| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
HEALTH POLICY AND ETHICS |
At the time of the study, David A. Savitz was with the Department of Epidemiology, School of Public Health, University of North Carolina, Chapel Hill. Roger E. Meyer is with the Department of Psychiatry, Georgetown University School of Medicine, Washington, DC, and the Department of Psychiatry, University of Pennsylvania School of Medicine, Philadelphia. Jason M. Tanzer is with the Department of Oral Diagnosis, School of Dental Medicine, and the Department of Laboratory Medicine, School of Medicine, University of Connecticut Health Center, Farmington. Sidney S. Mirvish is with the Eppley Institute for Research in Cancer, University of Nebraska Medical Center, Omaha. Freddi Lewin is with the Department of Oncology, Karolinska Institute, Stockholm, Sweden.
Correspondence: Requests for reprints should be sent to David A. Savitz, PhD, Department of Community and Preventive Medicine, Mount Sinai School of Medicine, One Gustave L. Levy Place, Box 1057, New York, NY 10029 (e-mail: david.savitz{at}mssm.edu).
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONHARM REDUCTION STRATEGIESEVIDENCE ON THE HEALTH...PUBLIC HEALTH CONCERNS WITH...QUESTIONS CONCERNING SMOKELESS...References |
|---|
Harm reduction strategies involve promoting a product that has adverse health consequences as a substitute for one that has more severe adverse health consequences. Smokeless tobacco low in nitrosamine content offers potential benefits in reducing smoking prevalence rates. Possible harm arises from the potential for such products to serve as a gateway to more harmful tobacco products, public misinterpretation of "less harmful" as "safe," distraction from the public health goal of tobacco elimination, and ethical issues involved in advising those marketing these harmful products. We offer a research agenda to provide a stronger basis for evaluating the risks and benefits of smokeless tobacco as a means of reducing the adverse health effects of tobacco.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONHARM REDUCTION STRATEGIESEVIDENCE ON THE HEALTH...PUBLIC HEALTH CONCERNS WITH...QUESTIONS CONCERNING SMOKELESS...References |
|---|
Recognition by leaders in some developed countries of these well-documented harmful consequences of smoking has resulted in increasingly effective actions, such as political action, taken to curtail the epidemic of tobacco-related diseases. Yet, the epidemic continues unabated and is even accelerating in many parts of the world. Tools for combating the epidemic include public policies intended to discourage tobacco use through taxation and restrictions on promotion, media campaigns designed to prevent smoking initiation and encourage cessation, individual counseling techniques1 and medications designed to promote and maintain smoking cessation, modification of tobacco products to reduce harmfulness, and substitution of less harmful for more harmful products (e.g., pharmaceutical nicotine for smoked tobacco).
|
HARM REDUCTION STRATEGIES |
|---|
|
TOPABSTRACTINTRODUCTIONHARM REDUCTION STRATEGIESEVIDENCE ON THE HEALTH...PUBLIC HEALTH CONCERNS WITH...QUESTIONS CONCERNING SMOKELESS...References |
|---|
The primary agents of concern in smokeless tobacco are the strongly carcinogenic tobacco-specific nitrosamines, especially N'-nitrosonornicotine (NNN), 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK), and nicotine itself. Although the exact magnitude of reduction in risk gained from substituting use of smokeless tobacco (particularly a low-nitrosamine product) for cigarette smoking is not easily quantified, a panel of experts estimated reductions in total mortality in the range of 90% to 95%.3 Despite such a large estimated benefit relative to smoking, important scientific and ethical questions arise.
Use of high-dose methadone maintenance treatment among heroin addicts has remained controversial despite 40 years of clear clinical evidence that it is moderately effective in rehabilitating opiate injection drug users and preventing the spread of HIV/AIDS. The price of this harm reduction is acceptance of continued addiction to a narcotic. Similar questions have been raised with regard to needle exchange programs designed to prevent the spread of HIV/AIDS among injection drug users. Parallel concerns arise with the substitution of less harmful for more harmful tobacco products: might this practice "sanitize" or even unintentionally initiate the harmful behavior? Does accommodating the harmful behavior suggest that society now condones or accepts it, discouraging more definitive solutions?
In Sweden the widespread use of Swedish snuff, called snus, a moist smokeless tobacco product placed under the upper lip, has been viewed as a possible model for successful harm reduction,4,5 although not without controversy.6 Sweden has achieved the lowest smoking prevalence rate in all of Europe, approximately 17% of adult men in 2000; an estimated 19% of adult men and 1% of adult women use snus daily.5 Furthermore, snus appears to be a component of successful smoking cessation.7 The low smoking prevalence rate and high rate of use of snus in Sweden may be related, but this association has not been established with certainty.
As recommended in the Institute of Medicine report Clearing the Smoke,8 manufacturers have now begun to develop and market tobacco products that reduce but do not eliminate exposure to tobacco-related toxicants. The report also called for consumers to be fully informed of the adverse consequences associated with these products and for surveillance to be conducted on health effects subsequent to marketing.
Star Scientific, a small tobacco company located in Chester, Va, began to market 2 smokeless tobacco products with very low levels of tobacco-specific nitrosamines and sought expert advice to better define the health risks associated with use of its products relative to smoked and conventional smokeless tobaccos. The company sought answers to the following questions: do smokeless tobacco products pose risks to health? If so, what is the nature of these risks, are there special populations at higher risk, and how do the risks compare with those of cigarette smoking? Are there physical or chemical characteristics of specific smokeless tobacco products or different uses that influence health risks?
Star Scientific provided an unrestricted grant to Best Practice Project Management Inc, a consulting and project management company located in Bethesda, Md, to convene a consensus conference to respond to these questions. A panel was convened in May 2003 with the agreement that it would respond to the questions and would, in addition, prepare a report for publication independent of the sponsor (the present article). The panel conducted a literature search on the topic and enlisted a range of experts with and without previous experience in tobacco research as members.
|
EVIDENCE ON THE HEALTH EFFECTS OF SMOKELESS TOBACCO |
|---|
|
TOPABSTRACTINTRODUCTIONHARM REDUCTION STRATEGIESEVIDENCE ON THE HEALTH...PUBLIC HEALTH CONCERNS WITH...QUESTIONS CONCERNING SMOKELESS...References |
|---|
Certain smokeless tobacco products have low levels of formaldehyde, and those that are smoke-cured also have significant amounts of polycyclic aromatic hydrocarbons, some of which, such as benzo[a]pyrene, are carcinogens.10 Swedish snus is composed of air-cured and fire-cured tobaccos. Since 1981, no fermentation has been used in its production, and a heating step sharply reduces microorganism content. Additives and flavors presumed to be safe are used in the process, and the net result is a product low in tobacco-specific nitrosamines (10 mg/kg or less).
The magnitude of the health risk associated with smokeless products appears to be associated with the type of tobacco and method of cultivation used. Greater potential for harm is associated with fire-curing (resulting in deposits of polycyclic aromatic hydrocarbons on the leaf), bacterial contamination, fermentation during production (which may favor the activity of micro-organisms that reduce nitrates to nitrites, leading to formation of nitrosamines),11 inclusion of certain additives in Asian products (e.g., areca nuts),12 and particular methods of product storage (some of which may promote continued bacterial formation of nitrosamines). Behavioral influences on health risks include amount of smokeless tobacco consumed and frequency of use, length of application, surface of application, oral hygiene, and rates of salivating, swallowing, and spitting. Risk associated with use may be modified by other exposures such as diet, alcohol consumption, and genetics.13–15
Carcinogenicity
Evidence that smokeless tobacco, which includes moist and dry snuff, causes oral cancer in humans is persuasive, given biological plausibility, specificity for buccal mucosa and gingiva (sites of contact), and the strength and consistency of epidemiological evidence across populations and geographic locations.16–18 The carcinogens NNN and NNK are found in the saliva of snuff dippers, and measurements of urinary excretions of NNK metabolites have been found to be similar among users of snuff and chewing tobacco and smokers.10
Reducing the nitrosamine content of smokeless tobacco (as in snus) should reduce carcinogenicity. Nonetheless, nitrosamines can be produced in vivo from nicotine itself and from tobacco-specific or other amines.9 Reports on the carcinogenicity of snus in the Scandinavian and other literature18–22 suggest minimal risk of oral or other cancers among users. However, as is the case with any smokeless tobacco product, snus contains carcinogenic nitrosamines, albeit at markedly lower levels than those found in the types of smokeless tobacco used in the United States and most other parts of the world; pharmaceutical nicotine does not contain these nitrosamines.23
American smokeless tobaccos can be divided into chewing tobacco, moist snuff, and dry snuff. In 1 review of different types of smokeless tobacco24 that evaluated 23 studies published between 1957 and 1998, no clear epidemiological evidence was uncovered that indicated chewing tobacco increases the risk of head or neck cancer. There was evidence of an increased risk of oral cancer associated with use of American dry snuff, but there were small or no clear risks of oral cancer associated with use of moist snuff, despite the presence of elevated nitrosamine levels in such products.
Cardiovascular Disease
Smokeless tobacco use produces a much slower onset and much lower peak concentration of nicotine in the blood supplying the heart and brain than does smoked tobacco, even with the same total daily dose of nicotine. Use of chewing tobacco or snuff for 30 minutes leads to a gradual rise in blood nicotine concentration followed by a sustained level of concentration that continues for up to 2 hours.25,26 The systemic dose from a single exposure to snuff or chewing tobacco is estimated at 2 to 3 mg.
Studies comparing cigarette smoking, snuff use, and use of chewing tobacco have demonstrated qualitatively similar effects on the sympathetic nervous system from nicotine.26 For all 3 products, the heart rate is increased, although its elevation is sharper and persists for a shorter interval with smoking than with snuff, consistent with the time course of blood concentrations. During most of the day, circadian heart rates are approximately 7 beats per minute higher among those who smoke cigarettes, chew tobacco, or use oral snuff than among those who are abstinent.
Epidemiological studies of snuff users have revealed no increased risk of myocardial infarction27 or increased atherosclerosis28 relative to nonusers. Although the acute nicotine-related effects of all tobacco products and pharmaceutical nicotine are essentially the same, the risk of clinically significant cardiovascular disease is clearly linked to smoking and not to use of smokeless tobacco.28 Similarly, risks associated with chronic obstructive pulmonary disease are a consequence of smoking but not of smokeless tobacco use.29
Oral Health Effects of Smokeless Tobacco
In addition to cancers, oral health concerns related to smokeless tobacco include leukoplakia, gingivitis, periodontitis, and dental caries as well as cosmetic concerns such as tooth staining, malodor, and tooth loss with resultant disfigurement. Leukoplakia is strongly associated with the use and placement position of smokeless tobacco and appears and disappears with changes in use.30 A Swedish study of mucosal and other leukoplakic lesions among snuff dippers showed reversible histological changes and suggested that Swedish snus produces less severe lesions than American snuff.31
Gingivitis and periodontitis are common infectious diseases in which bacteria colonize the tooth surface, with resulting gingival (gum) inflammation; recession from the tooth surface, exposing the roots; and accompanying destruction of the bony sockets of the teeth (periodontitis). Some data suggest that tobacco products adversely influence periodontitis-associated flora32,33 and host immune responses to inflammatory agents.34 There is no evidence of an association of smokeless tobacco with recession of the gums independent of pre-existing gingivitis. However, periodontitis is clearly more rapidly destructive among smokers and perhaps among smokeless tobacco users. Periodontitis also responds more poorly to treatment in smokers.35,36
One study conducted in the United States showed that caries (decay) of the root surfaces of teeth was associated with use of chewing tobacco but not snuff.37 Amount of decay was associated with intensity and duration of use and was probably a function of the high levels of sugar contained in chewing tobacco products.
Reproductive Health
The primary reproductive health concern with smokeless tobacco is nicotine itself, which has vasoconstrictive effects that can have an adverse influence on fetal growth and development. In rodents, nicotine exposure during pregnancy resulted in reduced birthweights, increased fetal mortality, abnormal bone development, and reduced activity levels.38 Among smokers, carbon monoxide also contributes to adverse effects on growth and brain development.38,39
One study focusing on infant birthweight suggested that women given nicotine patches usually continued to smoke but smoked less, and those who smoked less had improved birth-weights.40 Few studies of reproductive health among women who use smokeless tobacco are available from Western countries, because historically not many women of reproductive age have used such products. Some research has been conducted in India among women using chewing tobacco; although these studies are of limited relevance because of the differences between that country’s products and those used in the United States and Sweden, there were indications of increases in stillbirths41 and reductions in birthweights among the participants.41,42 A more recent study of Swedish snus users revealed decreases in birth-weights and increased risks of preterm delivery (relative risk [RR] = 1.6) and preeclampsia (RR = 1.6)43; these results call for corroboration.
|
PUBLIC HEALTH CONCERNS WITH SMOKELESS TOBACCO |
|---|
|
TOPABSTRACTINTRODUCTIONHARM REDUCTION STRATEGIESEVIDENCE ON THE HEALTH...PUBLIC HEALTH CONCERNS WITH...QUESTIONS CONCERNING SMOKELESS...References |
|---|
However, whereas scientists and public health experts acknowledge a gradient of harmfulness, the public may dichotomize products and behaviors as "harmful" or "safe." Applying the "harmful but safer" concept to the use of smokeless tobacco in comparison with active smoking poses a challenge to health educators and advertisers. Overstatement of harm could prevent smokers from switching to smokeless tobacco.44 Understatement of harm could lead non-users to adopt use of smokeless tobacco. Thus, the issue is not merely whether policymakers can agree on the potential value of risk reduction strategies but whether, in practice, the "harmful but safer" message can be effectively conveyed to the public.
The intense promotion of smokeless tobacco products to young men is clearly intended to foster initiation of use among this population. The legitimacy of harm reduction is predicated on effective targeting of active smokers and users of smokeless tobacco high in nitrosamine content. Ideally, a product should not be promoted or adopted among either nonusers of tobacco or active smokers capable of quitting. The Swedish experience indicates that snus does not serve as a gateway to smoking and appears to have contributed to dramatic declines in smoking as its use increased,22 but the response to such products may well differ in the United States. If it is not possible to isolate and market to the group of smokers who could benefit, there may be net harm from these products.
Given the financial incentive to market smokeless tobacco products on a wide scale, the success of a public health–based harm reduction strategy will depend in part on effective regulation. The complex regulatory environment affecting tobacco advertising and sales and the marketing of nicotine delivery products is applicable as well to the marketing of smokeless tobacco products low in nitrosamine content. Restrictions on advertising and sales to minors, reporting of constituents, and mandatory warning labels would be among the key considerations.
If a harm reduction strategy is adopted, it will require a clear definition of relative health risks associated with low-nitrosamine smokeless tobacco products, perhaps coupled with further limitations on advertising of more dangerous products. A comprehensive strategy is needed from the outset to ensure that the product is marketed solely as a harm reduction tool. The ultimate test of any regulatory approach to these new tobacco products is its impact on public health; thus, careful documentation of patterns and consequences of use is required.
Some public health advocates note that harm reduction strategies run counter to the ultimate goal of a tobacco-free society, confusing the public health message advocating abstinence from all forms of tobacco use. Furthermore, they argue, marketing one tobacco product as a substitute for another may divert attention and resources from policies designed to discourage or eliminate use altogether. Weakening the political will to aggressively pursue such proven strategies as increasing cigarette taxes, restricting public smoking, and enforcing age restrictions on purchasing tobacco may be an unintended consequence of promotion of harm reduction. Moreover, an attractive substitute in the form of smokeless tobacco could discourage active smokers from completely discontinuing their tobacco use.
A final concern facing researchers and public health advocates is ethical: whether and how to advise those who seek to market smokeless tobacco products. Manufacturers of smokeless tobacco would clearly be seeking profits through sales of a harmful product, albeit one that may have net public health benefits. These companies need scientific expertise if they are to address health concerns, devise marketing strategies consistent with the goal of harm reduction, and monitor the effectiveness of those strategies. The long history of dishonesty by the tobacco industry and by some of the researchers supported by that industry raises ethical concerns.
Proactively addressing the concerns expressed here should be helpful to policymakers and corporations contemplating the development and marketing of harm reduction products. If these issues can be raised objectively in advance, in an open forum, reputable scientists would have the opportunity to contribute their knowledge to policymakers, who would benefit from access to the best available information. Despite much success in eliminating tobacco use, we need more, not fewer, tools in the multifaceted effort to address this public health issue. Motivated current smokers who are unable to quit should be a specific target audience for harm reduction strategies.
As a result of the limited effectiveness of smoking cessation programs, recalcitrant smokers represent a sizable proportion of tobacco users both in the United States and around the world. Smokeless tobacco products low in nitrosamine content may represent a beneficial alternative for this group of smokers who have not been helped by other available tobacco control strategies.
|
QUESTIONS CONCERNING SMOKELESS TOBACCO |
|---|
|
TOPABSTRACTINTRODUCTIONHARM REDUCTION STRATEGIESEVIDENCE ON THE HEALTH...PUBLIC HEALTH CONCERNS WITH...QUESTIONS CONCERNING SMOKELESS...References |
|---|
Although many important issues remain unresolved, we believe that a harm reduction strategy needs to be considered as one of the elements of a broad program aimed at tobacco control. Finally, it is our belief that an effective harm reduction strategy merits the same rigorous assessment and critical evaluation as any other policy intended to advance public health.
|
Acknowledgments |
|---|
The author acknowledge the participation of the following individuals: Neal Benowitz and Martin Jarvis, who participated without compensation in the panel discussion on which this article was based, and Jerome Jaffe, Gio Gori, Herbert Severson, Stephen Hecht, Lars Ramstrom, and David Sweanor, who made presentations to the panel on the first day of deliberations.
|
Footnotes |
|---|
Contributors
D. A. Savitz chaired the panel discussion on which this article was based and was the principal author of the article. R. E. Meyer, J. M. Tanzer, S. S. Mirvish, and F. Lewin participated in generating ideas, wrote sections of the article, and reviewed and edited multiple drafts of the article.
Accepted for publication November 6, 2005.
|
References |
|---|
|
TOPABSTRACTINTRODUCTIONHARM REDUCTION STRATEGIESEVIDENCE ON THE HEALTH...PUBLIC HEALTH CONCERNS WITH...QUESTIONS CONCERNING SMOKELESS...References |
|---|
2. Hatsukami DK, Lemmonds C, Tomar SL. Smokeless tobacco use: harm reduction or induction approach? Prev Med. 2004;38:309–317.[CrossRef][Web of Science][Medline]
3. Levy DT, Mumford EA, Cummings KM, et al. The relative risks of a low-nitrosamine smokeless tobacco product compared with smoking cigarettes: estimates of a panel of experts. Cancer Epidemiol Biomarkers Prev. 2004;13: 2035–2042.
4. Bates C, Fagerström K, Jarvis M, Kunze M, McNeill, Ramström L. European Union policy on smokeless tobacco: a statement in favour of evidence-based regulation for public health. Available at: http://www.ash.org.uk/html/regulation/html/eusmokless.html. Accessed July 20, 2006.
5. Fagerström KO, Schildt E-B. Should the European Union lift the ban on snus? Evidence from the Swedish experience. Addiction. 2003;98: 1191–1195.[CrossRef][Web of Science][Medline]
6. Bolinder G. Swedish snuff: a hazardous experiment when interpreting scientific data into public health ethics. Addiction. 2003;98:1201–1204.[CrossRef][Web of Science][Medline]
7. Gilljam H, Galanti MR. Role of snus (oral moist snuff) in smoking cessation and smoking reduction in Sweden. Addiction. 2003;98:1183–1189.[CrossRef][Web of Science][Medline]
8. Stratton S, Shetty P, Wallace R, Bondurant S. Clearing the Smoke: Assessing the Science Base for Tobacco Harm Reduction. Washington, DC: Institute of Medicine; 2001.
9. Mirvish SS. Formation of N-nitroso compounds: chemistry, kinetics, and in vivo occurrence. Toxicol Appl Pharmacol. 1975;31:325–351.[CrossRef][Web of Science][Medline]
10. Hoffmann D, Adams JD, Lisk D, Fisenne I, Brunnemann KD. Toxic and carcinogenic agents in dry and moist snuff. J Natl Cancer Inst. 1987;79: 1281–1286.[Web of Science][Medline]
11. Mirvish SS. Role of N-nitroso compounds (NOC) and N-nitrosation in etiology of gastric esophageal, nasopharyngeal and bladder cancer and contribution to cancer of known exposures to NOC. Cancer Lett. 1995;93:17–48.[CrossRef][Web of Science][Medline]
12. Jeng JH, Chang MC, Hahn LJ. Role of areca nut in betel quid-associated chemical carcinogenesis: current awareness and future perspectives. Oral Oncol. 2001;37:477–492.[CrossRef][Web of Science][Medline]
13. Boyle P, Macfarlane GJ, Maisonneuve P, et al. Epidemiology of mouth cancer in 1989: a review. J R Soc Med. 1990;83:724–730.[Abstract]
14. McLaughlin JK, Gridley G, Block G, et al. Dietary factors in oral and pharyngeal cancer. J Natl Cancer Inst. 1988;80: 1237–1243.
15. Scully C. Oncogenes, tumor suppressors and viruses in oral squamous cell carcinoma. J Oral Pathol Med. 1993; 22:337–347.[CrossRef][Web of Science][Medline]
16. Preston-Martin S. Evaluation of the evidence that tobacco-specific nitrosamines (TSNA) cause cancer in humans. Crit Rev Toxicol. 1991;21: 295–298.[Web of Science][Medline]
17. Winn DM. Epidemiology of cancer and other systemic effects associated with the use of smokeless tobacco. Adv Dent Res. 1997;11:313–321.
18. Critchley JA, Unal B. Health effects associated with smokeless tobacco: a systematic review. Thorax. 2003;58: 435–443.
19. Ahlbom A, Olsson UA, Pershagen G. Health Hazards of Moist Snuff. Stockholm, Sweden: National Board of Health and Welfare; 1997.
20. Lewin F, Norell SE, Johansson H, et al. Smoking tobacco, oral snuff, and alcohol in the etiology of squamous cell carcinoma of the head and neck: a population-based case-referent study in Sweden. Cancer. 1998;82:1367–1375.[CrossRef][Web of Science][Medline]
21. Schildt EB, Eriksson M, Hardell L, Magnuson A. Oral snuff, smoking habits and alcohol consumption in relation to oral cancer in a Swedish case-control study. Int J Cancer. 1998;77:341–346.[CrossRef][Web of Science][Medline]
22. Foulds J, Ramstrom L, Burke M, Fagerström K. Effect of smokeless tobacco (snus) on smoking and public health in Sweden. Tob Control. 2003; 12:349–359.
23. Hatsukami DK, Lemmonds C, Zhang Y, et al. Evaluation of carcinogen exposure in people who used "reduced exposure" tobacco products. J Natl Cancer Inst. 2004;96:844–852.
24. Rodu B, Cole P. Smokeless tobacco use and cancer of the upper respiratory tract. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2002;93:511–515.[Web of Science][Medline]
25. Benowitz NL. Systemic absorption and effects of nicotine from smokeless tobacco. Adv Dent Res. 1997;11: 336–341.
26. Benowitz NL. Cardiovascular toxicity of nicotine: pharmacokinetic and pharmacodynamic considerations. In: Benowitz NL, ed. Nicotine Safety and Toxicity. New York, NY: Oxford University Press Inc; 1998:19–28.
27. Asplund K. Smokeless tobacco and cardiovascular disease. Prog Cardiovasc Dis. 2003;45:383–394.[Web of Science][Medline]
28. Huhtasaari F, Asplund K, Lundberg V, Stegmayr B, Westor PO. Tobacco and myocardial infarction: is snuff less dangerous than cigarettes? BMJ. 1992; 305:1252–1256.
29. Accortt NA, Waterbor JW, Beall C, Howard G. Chronic disease mortality in a cohort of smokeless tobacco users. Am J Epidemiol. 2002;156: 730–737.
30. Larsson A, Axell T, Andersson G. Reversibility of snuff dipper’s lesion in Swedish moist snuff users: a clinical and histologic follow-up study. J Oral Pathol Med. 1991;20:258–264.[CrossRef][Web of Science][Medline]
31. Andersson G, Axell T, Larsson A. Impact of consumption factors on soft tissue changes in Swedish moist snuff users: a histologic study. J Oral Pathol Med. 1990;19:453–458.[CrossRef][Web of Science][Medline]
32. Grossi SG, Zambon J, Machtei EE, et al. Effects of smoking and smoking cessation on healing after mechanical periodontal therapy. J Am Dent Assoc. 1997;128:599–607.
33. Haffajee AD, Socransky SS. Relationship of cigarette smoking to the sub-gingival microbiota. J Clin Periodontol. 2001;28:377–388.[CrossRef][Web of Science][Medline]
34. Bergström J, Preber H. The influence of cigarette smoking on the development of experimental gingivitis. J Periodontal Res. 1986;21:668–676.[CrossRef][Web of Science][Medline]
35. Kinane DF, Chestnutt I. Smoking and periodontal disease. Crit Rev Oral Biol Med. 2000;11:356–365.
36. Novak MJ, Novak KF. Smoking and periodontal disease. In: Newman MG, Takei HH, Carranza FA, eds. Carranza’s Clinical Periodontology. 9th ed. Philadelphia, Pa: WB Saunders Co; 2002: 245–252.
37. Tomar SL, Winn DM. Chewing tobacco use and dental caries among US men. J Am Dent Assoc. 1999;130: 1601–1610.
38. Dempsey DA, Benowitz NL. Risks and benefits of nicotine to aid smoking cessation in pregnancy. Drug Safety. 2001;24:277–322.[CrossRef][Web of Science][Medline]
39. Benowitz NL, Dempsey DA. Pharmacotherapy for smoking cessation during pregnancy. Nicotine Tob Res. 2004;6:S189–S202.
40. Wisborg K, Henriksen TB, Jespersen LB, Secher NJ. Nicotine patches for pregnant smokers: a randomized controlled study. Obstet Gynecol. 2000;96:967–971.[CrossRef][Web of Science][Medline]
41. Krishna K. Tobacco chewing in pregnancy. Br J Obstet Gynaecol. 1978; 85:726–728.[Web of Science][Medline]
42. Verma RC, Chansoriya M, Kaul KK. Effect of tobacco chewing by mothers on fetal outcome. Indian Pediatr. 1983; 20:105–111.[Medline]
43. England LJ, Levine RJ, Qian C, et al. Smoking before pregnancy and risk of gestational hypertension and preeclampsia. Am J Obstet Gynecol. 2002;186:1035–1040.[CrossRef][Web of Science][Medline]
44. Kozlowski LT, O’Connor RJ. Apply federal research rules on deception to misleading health information: an example of smokeless tobacco and cigarettes. Public Health Rep. 2003;118:187–192.[CrossRef][Web of Science][Medline]
This article has been cited by other articles:
|
|
 |
|
  L. Biener and K. Bogen Receptivity to Taboka and Camel Snus in a U.S. test market Nicotine Tob Res, June 29, 2009; (2009) ntp113v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. S. Timberlake, J. Huh, and C. M. Lakon Use of propensity score matching in evaluating smokeless tobacco as a gateway to smoking Nicotine Tob Res, April 1, 2009; 11(4): 455 - 462. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Wiium, L. E. Aaro, and J. Hetland Subjective attractiveness and perceived trendiness in smoking and snus use: a study among young Norwegians Health Educ. Res., February 1, 2009; 24(1): 162 - 172. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S Overland, J Hetland, and L E Aaro Relative harm of snus and cigarettes: what do Norwegian adolescents say? Tob. Control, December 1, 2008; 17(6): 422 - 425. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S S Hecht, S G Carmella, A Edmonds, S E Murphy, I Stepanov, X Luo, and D K Hatsukami Exposure to nicotine and a tobacco-specific carcinogen increase with duration of use of smokeless tobacco Tob. Control, April 1, 2008; 17(2): 128 - 131. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. S. Hecht, S. G. Carmella, S. E. Murphy, W. T. Riley, C. Le, X. Luo, M. Mooney, and D. K. Hatsukami Similar Exposure to a Tobacco-Specific Carcinogen in Smokeless Tobacco Users and Cigarette Smokers Cancer Epidemiol. Biomarkers Prev., August 1, 2007; 16(8): 1567 - 1572. [Abstract] [Full Text] [PDF]
|
|
Read all eLetters
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
