Philip Morris
Report of the Surgeon General's Advisory Committee on the Health Consequences of Using Smokeless Tobacco
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Marilyn M. Massey, M.P.H., Technical Support Staff Coordinator for the Advisory
Committee, Senior Associate, Prospect Associates, Rockville, Maryland
Gardner C. McMillan, M.D., Associate Director for Etiology, Arteriosclerosis
and Hypertension, National Heart, Lung, and Blood Institute, Bethesda, Maryland
Jens J. Pindborg, D.D.S., Dr. Odont., Professor of Oral Pathology, Royal
Dental College, Copenhagen, Panum Institute, Copenhagen, Denmark
John M. Pinney, Executive Director, Institute for the Study of Smoking Behavior
and Policy, John F. Kennedy School of Government, Harvard University,
Cambridge, Massachusetts
Earl S. Pollack, Sc.D., President, Pollack Associates Ltd., Bethesda, Maryland
Richard J. Riseberg, Chief Counsel, United States Public Health Service,
Rockville, Maryland
Thomas L. Robertson, M.D., Chief, Cardiac Diseases Branch, National Heart,
Lung, and Blood Institute, Bethesda, Maryland
Beatrice A. Rouse, Ph.D., Epidemiologist, Division of Epidemiology and Statistical
Analysis, National Institute*on Drug Abuse, Rockville, Maryland
Donald R. Shopland, Acting Director, Office on Smoking and Health, United States
Public Health Service, Rockville, Maryland
Sol Silverman, Jr., M.A., D.D.S., Professor and Chairman of Oral Medicine,
University of California, San Francisco, California
Chester Slaughter, M.A., Deputy Regional Inspector General for Analysis and
Inspections, Office of the Inspector General, Dallas, Texas
K.W. Stephen, D.D.Sc., H.D.D.R.C.P.S., Head of Oral Medicine and Pathology,
University of Glasglow, Glasgiow, Scotland .
Ronald W. Wilson, M.A., Director, Division of Epidemiology and Health Promotion,
National Center for Health Statistics,~Hyattsville, Maryland
Ernst L. Wynder, M.D.., President, American Health Foundation, New York, New
York
Maruta Zitans, M.Sc., Program Analyst, Office of the Inspector General,
Washington, D.C.
The Advisory Committee and authors also acknowledge several organizations
for their contributions in identifying relevant literature and/or in offering
critical reviews of the manuscript.
Institute of Medicine, National Academy of Sciences for providing through its
Board on Health Promotion and Disease Prevention a critique of the Advisory
Committee's review methods and drafts of the report.
2501250011
.
X11
International Agency for Research on Cancer (IARC), Lyon, France, for providing
IARC Monograph No. 37 on the Evaluation of the Carcinogenic Risk of Chemicals
to Humans: Tobacco Habits Other Than Smoking; Betel-Quid and Areca-Nut
Chewing and Some Related Nitrosamines, September 1985.
National Center for Health Statistics and National Institute on Drug Abuse
for providing data on the prevalence and trends of smokeless tobacco use in
the United States.
Office on Smoking and Health for bibliographic citations and other documents
pertinent to the literature review.
Smokeless Tobacco Council, Inc. (Michael J. Kerrigan, President), for providing
approximately 15,000 citations considered relevant by a number of the smoke-
less tobacco companies, including the collection of testimonies representing
the smokeless tobacco industry's position concerning the health consequences'
of smokeless tobacco.
The Advisory Committee and authors also acknowledge the contributions
of the following staff members and others who assisted in the preparation of
the report:
Kathy Bauman, Editorial Assistant to the Deputy Director, Division of Cancer
Prevention and Control, National Cancer Institute, Bethesda, Maryland
Julie Begun, Research Assistant, Prospect Associates, Rockville, Maryland
Barbara Clark, M.S., M.P.H., Technical Support Staff Coordinator for ,Ion-Ca.ncer-
Oral Effects Experts, Prospect Associates, Rockville, Maryland
Shelley Clark, Conf erence Coordinator, Prospect Associates, Rockville, Maryland
Nancy Cowan, Conf erence Coordinator, Prospect Associates, Rockville, Maryland
Kathleen Edmunds, Library Research Assistant, Prospect Associates, Rockville,
Maryland
Robyn Ertwine, Librarian-Information Specialist, Prospect Associates, Rockville,
Maryland
Catherine Fisher, Secretary, Prospect Associates, Rockville, Maryland
Barbara Hayden, Secretary, Prospect Associates, Rockville, Maryland
Douglas Hunter, Library Assistant, Prospect Associates, Rockville, Maryland
Karen Jacob, Editor, Prospect Associates, Rockville, Maryland
tV
Margaret Johnson, Typist, Prospect Associates, Rockville, Maryland LA
~
Mary Johnson, Typist, Prospect Associates, Rockville, Maryland !`J
LJ1
Virginia Knill, Typist, Prospect Associates, Rockville, Maryland ~p
©
t%J
xiii
Solomon Levy, M.P.H., Associate Director, Office of the Surgeon General,
Rockville, Maryland
Paula Margus, Library Research Assistant, Prospect Associates, Rockville,
Maryland
Nancy McCormick-Pickett, M.A., Technical Support Staff Coordinator for
Carciaogenesis Experts, Prospect Associates, Rockville, Maryland
Lee McPherson, Typist, Prospect Associates, Rockville, Maryland
Robbie Morsette, Library Assistant, Prospect Associates, Rockville, Maryland
Elizabeth Mugge, Secretary to the Deputy Director of the Division of Cancer
Prevention and Control, National Cancer Institute, Bethesda, Maryland
Arthur Nelson, Library Research Assistant, Prospect Associates, Rockville,
Maryland
Ro Nemeth-Coslett, Ph.D., Visiting Scientist, Biology of Dependence and Abuse
Potential Assessment Laboratory, Addiction Research Center, National Insti-
tute on Drug Abuse, Baltimore, Maryland
Simon Plog, Typist, Prospect Associates, Rockville, Maryland
Nancy Rudner, M.S.N., M.P.H., Technical Support Staff Assistant, Prospect
Associates, Rockville, Maryland
Estelle Schwalb, Technical Writer-Editor, Prospect Associates, Rockville,
Maryland
Barbara Shapiro, Editor, Prospect Associates, Rockville, Maryland
John Shea, Ph.D., Technical Writer-Editor, Prospect Associates, Rockvi Lle,
Maryland
Dorritt Silber, Secretary, Prospect Associates, Rockville, Maryland
Dori Steele, Proofreader, Prospect Associates, Rockville, Maryland
Deborah S. Swansburg, Program Officer, Institute of Medicine, National
Academy of Sciences, Washington, D.C.
xiv
INTRODUCTION, OVERVIEW, AND CONCLUSIONS
DEVEIAPMENT AND ORGANIZATION OF THE REPORT
This report from the Surgeon General's Advisory Committee on the Health
Consequences of Using Smokeless Tobacco represents the first comprehensive
assessment of the biomedical and behavioral literature describing experimental
and human evidence on the health consequences of using smokeless'tobacco. The
content of this report is the work of numerous erperts within the Department
of Health and Human Services as well as distinguished scientists outside the
organization.
Each chapter of the report was prepared based on manuscripts written by
scientists who are recognized for their understanding of the specific content
areas. Manuscripts were subjected to extensive peer review by a large
number of experts in the specific areas of interest.
The report includes a "Preface" that presents the essence of the entire re-
port and an "Introductioa, Overview, and Conclusions." The body of the report
consists of the following four chapters:
Chapter 1-Prevalence and Trends of Smokeless Tobacco Use in the United
States
Chapter 2-Carcinogenesis Associated With Smokeless Tobacco Use
Chapter 3--Noacancerous Oral Health Effects Associated With Smokeless
Tobacco Use
Chapter 4-Nicotine Exposure: Pharmacokinetics, Addiction, and Other
Physiologic Effects
HISTORICAL PERSPECTIVE
The use of smokeless tobacco is a worldwide practice with numerous vari-
ations in the nature of the product used as well as in the customs associated
with its use. In the United States, smokeless tobacco consists of chewing
tobacco and snuff. The predominant mode of use of these nonsmoked tobaccos
is oral, although they may be placed in or inhaled into the nasal cavity.
Tobacco sniffing, however, has been and remains a rare practice in the United
States.
Smokeless tobacco was used in the United States in the early 1600's when
snuff made its way to the Jamestown Colony in Virginia through the efforts of
John Rolfe in 1611 (1). Evidence of tobacco chewing, however, was not found
until a century later in 1704 (2).
The use of tobacco, including smokeless tobacco, has been controversial
since its introduction. In the past, tobacco use was considered by some as
beneficial. As early as 3500 B.C., there are indications that tobacco was an
article of established value to the inhabitants of Mexico and Peru. It
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appears that people who frequently lacked sufficient food alleviated their
hunger pains by chewing tobacco (3). Smokeless tobacco was also thought to
have several medicinal uses. Among Native Americans, for example, chewing
tobacco was used to alleviate toothaches, disinfect cuts, and relieve the
effects of snake, spider, aad insect bites (4). Moreover, during the 19th
and early 20th centuries in America, dental snuff was advertised to relieve
toothache pain; to cure neuralgia, bleeding gums, and scurvy; and to pres-erve
and whiten teeth and prevent decay (1). _
On the other hand, the history of tobacco use has had numerous adversaries,
including the following (1):
In 1590 in Japan, tobacco was prohibited. Users lost their property
and were jailed.
King James VI of Scotland in the early 1600's was a strong antismoking
advocate who increased taxes on tobacco 4,000 percent in an attempt
to reduce the quantity imported to England.
In 1633, the Sultan Murad IV of Turkey made any use of tobacco a
capital offense, punishable by death from hanging, beheading, or
starvation. He maintained that tobacco caused infertility and reduced
the fighting capabilities of his soldiers.
The Russian Czar Michael Fedorovich, the first Romanov (1613-1645),
prohibited the sale of tobacco, stating that users would be subjected
to physical punishment and that persistent users would be killed.
A Chinese law in 1683 threatened that anyone possessing tobacco would
be beheaded.
During the mid-1600's, Pope Urban VIII banned the use of snuff in churches,
and Pope Innocent X attacked its use by priests in the Catholic Church.
Other religious groups also banned snuff use: John Wesley, the founder
of Methodism, attacked its use in Ireland; the Mormons, Seventh-Day
Adventists, Parsees and Sikhs of;India, Buddhist monks of Korea,
members of the Tsai Li sect of China, and some Ethiopian Christian
sects forbade the use of tobacco.
Frederick the Great, King of Prussia, prevented his mother, the
Dowager Queen of Prussia, from using snuff at his coronation in
1790.
Louis XV, ruler of France from 1723-1774, banned snuff use from the
Court of France.
Scientific observations concerning the health effects of smokeless
tobacco use were first noted in 1761 by John Hill, a London physician and
botanist who reported five cases of polypuses, a"swelling in the nostril
that was hard, black and adherent with the symptoms of an open cancer" (5).
He concluded that nasal cancer could develop as a consequence of tobacco
snuff use (sniffing).
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Evidence that suggested a possible association between smokeless tobacco
use and oral conditions in North America and Europe was not reported until
1915 when Abbe identified several tobacco chewers among a series of oral
cancer patients and commented that smokeless tobacco use may be a risk factor
for this cancer (6). In the late 1930's, Ahblom observed in Sweden that more
patients with buccal, gingival, and "mandibular" cancers than with other
cancers reported the use of snuff or chewing tobacco (7). In the United States,
case reports of oral cancer among users of snuff or ,chewing tobacco appeared
in the early 1940's (8). The first epidemiologic study of smokeless-tobacco
was not conducted until the early 1950's (9). Since that time, several
scientists have described a pattern of increased risk of oral cancer among
smokeless tobacco users.
Investigations of other possible health effects of smokeless tobacco use
(e.g., noncancerous oral effects, addiction, and other physiologic consequences)
are more recent subjects of scientific inquiry that have been undertaken pri-
marily in the past two decades.
A brief review of the health consequences of smokeless tobacco was presented
in the 1979 Surgeon General's report on smoking and health (10). Since that
review, the results of additional studies addressing the role of smokeless
tobacco in health have become available and thus provide the basis of this
current comprehensive review.
REVIEW METHODS
For the purpose of evaluating the scientific evidence to be included in
this report, the Advisory Committee called upon the same criteria to determine
causality as have been used for a number of Surgeon General's reports on smok-
ing for the past two decades. The following criteria were used as the primary
guidelines for assessing whether any associations between smokeless tobacco
use and each of the disease areas or health condition's under examination
were likely to be causal in aature:
Consistency of the association-similar observations by multiple
investigators in different locations and situations, at different
times, and using different methods of study.
Strength of the association-high ratio of disease rate for the
population exposed to the suspected risk factor compared to the
population unexposed to the risk factor.
Specificity of the association-associations with the exposure
exist for a specific or limited set of diseases, and associations
with the disease exist for a specific or limited set of exposures.
Temporal relationship of the association-exposure tq the suspected
etiologic factor precedes the disease.
Coherence of the association-epidemiologic observations are conso-
nant with all else that is known about the disease.
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In addition to these criteria, the general principles employed by the Inter-
national Agency for Research on Cancer (IARC)* in evaluating the carcinogenic
risk of chemicals or complex mixtures (table 1) were used as needed to supple-
ment the primary causation criteria (11).
OVERVIEW
The use of smokeless tobacco products in the United States was widespread
until the end of the 19th century. With the advent of antispitting laws, loss
of social acceptability, and increased popularity of cigarette smoking, its
use declined rapidly in this century. However, recent national data indicate
a resurgence in smokeless tobacco habits with more than 12 million persons -
estimated as users of some form of smokeless tobacco in 1985. An upward trend
in use is emerging, particularly among young males.
Given the evidence that smokeless tobacco is regaining popularity, seri-
ous questions have been raised about its adverse health effects. Most notably,
this behavior has been linked to cancer, specifically, oral cancer. Analytic
epidemiologic studies now indicate that the use of oral snuff increases the
risk of oral cancer several fold and that among long-term snuff dippers the
excess risk of cancers of the cheek and gum may reach nearly fiftyfold. This
conclusion is consistent with the judgment of a recent working group of the
IARC, which assessed the carcinogenic risk associated with tobacco habits other
than smoking (11).
The conclusion that smokeless tobacco causes cancer results from several
lines of evidence: the presence of high levels of carcinogens in smokeless
tobacco; the metabolic conversion of products of smokeless tobacco into geno-
toxic agents; the consistency of the oral cancer-smokeless tobacco association
across epidemiologic investigations conducted in diverse locations; the trend
in increasing oral cancer risk with duration of exposure; the strength of the
association with oral cancer; and the occurrence of the highest risks for
cancers at the anatomic sites where the tobaccoo exposures are the greatest.
In addition, a number of clinical observations and studies show an asso-
ciation between smokeless tobacco use and some noncancerous and precancerous
oral health conditions. The development of a portion of oral leukoplakias in
both teenage and adult users can be attributed to the use of smokeless tobacco.
The risk of developing these leukoplakic lesions increases with increased ex-
posure, and a number of studies now suggest that some snuff-iaduced leukoplakias
can undergo transformation to dysplasia and further to carcinoma. The evidence
concerning the adverse health effects of smokeless tobacco use on other oral
soft and hard tissues is only suggestive at this time.
*The IARC was established in 1965 by the World Health Assembly as an indepen-
dently financed organization within the framework of the World Iieaith Orga-
nization. It conducts a program of research concentrating particularly on the
epidemiology of cancer and the study of potential carcinogens in the human
environment.
2501259017
t
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xviii
The magnitude of blood nicotine levels resulting from smokeless tobacco
use has been shown to be similar to that from cigarette smoking. Therefore,
the nicotine-related health consequences of smoking would also be expected to
result from smokeless tobacco use. Given the nicotine content of smokeless
tobacco, the users ability to sustain elevated blood levels of nicotine, and
the well-established data implicating nicotine as an addictive substance, it
is reasonable to expect that smokeless tobacco is capable of producing nicotine
addiction in users.
There is also some suggestive evidence that nicotine may play a contribu-
tory or supportive role in the development of coronary artery and periphera]i
vascular disease, hypertension, peptic ulcer disease, and fetal mortality and
morbidity. .
The conclusions in this report on the relationship between smokeless to-
bacco use and cancer, noncancerous and precancerous oral conditions, and
addiction and dependence are substantially in agreement with those published
at a recent National Institutes of Health (NIH) Consensus Development'Confer-
ence on the Health Implications of Smokeless Tobacco Use (12).
CONCLUSIONS
Prevalence and Trends of Smokeless Tobacco Use in the United States
1. Recent national data indicate that over 12 million persons used some form
of smokeless tobacco (chewing tobacco and snuff) in 1985 and that approxi-
mately 6 million used smokeless tobacco weekly or more often. Use is
increasing, particularly among young males.
2. The highest rates of use are seen among teenage and young adult males. A
recent national survey indicates that 16 percent of males between 12 and 25
years of age have used some form of smokeless tobacco within the past year
and that from one-third to one-half of these used smokeless tobacco at
least once a week. Use by females of all ages is consistently le'ss than
that of males; about 2 percent have used smokeless tobacco in the last year.
3. State and local studies corroborate the national survey findings. The
prevalence of smokeless tobacco use by youth and young adults varies widely
by region, but use is not limited to a single region. In several parts of
the country, as many as 25 to 35 percent of adolescent males have indicated
current use of smokeless tobacco.
Carcinogenesis Associated With Smokeless Tobacco Use
1. The scientific evidence is strong that the use of smokeless tobacco can
cause cancer in humans. The association between smokeless tobacco use
and cancer is strongest for cancers of the oral cavity.
2. Oral cancer has been shown to occur several times more frequently among
snuff dippers than among nontobacco users, and the excess risk of cancers
of the cheek and gum may reach nearly fiftyfold among long-term snuff
users.
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XLX
3. Some investigations suggest that the use of chewing tobacco also may
increase the risk of oral cancer.
4. Evidence for an association between smokeless tobacco use and cancers
outside of the oral cavity in humans is sparse. Some investigations
suggest that smokeless tobacco users may face increased risks of tumors
of the upper aerodigestive tract, but results are currently inconclusive.
5. Experimental investigations have revealed potent carcinogens in snuff and
chewing tobacco. These include nitrosamines, polycyclic aromatic hydro-
carbons, and radiation-emitting polonium. The tobacco-specific nitrosamines
N-aitrosoaornicotine and 4-(methylnitrosamino)-l-(3-pyridyl)-l-butanone,
have been detected in smokeless tobacco at levels 100 times higher than
the regulated levels of other nitrosamines found in bacon, beer, and
other foods. Animals exposed to these tobacco-specific nitrosamines, at
levels approximating those thought to be accumulated during a human life-
time by daily smokeless tobacco users, have developed an excess of a
variety of tumors. The nitrosamines can be metabolized by target tissues
to compounds that can modify cellular genetic material.
6. Bioassays exposing animals to smokeless tobacco, however, have generally
shown little or no increased tumor production, although some bioassays
suggest that snuff may cause oral tumors when tested in animals that are
infected with herpes simplex virus.
Noncancerous and Precancerous Oral Health Effects Associated With Smokeless
Tobacco Use
1. Smokeless tobacco use is responsible for the development of a portion of
oral leukoplakias in both teenage and adult users. The degree to which
the use of smokeless tobacco affects the oral hard and soft tissues is
variable depending on the site of action, type of smokeless tobacco pro-
duct used, frequency and duration of use, predisposing factors, cofactors
(such as smoking or concomitant gingival disease), and other factors not
yet determined.
2. Dose response effects have been noted by a number of investigators. Longer
use of smokeless tobacco results in a higher prevalence of leukoplakic
lesions. Oral leukoplakias are commonly found at the site of tobacco
placement.
3. Some snuff-induced oral leukoplakic lesions have been noted upon continued
smokeless tobacco use to undergo transformation to a dysplastic state. A
portion of these dysplastic lesions can further develop into carcinomas
of either a verrucous or squamous cell variety.
4. Recent studies of the effects of smokeless tobacco use on gingival and
periodontal tissues have resulted in equivocal findings. While gingival
recession is a common outcome from use, gingivitis may or may not occur.
Because longitudinal data are not available, the role of smokeless
tobacco in the development and progression of gingivitis or periodontis
has not been confirmed.
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5. The evidence concerning the effects of smokeless tobacco use on the
salivary glands is inconclusive.
6. Negative health effects on the teeth from smokeless tobacco use are
suspected but unconfirmed. Present evidence, albeit sparse, suggests
that the combination of smokeless tobacco use in individuals with existing
gingivitis may increase the prevalence of dental caries compared to nonusers
without concomitant gingivitis. Reports of tooth abrasion or staining have
not been substantiated through controlled studies; only case reports are
available.
Nicotine Exposure: Pharmacokinetics, Addiction, and Other Physiologic Effects
1. The use of smokeless tobacco products can lead to nicotine dependence or
addiction.
2. An examination of the pharmacokinetics of nicotine (i.e., nicotine absorp-
tion, distribution, and elimination) resulting from smoking and smokeless
tobacco use indicates that the magnitude of nicotine exposure is similar
for both.
3. Despite the complexities of tobacco smoke self-administration, systematic
analysis has confirmed that the resulting addiction is similar to that
produced and maintained by other addictive drugs in both humans and animals.
Animals can learn to discriminate nicotine from other substances because of
its effects on the central nervous system. These effects are related to
the dose and rate of administration, as is also the case with other drugs
of abuse.
4. It has been shown that nicotine functions as a reinforcer under a variety
of conditions. It has been confirmed that nicotine can function in all
of the capacities that characterize a drug with a liability to widespread
abuse. Additionally, as is the case with most other drugs of abuse,
nicotine produces effects in the +iser that are considered desirable to
the user. These effects are caused by the nicotine and not simply by the
vehicle of delivery (tobacco or tobacco smoke).
5. Nicotine is. similar on all critical measures to prototypic drugs of abuse
such as morphine and cocaine. The methods and criteria used to establish
these similarities are identical to those used for other drugs suspected
of having the potential to produce abuse and physiologic dependence.
Specifically, nicotine is psychoactive, producing transient dose-related
changes in mood and feeling.. It is a euphoriant that produces dose-related
increases in scores on standard measures of euphoria. It is a reinforcer
(or reward) in both human and animal intravenous self-administration
paradigms, functioning as do other drugs of abuse. Additionally, nicotine
through smoking produces the same effects, and it causes neuroadaptation
leading to tolerance and physiologic dependence. Taken together, these
results confirm the hypothesis that the role of nicotine in the compulsive
use of tobacco is the same as the role of morphine in the compulsive use of
opium derivatives or of-cocaine in the compulsive use of coca derivatives.
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