Oversight Committee (TEROC),
recommended that the University of California Regents “take formal action
to establish a strong and unequivocal policy prohibiting University of
California faculty from accepting financial support from the Philip Morris
External Research Program.” (18) In response to TEROC’s concern, the
University of California responded:

“We believe that the comprehensive policies the University already
has in place, which address research funding from private entities, are
appropriate and adequate. The University’s policies are intended to
achieve two broad goals. They protect researchers’ academic freedom to
investigate issues they believe are important, independently of political,
cultural, commercial, or other sources of influence. They also protect
the University, the State, and the public by maintaining the highest
scholarly standards, administering funds prudently, and controlling
potential conflicts of interest. The University’s policies ensure that
funders cannot censor or otherwise control the nature or outcomes of the
research.” (19)

In short, the University of California’s value on academic freedom
precludes TRDRP from denying funding to individuals or organizations
because they receive funding from others, regardless of their social,
political or economic views or interests. Any implication from Drs.
Enstrom’s and Kabat’s footnote that their affiliation with the tobacco
industry had something to do with TRDRP’s decision not to renew funding of
Dr. Enstrom’s research project is seriously off the mark.

Forced Into the Arms of the Tobacco Industry?

It is unfortunate that Drs. Enstrom and Kabat described TRDRP’s
decision not to award a competing continuation grant to Dr. Enstrom in
such a way as to mislead readers about TRDRP’s motivation. Of equal
concern is the implication that TRDRP’s action forced Dr. Enstrom to seek
funding from the tobacco industry. “In recent years JEE has received
funds originating from the tobacco industry for his tobacco related
epidemiological research because it has been impossible for him to obtain
equivalent funds from other sources” (1). This statement by the authors
serves to cloud the issue rather than clarify. The take-home message that
they would like readers to have is that after TRDRP “denied” Dr. Enstrom
further funding, he turned to the tobacco industry, because it was (is)
impossible to obtain equivalent funds. But history tells a different

In 1975, Dr. Enstrom solicited funds for his research, “Mortality
Among Mormons,” from the tobacco industry’s Council for Tobacco Research
(CTR) (20). In 1976, Dr. Enstrom approached the Tobacco Institute to help
him secure funds from the CTR (21). Again, in 1978, Dr. Enstrom requested
funds again from the CTR, this time for another study titled “Smoking
Cessation and Mortality Trends Among California Physicians” (22). By
1992, one of Dr. Enstrom’s research proposals was funded by the CTR,
“Mortality trends among smokers and non-smokers” (23). In a 1996 letter
to Max Eisenberg, Director of the Center for Indoor Air Research (CIAR),
Dr. Enstrom touted his ties to the tobacco industry by stating: “For the
past three years I have done consulting and research on passive smoking
for Jeffrey L. Furr of Womble Carlyle on behalf of R.J. Reynolds and
Philip Morris” (24). As Martin McKee points out, “Womble Carlyle Sandridge
& Rice is a law firm based in Winston-Salem, North Carolina, that was
extensively involved on behalf of the tobacco industry in litigation in
respect of the hazards of exposure to tobacco smoke indoors and Dr Enstrom
had written reports on this topic for RJ Reynolds’ legal department” (25).
Indeed, prior to the receipt of CIAR funding, Dr. Enstrom received
$150,000 grant in 1997 directly from Philip Morris for a research project
titled, “The relationship of low levels of active smoking to mortality”
(26). Hence, Drs. Enstrom and Kabat were not forced into the arms of the
tobacco industry, as their footnote implies; rather the historical record
shows that Dr Enstrom already had a long-established relationship with the
Council for Tobacco Research, the Tobacco Institute, Philip Morris, Inc.,
and R.J. Reynolds.

It should be noted that Dr. Enstrom roundly criticized the 1992 EPA
report on second hand smoke as “flawed science” (27), and while his
conclusions were and are disputed by many in the scientific community, his
association with the tobacco industry did not affect his 1991 TRDRP grant
submission from being reviewed and funded (28). Hence, Enstrom’s receipt
of TRDRP funding belies the statement “it has been impossible for him to
obtain equivalent funds from other sources.”

Phillip S. Gardiner, Dr. P.H.

Charles L. Gruder, Ph.D.

Francisco O. Buchting, Ph.D.

Dr. Gardiner is the Social and Behavioral Sciences Research
Administrator for the Tobacco Related Disease Research Program

Dr. Gruder, is the Acting Director of the Tobacco Related Disease
Research Program.

Dr. Francisco Buchting is the Epidemiology, Economic, and Policy
Research Administrator for the Tobacco Related Disease Research Program

Dr. Gruder is Acting Director and Drs. Gardiner and Buchting are
Research Administrators with the Tobacco-Related Disease Research Program.


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related mortality in a prospective study of Californians, 1960-98. BMJ
2003; 326:1057-61.

2. British Medical Journal. Rapid Responses to Enstrom and Kabat.

3. LexisNexis.

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9. Shatenstein S. BMJ Study & Editorial Undermining the Case
Against SHS Risk. GLOBALink News & Information, May 15, 2003;

10. Jaffe MJ, Wurtman E, Zauer W, Dombey K, Tor D, Alcabes N.
Letters to the Editor, Jerusalem Post, May 30th 2003.

11. Lau E. UCLA smoking study criticized. Sacramento Bee, Friday
May 16, 2003;

12. Russell S. Study disputes fears about second hand smoke / but
critics say data is dated. San Francisco Chronicle, May 16, 2003;

13. Hall GH. Pots calling kettles black. Letter to the Editor, BMJ,
Rapid Responses, May 19, 2003;

14. Gruder L. Re: James E. Enstrom, Ph.D., 5RT-0207, Tobacco-Related
Disease Trends Among 118,000 Californians. Tobacco Related Disease
Research Program (TRDRP), Correspondence, July 5, 1994.

15. TRDRP. Annual Report. Tobacco Related Disease Research Program,
January, 2003 (figures in text include 12th cycle grants).

16. TRDRP. Compendium of Awards. Tobacco Related Disease Research
Program, July 2002.

17. American Legacy Foundation, California Tobacco Related Disease
Research Program, National Cancer Institute. Tobacco Funding &
Scientific Research: Workshop, Ethical, Legal and Policy Issues, February
22-23, 2003, New Orleans

18. Cook J. Letter from the Chairperson of the Tobacco Education and
Research Oversight Committee to S. S. Johnson, Chairman of the University
of California Board of Regents, September 22, 2000.

19. Atkinson R. Letter from the President of the University of
California to J. Cook, Chairperson of the Tobacco Education and Research
Oversight Committee, November 1, 2000.

20. Breslow L, Rogers HT. Cancer Mortality Among Mormons.
Application for grant funding to Council for Tobacco Research, December
23, 1975. Bates #: 2232059-2066

21. Enstrom JE. “Discusses Research of Cancer Mortality Among
Mormons and Smoking and Health in General.” Letter to Anne E. Duffin,
Vice President, Tobacco Institute, January 5, 1976; Bates# 2232075;

22. Enstrom JE. Letter to Robert C. Hackett, Ph.D., Director of
Research, Council for Tobacco Research, February 13, 1978.

23. Ctr, Council for Tobacco Research. Report of the Council for
Tobacco Research U.S.A. Inc. 930000. Page 224, James E. Enstrom,
Associate Researcher, University of California Los Angeles: Mortality
trends among smokers and non-smokers, 1993. Bates #: 2022882366-2637.

24. Enstrom JE. Proposed research on passive smoking. Letter to Max
Eisenberg, Ph.D., Director Center for Indoor Air Research, July 15, 1996.
Bates Number: 2063610840.

25. McKee M. More Details on competing concerns. Letter to the
Editor, BMJ, Rapid Responses, May 20, 2003;

26. Carchman RA. Principal Investigator: James E. Enstrom, Ph.D.,
M.P.H. Grant Title: “The relationship of low levels of active smoking to
mortality.” Bates # : 2063610867

27. Smokers Advocate. Media Report Casts Doubt Over EPA Report on
Tobacco Smoke Is EPA Blowing It’s Own Smoke? Smokers Advocate, National
Edition, April 1993. Bates #: 2044178484-8486.

28. TRDRP. Compendium of Awards. Tobacco Related Disease Research
Program, July 1991. (TRDRP Archives).

Competing interests:  
None declared

Competing interests: No competing interests

19 August 2003
Phillip S. Gardiner
Research Administrator
Charles L. Gruder, Francisco Buchting
University of California Office of the President, Tobacco Related Disease Research Program
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