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Business Bias:
How Epidemiologic Studies May Underestimate or Fail to
Detect Increased Risks of Cancer and Other Diseases
VALERIO GENNARO, MD, LORENZO TOMATIS, MD
In spite of claiming primary prevention as their aim,
studies of potential occupational and environmental
health hazards that are funded either directly or
indirectly by industry are likely to have negative
results. The authors present three common scenarios in
which faulty design of epidemiologic studies skews
results, and list 15 study design flaws that lead to
results that are dangerously misleading with regard to
both the evaluation and the improvement of public health.
Key words: epidemiology; industry influence; study
design; public health.
INT J OCCUP ENVIRON HEALTH 2005; 11:356-359
Interests other than those concerned with the protection
of public health - in particular, personal ambition or
economic profit - can heavily affect biomedical research,(1)
and cancer rescarch in particular(2-5) There is ample
evidence that, in spite of claiming primary prevention
as their aim, occupational and environmental studies
that are directly or indirectly sponsored by
multinational corporations almost invariably lead to
negative results. In such studies the real risk of
disease in subjects exposed to harmful factors is often
underestimated.
One way this is done is by indicating a safe
environmental situations that very likely present risk.
For example, in petrochemical and refinery-based
epidemiologic studies conducted (or simply supported) by
corporations workers potentially exposed to about 50
substances classified as toxic, mutagenic and
carcinogenic (9) are regularly declared healthy (10-11).
There are several reasons to question these results.
Studying the scientific literature oriented to the
identification of the disease risks in strategically and
economically relevant activity sectors such as oil
refineries and petrochemicals, it is common to observe a
statistically significant reduction of the observed/expected
ratio of cases (dead or ill) among exposed workers (vs
unexposed). This may, of course, occur because there is
no exposure at all, but in other instances the real
cause of the negative results-that is, the absence of an
association between exposure and adverse health
effects-may reside in the epidemiologic study design.
We present three scenarios, examples of which have been
observed in recent studies, in which real risks of
disease are underestimated. In addition we put forth 15
points, some of which are borrowed from a nearly
25-year-old analysis, (12) that are both critical and
dangerously misleading with regard to both the
evaluation and the improvement of public health. As
reanalysis of specific data sets are not available, we
cannot, however, make any direct evaluation or
simulation of specific studies.
Scenario 1
If exposed and unexposed workers are not separated, the
automatic and obvious; consequence is a large
underestimatíon of the real magnitude of risk among the
exposed workers (misclassification error). This error
might be negligible (statistically, not ethically, of
course) only if and where the proportion of unexposed
workers is not relevant (in terms of size, Person-years,
etc.). Only the classification of the whole cohort in
the homogeneous subgroups of workers, therefore, will
permit an estimate of the real risk magnitude.(13)
Scenarío 2
A more serious misclassification bias occurs when
exposed diseased workers are classified as unexposed
controls. (14) This is often the case in studies of U.S.
refinery workers, among whom the most heavily exposed
workers are often "contract workers" who may work at a
refinery or refineries cleaning tanks or installing
insulation but who are not regular "employees" of the
refinery. This "problem" has been known to the American
Petroleum Institute (API) for more than 40 years. In
1958, the American Petroleum Institute (API) contracted
with Dr. Robert Kehoe to design "An Epidemiologic Study
of Cancer among Employees in the American Petroleum
Industry."14 In describing worker exposure
classification Kehoe noted:
It was quickly discovered as various índustrial
situations were studied also that job titles differed
greatly from company to company and indicated little if
any relationship to the degree and kind of hazard. Men
charged with the actual operation of the equipment, for
example in the petroleum industry, may have very little
or no contact with either petroleum or the various
refined products, but the samplers and maintenance
personnel may have frequent and heavy exposures. At the
same time, maintenance and labor classifications may
work in all parts of the refinery or, equally common, be
assigned for a significant period of time to a single
area. In reviewing the effect of technical changes in
the refining processes on the exposure factor, one is
immediately impressed by the fact that this is an
extraordinarily, fluid and dynamic industry. New
processes evolve constantly, and this has been
particularly true in recent years as companies moved
rapidly from 'batch' type of operations to essentially "assembly
line" procedures. With this evolution, the degree and
kind of contact change markedly. Maintenance problems
are reduced and even presently widely-spaced 'turn
arounds' are being substantially subcontracted by many
companies. (It must be admitted that, although this
development may diminish the exposure hazard for the
refinery worker, it may be concentrating and augmenting
the danger to the employees of companies specializing in
this service type operation.)
Consequently, even if accurate and reliable occupational
records were obtainable, the local situations are
constantly changing and improving so that the exposures
of today are much less than those ten years past, and it
can be predicted confidently that they are probably much
greater than those of ten years hence.
Unfortunately, instead of trying to correct this problem,
API-funded researchers have capitalized on this
phenomenon to generate study findings that appear to
show that workers potentially exposed to all kinds of
known carcinogens and other toxins live longer than
unexposed population controls. This is in part due to
the fact that exposed contract workers with disease are
moved from the exposed diseased category (the "a"box) to
the unexposed disease category. For example, Otto Wong
stated that a contract worker with leukaemia (a
plaintiff in a lawsuit against Mobil) who worked at a
Mobil facility cleaning reactor vessels but did not work
as a regular employee for Mobil would not be categorized
as a Mobil worker. On the other hand, Wong stated that a
Mobil lawyer whose office was located at the same
facility would be included in the exposed group. (15)`
For rare diseases, such non-random misclassification
that switches exposed-diseased workers to the
unexposed-disease category can easily produce results
that show that "exposure" is protective. This is in fact
what Wong has often found.(16)
Scenario 3
1f we compare illness frequencies among exposed workers
with those in the general population (which is normally
less healthy than the workers when hired and even later)
we create a "healthy-worker effect" (HWE) with the
consequent related comparison bias. The HWE is too often
considered inevitable. As a matter of fact, ít is not
only an effect, a bias, or finally, an epidemiologic
artefact, but a serious error that can be avoided by an
epidemiologic study design in which an internal
comparison between exposed and unexposed workers is
performed correctly. As a matter of fact, an unexposed
group of oil refinery workers is often readily
identifiable within the plant under study.
When two of these errors occur at the same time, a
"negative" result is practically certain: a protective
effect will be demonstrated, and the studied workers
will show a reduction of their risk with a lower-than
expected number of observed cases (dead or ill).
In addition, the reduction of this risk might also be
statistically significant when the 90% confidence
ínterval (CI) - instead of the conventional 95% CI-is
calculated around the point estimate (Le, RR, SIR, SMR).
In fact, the conventional 95% interval might not show
any significant reduction due to its larger interval.
When we asked why this questionable methodologic
approach is used, we received different answers: the
data were analysed in many ways (and that is often true);
this way of analysis is usual (and .again, this is often
true); other approaches were not available; and, hard to
believe, a different approach would be too costly.
In the light of such premises, we have identified 15
elements that, when present in epidemiologic studies,
may lead to falsely negative results.12
These elements do not meet the criteria for good
epidemiologic practice oriented to the improvement of
public health.
CRITICAL POINTS
(ERRORS TO BE AVOIDED)
I. Privilege the use of descriptive instead of analytic
statistics, and the adoption of cross-sectional instead
of longitudinal epidemiologic studies;
2.fail to study the single homogeneous subgroups of
workers (in terms of exposure);
3.consider only the exposure to one single substance,
ignoring the possibility of exposure to multiple
substances and their interaction;
4.keep the unexposed and exposed workers mixed (creating
a dilution effect);
5.compare the exposed workers, who are usually selected
according to their overall positive health condition,
with the general population (instead of unexposed
workers), creating a healthy-worker effect (and
comparison bias);
6.take into consideration only one single disease (or
disease family, e.g., cancers) rather than all diseascs;
7.maintain desegregation of homogenous pathologies, thus
making statistical significance more difficult to
achieve;
8.fail to study reversible symptoms or serious sentinel
abnormalities;
9.study neoplastic effects (usually having medium long
latency periods) at follow-up periods too short to allow
for their development;
10.compare effects on the same target organ between
groups of individuals exposed to different agents (c,g.,
asbestos workers vs tobacco smokers) having the same
target (c.g., lung);
11 interpret the absence (or inadequacy) of both
environmental (and biological) monitoring and
epidemiologic studies as evidence of absence of exposure
and negative health effects;
12.keep the measurements of exposures separated from the
measurements of health effects;
13 privilege statistical significance rather than
biological significance, and consider the results of
large and multicentric studies more important than other
factors (biology, exposure, etc.);
14.use the conventional two-sided statistical test
instead of the one-sided statistical test, which appears
to provide the greatest reassurance against missing an
exposure-related effect; and, last but not least,
15 use univariate analysis instead of a multivariate
analysis that permits the simultaneous study of all the
relevant variables (c.g., age at hire, sex, area job,
calendar period, length of employment, latency, etc.).
CONCLUSIONS
The scientific evidence currently available suggests
that epidemiologic studies addressing the identification
of health risks for workers occupationally exposed to
noxious agents, as well as for residents in polluted
areas, rarely fulfil the standards of scientific rigor
and commitment to the principles of public health
protection if they are sponsored by strong economic
interests. For instance, studies of workers in oil
refineries conducted with total economic independence
have identified possible environmental and health risks
associated with exposures to more than 50 substances
classified as toxic, mutagenic, and carcinogenic, such
as asbestos, arsenic, benzene, chromium, nickel,
polycyclic hydrocarbons, and silica. The LARC has
therefore evaluated exposures in oil refineries as
probably carcinogenic to humans (9) By contrast, other
studies undertaken within the same areas of industrial
production, supported by industry and of doubtful
independence, do not report the existence of any risks.(6,10,11,15)
Epidemiologic investigations on oil refinery workers
carried out in Liguria (Italy) have identified specific
asbestos-related tumors,-such as pleural (18-19 and lung
(13) tumors, a finding that was subsequently and
independently confirmed in Canada .(20) These findings
were initially ignored and/or openly disputed, but were
later accepted. (15) Only Kaplan (21) had previously
registered an excess of mesotheliomas in these workers.
A review of studies of effects of exposures to selected
chemicals (alachIor, atrazine, formaldehyde, and
perchloroethylene) shows that 60% of such studies
conducted by non-industry researchers found these
chemicals hazardous, while only 14% of
industry-sponsored studies did so. (15-22)
There is a legitimate doubt that at least part of these
studies effectively pursued the actual identification of
specific risks, or complied with rigorous scientific
criteria. Such studies have contributed to a harmful
delay in the adoption of preventive measures and have
down played the significance of primary prevention,
especially in developing countries. (23)
The power of the limited number of multinational
corporations is proven by the fact that they operate
worldwide, with over 700 petroleum refineries where they
employ about 1,200,000 workers. Additional workers are
employed in related industries, where about 2,500
different products such as lubricants, bitumen (residual
oils), fueIs, solvents, fabrics, plastics,
disinfectants, perfumes, etc., are produced. (24) Most
studies sponsored by the companies owning the refineries
have provided reassuring results. (6-15) Given the way
in which the data were assembled and analysed, however,
they are definitely not reassuring.(7)
Based on this background, there is an urgent need for
strengthening economically and intellectually
independent scientific research that is explicitly
oriented toward primary prevention (i.c., the protection
of public health) and free from any business bias or
bias due to any vested economic interest. We suggest,
therefore, that qualified independent scientists be
allowed to reanalyse the original data sets of studies
that either 1) have been conducted or supported by
sponsors having strong conflicting economic interests or
2) report negative results or a protective effect where
there is a reasonable suspicion (a priori or
suggested by other studies) of the presence of increased
risk of an adverse health effect.
The authors thank Marcello Ceppi, Fabio Montanaro, and
Stefano Parodi for their helpful comments, and David
Egilman for his comments and substantial contribution to
Scenario 2.
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Contributor Biographies :
David Egilman, MD, MPH, à Clinical Associate ~roféssor,
in the Department of Community Health at Brown Unimrsity.
He is the faunder and chair of the board of the
Massachusetts-based nonprofit, Global Health through
Education, Training and Seriice, an organization
dedicated to improi4ng health in developing countries'
through innovations in education and service. Dr.
Egilman has published widely on issues of occupational
health and saféty ~ includíng the corporate corruption
of science in the asbestos, beryWum, pharmaccutical, and
other industrics. He is frequendy asked to serve as an
expert witness by both plaintiffs and defendants in
toxic tort and other litigation, including fitigation
involving several of the industrics discussed in the
articles authored and co-authored by him in this volume.
Susanna Rankin Bohme. AM, is a doctoral candidate at
Brown University, Department of American Civilization,
where she received her Master's Degree in 1999. Her work
at Brown focuscs on the intersections of health and
globalization. Her dissertation looks at the
international pesticide trade and worker and consumer
anti-pesticide activism in the United States and Central
America. She has co-authored papers on the ínfluence of
the asbestos industry on science, the history of
consumer and labor warnings, and the ideology of health
and science. She. works as a rescarcher at Never Again
Consulting in Affleboro, Massachusetts.
Marion Billings received her Bachelor of Arts degree at
Brown University in 2004 in Human BioIogy~ with a focus
in human health and discase. She has done critical
research on the epidemiology of the association between
asbestos containing automobile brake pads and
mesothelioma. In addition she has done extensive work ín
New York C.Naty with the newly emer~ cohort of
adolescents with perinatally acquired HIV. She is
currendy completing her Master's Degree in Public Health
afthe London School of Hygiene and Tropical Medicine, in
the United Kingdom.
Valerio Gennaro, MD, PhD, currendy serves as Director of
the Liguria Operative Center of the Nationai
Mewtheliorna Registy, Consultant at the Senate (Italian
Republic), and Executive medicai epidemiologist at the
Descriptive Epiderniology and Cancer Registry Unit in
the Epidemiology and Prevention Department of the
National Cancer Research Institute. He is President for
the Genoa Province of the Associazione Italiana Medici
per l'Ambiente [International Society of Doctors for
Enviroriment].
Peter Infante. DDS. DrPh, is Adjunct Professor of
Eniirorimental and Occupational Health at George
Washington University, School of Public Health and
Health Seriices. He has a Doctor of Public: Ilealth
degree frorn the Department of Epiderniology, Uníversity
of Michigan School of Public Health. He is a Fellow of
the American College of Epidemiology and of the
Collegium Rarnazzini. For 27 years, he conducted
research into the cancercausing effects of toxíc
substances found in the workpiace, and he is
internationally recognized for identifying two causcs of
human cancer. He has served on numerous national and
internatíonal panels and working groups related to the
identificafion of causcs of human cancers, including the
International Agency for Rescarch on Cancer, the
National Cancer Institute, the Presídent's Cancer Panel,
the Office of Technology Assessmen t of the U.S.
Congress and the National Academy of Sciences Committec
on Toxicology.
Dr. Infante has served as aà expert witness in
toxics-related litigation.
Michael E jacobson, PhD, is co-founder and Executive
Director of the Center for Science in the Public
Interest (CSPI), a nonprofit health-advocacy
organization. aPI advocates for improved public polícies
and corporate practices related to nutrition, food
safety, alcobol, and other issues. Its educatíon efforts
include media advocacy and publication of the *Nutrition
Action Healthletter» (circulatíon 900,000) and reports.
Sínce its foundíng in 1971, jacobson and C-SPI have led
the efforts > to win passage of the Nutrition Labeling
and Education Art, which requires nutrition infarmation
on most food labels; laws requíring warníng notices on
alcoholic beverage labels and setting a federal
definition for 'organic: food.»
W. Kovanlk, PhD, is Professor of Media Studics at
Radford University in southwestem VùZúùa, where he
teaches science and envirownent writing, media history,
and Media law. He is a graduate of VirZinia Commonwealth
UniVersitY (1974), the University of South Carolina (MA,
1983), and the
University of Maryland (PhD, 1993). Kovarik also has
served on the facuity at Vu~ Tech and the University of
Maryland. Ifis professional experience as a journalist
includes reporting and editing forjack Anderson, the
Associated Press, lime-111è Books, and the National
Center for Appropriate Technology.
Jock MeCulloch, PhD, ha% worked as a Ugislative Rescarch
Specialist for the Aust parliament and has taught at
vafiotes universities. His principal research interests
are in the history of medicine. He is thc author of
seven books, including a hístory of the ashestos
industry in Australia called A~s: ILT Human Cost (1986)
and Asbe_Sto.v Blues (2002), a study of blue asbestos
mining in South Africa. He is presendy writing a global
history of the ashestos índustry. Over the past 15 years
Dr.McCuUoch bas on four occasions worked as a consultant
for litigants.
Phyflis j. Mullenix, PhD, under a National Science
Foundation Fellowship Award, reccived a doctorate in
Pharmacology from. the University of Kansas Medical
Center in Kansw City in 1975. After completing
postdoctoral training in enkironmental medicine at the
johns Hopkins School ofSygine and Public Health in
Baltimore, sheheld academic appoíntments at Boston's
Children's Hospital Medical Center and the Harvard
School of Medicíne in the departrnents of Psychiatry,
Neuropathology, and Radiation Oncology.
Her many original rescarch publications focused on
detection of beliadoral dysfunction induced by perinatal
expostire to drugs and environrnental pollutants, and
they led to the development of the first computerized
pattern-recognition system that evaluated abnormal motor
pattems related to clinícal disorders. Dr. Mullenix has
served as an expert witness in fluoriderelated
litigation,
Rajeev Patel, MSc, PhD, is currently a po-,tdoctoral
fellow at the Centre for Civil Society, School of
Development Studics, University of KwaUlu-Natal, South
Affica, where he rescarches agrarian change. He has
degrees from the Universitics of Oxford and London, and
Comell University.
He previously worked with the Institute for Food and
Development Policy (Food First) in Oakland, California,
and is currently writing a book on the global food
system.
Enika RosenthaI, JD, MSI, is an attorney with
Earthjustce's international department, and has
consulted for the Pan American Health Organizatíon, the
Pesticide Action Network-Latin America, and Development
& Equíty, a consulting firm that analyzcd pesticide
issues for the Danish Agency for Intemational
Development (DANIDA).
PeteT Rosset, phD, is an agroccologist with a doctorate
in biology from the University of Michigan. He is past
director of the Institute for Food and Development
Policy (Food First), andis a researcher at the Center
for the Study of Rural Change in Mexico, an associate at
the Center for the Study of the Americas, in Berkeley,
CA, and a-visiting scholar in EnNironmental Science,
Policy and Management of the Universky of Calffornia at
Berkeley.
J.r Sass, PhD, is a Senior Scientist at the Natural
Resources Defense- Council. She has spent over a decade
as a laboratory researcher, in biomedical rescarch. Her
areas of study include neurobiology, cell and molecular
biology, and toxicology. Research specifics include
study of the effect of mercury on neural development,
study of the effect of alumínum on neurobiochemistry,
and study of stress proteins (chaperones) in embryonic
development. Her PhI) was completed in 1998, from. the
University of Saskatchewan, in the Department of Anatomy
and
VOI 11 /NO 4, OCTJDEC 2005 o
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Cell Biolooy. Her postdoctoral rescarch was completed in
2000, at the University of Maryland, Baltimore, in the
Program of Human Health and the Ensironment.
Caroline Snyder, PhD, did her undergraduate work at
Radcliffe College and graduate studíes at Han-ard
University. She is Professor Emerita at the Rochester
Institute of Technology, where she was one of the first
faculty members nationwide to design and teach
Ensironmental Studics and Environmental Science courses.
Before retiring, she chaired the Department of Science,
Technology, and Society. In 2003, the New
HampshireSierra Club awarded Snyder the Consevration
ActíNist Award «for her relentless efforts to raise the
consciousness of the publíc and legislators, both
national and local" to the problen-L% related to the
land applícation of munícipal scwage sludge. She is a
charter member of the Union of C3oncerned Scientists.
Dr. Snyder has scrved as a volunteer expert witness in
sludgerelated litigation.
Skip Spitzer, MA, is Program Coordinator at Pesticide
Action Network North America (PANNA). He holds an MA in
sociology from the University of California, Santa Cruz.
Beforejoining PANNA, he taught sociology at several
California colleges and universitics. Mr. Spítzer has
worked for almost 25 years as an acti-dst on a wide
range of socíaI and environmental issues. He is also an
activist skills trainer and a software engincer.
Robert Torres, PhD, is an Assistant Professor of
Sociology at St. Lawrence University. His rescarch
interests include the political economy of the global
agro-food system and the social ímplica-tions of
genetically modified organi.sms in agriculture.
Lorenzo Tomatis, RD, has served as Chairman of the
Scientific Council of the International Society of
Doctors for the Environrnent (ISDE) since 1999. He was
Director of the International Agency for Re~.ch on
Cancer (IARC), Lyon, France, fi-om 1982 to 1993, and
Scientific Director of the Institute for Mother's aRd
Child Health, Trieste, Italy, from 1996 to 1999.
John Zorabedian has worked as a jo urnalist covering
local and national govemment, economics, and sports. He
reccived his RA from Wesleyan University in 1999. He is
currently a rescarcher at Never Again Consulting.
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