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J Am Dent Assoc, Vol 135, No 9, 1279-1286.
© 2004 American Dental Association

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RESEARCH

JADA Continuing Education

The prevalence of oral mucosal lesions in U.S. adults

Data from the Third National Health and Nutrition Examination Survey, 1988–1994



JAY D. SHULMAN, D.M.D., M.A., M.S.P.H., M. MILES BEACH, D.M.D., M.S., M.B.A. and FRANCISCO RIVERA-HIDALGO, B.S., D.M.D., M.S.


   ABSTRACT
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background. Most reports of oral lesion prevalence are based on studies of atypical populations. There are no published studies on oral mucosal lesion prevalence in U.S. adults that are based on a national probability sample.

Methods. The Third National Health and Nutrition Examination Survey, or NHANES III, employed a complex, multistage sample of 33,994 civilian, noninstitutionalized people from 19,528 households. Dentist examiners were trained to recognize, classify and record in a standardized manner the clinical characteristics of each of the 48 conditions of interest to include diagnosis, size, location, surface morphology, color consistency, pain, duration and history using procedures based on the World Health Organization’s Guide to Epidemiology and Diagnosis of Oral Mucosal Diseases.

Results. Examinations were performed on 17,235 people aged 17 years and older, of whom 4,801 (27.9 percent) had a total of 6,003 lesions. Denture-related lesions (stomatitis, hyperplasia, ulcers, inflammation and angular cheilitis) composed 8.4 percent and tobacco-related lesions (smokeless tobacco–related and nicotinic stomatitis) composed 4.7 percent of all lesions. Discounting denture-related lesions, amalgam tattoos were the most prevalent lesions (3.30 percent), followed closely by cheek/lip bites (3.05 percent) and frictional white lesions (2.67 percent). Smokeless-tobacco users (odds ratio, or OR, = 3.90) and removable denture wearers (OR = 3.57) had the highest odds of having a lesion.

Conclusion. Lesion prevalences differed significantly by age, sex, race/ethnicity, denture wearing and tobacco use. When lesion-specific prevalences are cited in the literature, they should be stratified by covariates known to be associated with them.

Diagnosis of the wide variety of lesions that occur in the oral cavity is an essential part of dental practice. An important element in establishing a diagnosis is knowledge of the lesions’ relative frequency, or prevalence at one point in time (otherwise known as "point prevalence"). While oral mucosal lesion prevalence data from the National Survey of Oral Health in U.S. School Children1 provide such a knowledge base regarding children, this is not the case for U.S. adults. None of the studies pub lished on this topic has been based on national probability samples, and reports in the literature generally are based on convenience samples of atypical populations such as dental school patients, college students, or people examined at health fairs, nursing homes or veterans’ facilities. These sampling frames pose serious challenges to validity, because they are not representative of the general population. For example, patients examined at health fairs in low-income areas likely would have a different distribution of risk factors than would those drawn from more affluent areas. Similarly, subjects drawn from institutionalized populations such as nursing homes2 are likely to be nonrepresentative, as they are likely to have more comorbidities. To the extent that such studies tell us anything, it is about the population studied. Even Knapp’s3 study of 181,338 Army recruits is limited in its generalizability to healthy young adults. Moreover, many studies have neither explicit diagnostic criteria for the oral mucosal lesions nor examiner standardization when more than one examiner is used.

Lesion prevalences differed significantly by age, sex, race/ethnicity, denture wearing and tobacco use.

With the notable exception of Axéll,4 who reported the results of a random sample of 20,333 drawn from approximately 250,000 residents older than the age of 15 years from Uppsala County, Sweden, the literature is devoid of credible prevalence data for the adult general population. Axéll4 found that among the most prevalent lesions were recurrent aphthae (two-year prevalence rate: 17.70 percent), recurrent herpes labialis (two-year prevalence rate: 17.38 percent), denture stomatitis (two-year prevalence rate: 16.02 percent) and geographic tongue (two-year prevalence rate: 8.57 percent).

With the notable exception of one article, the literature is devoid of credible prevalence data for the adult general population.

Because of the paucity of information about the prevalence of oral mucosal lesions, we report the results of the oral mucosal examination from the Third National Health and Nutrition Examination Survey, or NHANES III, a probability sample of civilian, noninstitutionalized people in the United States conducted from 1988 through 1994.5


   METHODS
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Oral mucosal examinations were performed as part of NHANES III, a periodic survey conducted by the National Center for Health Statistics on the basis of a complex, multistage sample plan. The survey was designed to provide national estimates of the health and nutritional status of the civilian, noninstitutionalized U.S. population two months of age and older. From 19,528 randomly selected representative households, 33,994 subjects were interviewed by NHANES III staff members; 30,818 were examined in mobile examination centers and 493 were examined at home. Calibrated physicians and dentists performed all examinations and extensive health, social and nutritional medical histories were obtained via interviews with the subjects or their parents. A detailed discussion of the survey methods is presented in an article by Drury and colleagues.6

Dentist examiners were trained to recognize, classify and record in a standardized manner the clinical characteristics of each of the 48 conditions of interest, to include diagnosis, size, location, surface morphology, color consistency, pain, duration and history using procedures based on the World Health Organization’s Guide to Epidemiology and Diagnosis of Oral Mucosal Diseases and Conditions.7 While smears for yeast were taken on lesions suspected of being angular cheilitis, candidiasis, denture stomatitis, erythroplakias, leukoplakias, lichen planus and median rhomboid glossitis, all diagnoses were clinical.8

We analyzed point prevalence—the proportion of subjects who had a lesion—in the aggregate and by sex, age, race/ethnicity (non-Hispanic white, non-Hispanic black and Mexican-American), use of removable dentures and tobacco-use history. Tobacco-use history was determined during the health interview. We created six mutually exclusive categories of tobacco-use history:

– smokers who also use smokeless tobacco;
– mokeless-tobacco users;
– smokers;
– former smokers;
former smokeless-tobacco users;
– those who never smoked more than 100 cigarettes, 20 cigars or 20 pipefuls or used smokeless tobacco or snuff in their lifetime.

We excluded from analyses using the race/ethnicity variable any subject who did not fall into one of the three race/ethnicity categories. This resulted in the removal of 702 subjects, categorized as "other," from the analysis.

Since the survey used complex, multistage sampling, we used a specialized software package (SAS-callable SUDAAN 8.0, Research Triangle Institute, Research Triangle Park, N.C.) to compute standard errors for all variables, adjusting for the effects of the survey design (design effect) as well providing the (weighted) population size to which the prevalence data can be projected. For example, the 17,245 subjects aged 17 years and older who received an oral mucosal examination are projected to represent 182,292,666 people in the U.S. population.

Results are presented in tables showing the actual number of lesions found, weighted count and standard error adjusted for the design effect, 95 percent confidence intervals, or CIs. In addition, odds ratios, or ORs, from bivariate and multivariate logistic regressions are presented with 95 percent CIs for the adjusted ORs. The multivariate model adjusts the ORs for the effect of the other variables in the model. If unity does not fall within the confidence limits of an OR, the OR is significantly different from unity at (at least) the .05 level.


   RESULTS
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Oral mucosal examinations were performed on 17,235 adults aged 17 years and older, of whom 4,801 (27.9 percent) had a total of 6,003 clinically detectable lesions. After adjusting for the design effect, we can project that 28.24 percent of the U.S. population has at least one clinically recognized lesion. Figure 1Go shows the locations of the lesions. The hard palate had the most lesions (25.9 percent), followed by the gin-giva (20.4 percent), lip (15.4 percent) and dorsum of the tongue (14.2 percent). Figure 2Go compares lesion prevalence by site for four categories of tobaccouse history. Smokeless-tobacco users had significantly higher prevalences of lesions on the lips, mucosa, tongue, commissures and vestibule than did nonusers. Cigarette smokers who used smokeless tobacco had a severalfold higher prevalence of lesions on the floor of the mouth than did users of either tobacco product alone and nonusers of tobacco. Smokers had a higher prevalence of palatal lesions than did nonsmokers.



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Figure 1. Site distribution of mucosal lesions.

 


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Figure 2. Prevalence of lesion site, by tobacco-use category.

 
Table 1Go shows for each type of lesion the total number, overall prevalence ranking, point prevalence, standard error and 95 percent CIs. For some lesions with low prevalences and large standard errors, lower limits of the 95 percent CIs were negative and were truncated to zero.


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TABLE 1 PREVALENCE OF MUCOSAL LESIONS IN 17,235 U.S. ADULTS 17 YEARS OF AGE AND OLDER.*

 
Candida-related lesions (many of which were denture-related) composed 8.65 percent and tobacco-related lesions (smokeless tobacco–related and nicotinic stomatitis) composed 2.55 percent of all lesions. Discounting Candida-related lesions, amalgam tattoos were the most prevalent type of lesions (3.30 percent) followed closely by cheek/lip bites (3.05 percent) and frictional white lesions (2.67 percent). Of the 1,291 subjects of whose lesions smears were taken, 208 (16.10 percent) were positive for yeast. The lesion-specific positive rates were median rhomboid glossitis (50.0 percent), candidiasis (35.0 percent), angular cheilitis (23.3 percent), denture stomatitis (14.9 percent), leukoplakias (10.3 percent), lichen planus (6.3 percent) and erythroplakias (0.05 percent).
Smokeless-tobacco use was the strongest risk factor, followed by use of removable dentures. The odds of having a lesion increased with age.

Table 2Go (page 1284) shows the prevalence of mucosal lesions by age group, sex, race/ethnicity, tobacco use and use of removable dentures; ORs from bivariate and multivariate logistic regressions; and 95 percent CIs for the adjusted ORs. The odds of having a mucosal lesion increase steadily with age; people aged 70 years and older have almost twice the odds of having a lesion as do those aged from 17 through 29 years. Note that the adjusted ORs are appreciably lower than the bivariate ORs for age and race/ethnicity suggesting that a substantial amount of the bivariate effect of age and race/ethnicity was due to other variables in the multivariate model. Whites had higher odds of having a lesion (OR = 1.25) than did blacks (OR = 1.03) or Mexican-Americans (the reference level). Male subjects (OR = 1.28) had significantly greater odds of having a lesion than did female subjects. Smokeless-tobacco users had almost four times the odds of having a lesion as did those who never used tobacco (OR = 3.90), smokeless-tobacco users who also smoked had more than two times the odds of having a lesion (OR = 2.29), and smokers’ odds of having a lesion were 25 percent greater (OR = 1.25) than those of subjects who had never used tobacco. Removable-denture wearers had more than three times the odds of having a lesion (OR = 3.57) than did those who did not wear removable dentures.


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TABLE 2 PREVALENCE OF MUCOSAL LESIONS BY AGE GROUP, SEX, RACE/ETHNICITY, TOBACCO USE AND USE OF REMOVABLE DENTURES.*

 

   DISCUSSION
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
The NHANES III data yield fairly tight 95 percent CIs for the more prevalent lesions, but the intervals widen as the prevalence decreases. For example, geographic tongue lesions have a prevalence of 1.85 percent (95 percent CI, 1.41 to 2.29), a range of 0.88 percentage points or 46 percent of the prevalence. Compare this, however, with lichen planus (Table 1Go), for which the prevalence is 0.10 percent (95 percent CI, 0.03 to 0.17) and the difference between lower and upper limits is 140 percent of the prevalence. Consequently, reported prevalences for rare conditions (especially if standard errors or CIs are not provided) should be interpreted with caution.

The 48 mucosal lesions reported were diverse with respect to etiology and morbidity. For lesions associated with specific risk factors such as nicotinic and denture stomatitis, the overall prevalence depends on the underlying distribution of the risk factor (that is, smoking and denture-wearing, respectively). Consequently, comparing population prevalences for such lesions without knowing the underlying distribution of these risk factors is not advisable.

Smokeless-tobacco use was the strongest risk factor, followed by use of removable dentures. The odds of having a lesion increased with age, even after we adjusted for tobacco use, the presence of removable dentures, race/ethnicity and sex. While tobacco use was a substantial risk factor, it likely would have been greater if the dose (number of cigarettes smoked and amount of smokeless tobacco used per day) were included in the model.

Since NHANES III used similar methods as used in the Swedish study,4 it is instructive to compare the results of the two studies. Table 3Go (page 1285) compares selected prevalence estimates for different types of lesions (shown in Table 1Go) with those from the Swedish study.4 Axéll4 found higher prevalence rates of most common mucosal lesions than were found in NHANES III. Keeping in mind that both studies represent large probability samples from the general population and used World Health Organization diagnostic categories,7 it is surprising that the prevalences are so different to the point that for every lesion, the prevalence estimates from one study fall outside the 95 percent CI of the other study. Moreover, the standard errors from the Swedish study generally were greater than those from NHANES III, perhaps reflecting the greater racial/ethnic homogeneity of the Swedish population.


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TABLE 3 COMPARISON OF SELECTED STATISTICAL VARIABLES REGARDING LESION TYPE IN NHANES III* AND IN THE SWEDISH STUDY.{dagger}

 
The prevalence of angular cheilitis in the Swedish study was 3.76 percent compared with 0.71 percent in NHANES III. How can this difference be explained? First, while there may be differences in diagnostic criteria, it is unusual to see such a consistent difference across virtually all lesion types. Second, to the extent that prevalence is a function of age or sex, samples with different age and sex distributions will have different prevalences even if the age-specific prevalences are the same. Finally, in cases in which the lesion is associated with another risk factor (such as wearing complete dentures, using tobacco, having amalgam restorations), the samples may have a different distribution of the risk factor, so the analysis again must be stratified. Table 2Go shows that the prevalence of mucosal lesions, in general, does vary with age, sex, race/ethnicity, tobacco use and the wearing of removable dentures. Our point here is that most of the prevalence rates cited in pathology textbooks are, at best, of minimal utility in making generalizations to the entire adult population, since they cannot be broken down into strata.

While NHANES III is a robust, well-respected population-based data source that used trained examiners and a sophisticated sampling methodology, it nonetheless has limitations. One limitation is inherent in its design. Since it is cross-sectional, it can be used to explore only associations, not causal relationships. Second, the lesions were identified without benefit of laboratory or histologic tests. While trained examiners can be expected to identify many entities (such as aphthous ulcers, nicotinic stomatitis and recurrent herpes labialis) without additional diagnostic aids, others (such as nevus) may have other differential diagnoses and can be diagnosed clinically with less certainty. Furthermore, some lesions (tumors, nonspecific lesions and lesions of unknown etiology) could not be identified at all. Finally, the study may understate the prevalence of mucosal lesions that present as acute problems. For example, people may be more inclined to seek treatment for mucoceles, ranulas (even buccal mucosa fibromas that suffer biting trauma at every meal) and other acute conditions, so these are less likely to be seen in prevalence studies.


   CONCLUSION
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
We found that the prevalence of many mucosal lesions depends greatly on individual characteristics. Because of this, prevalence rates for oral mucosal lesions cited in texts should be based on studies of general populations and be stratified by risk factors for the specific lesion. These may include sex, age, race/ethnicity, tobacco use and use of removable dentures. Also, in comparing prevalences from different studies, it is important to know whether the subjects selected for examination were selected using a probability sample of a representative population. Finally, even well-executed studies in one country may not produce valid estimators of prevalences in other countries. Future studies should focus on multivariate models to explore the risk factors for lesions that are of clinical significance.


   FOOTNOTES
 

Dr. Shulman is a professor and the graduate program director, Dental Public Health, Department of Public Health Sciences, Baylor College of Dentistry, Texas A&M University System Health Science Center, 3302 Gaston Ave., Dallas, Texas 75246, e-mail "JShulman{at}bcd.tamhsc.edu". Address reprint requests to Dr. Shulman.


Dr. Beach is an assistant professor, Department of Periodontics, Baylor College of Dentistry, Dallas.


Dr. Rivera-Hidalgo is an associate professor and the director of research, Department of Periodontics, Baylor College of Dentistry, Dallas.


   REFERENCES
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

  1. Kleinman DV, Swango PA, Pindborg JJ. Epidemiology of oral mucosal lesions in United States schoolchildren: 1986–87. Community Dent Oral Epidemiol 1994;22:243–53.[Medline]

  2. Bhaskar SN. Oral lesions in the aged population: a survey of 785 cases. Geriatrics 1968;23(10):137–49.

  3. Knapp MJ. Oral disease in 181,338 consecutive oral examinations. JADA 1971;83:1288–93.[Medline]

  4. Axéll T. A prevalence study of oral mucosal lesions in an adult Swedish population. Odontol Revy 1976;27:1–103.[Medline]

  5. National Center for Health Statistics. Third National Health and Nutrition Examination Survey, 1988–1994, NHANES III examination and adult data files (on CD-ROM). Hyattsville, Md.: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention; 1996.

  6. Drury TF, Winn DM, Snowden CB, Kingman A, Kleinman DV, Lewis B. An overview of the oral health component of the 1988–1991 National Health and Nutrition Examination Survey (NHANES III—Phase 1). J Dent Res 1996;75(special issue):620–30.[Medline]

  7. Kramer IR, Pindborg JJ, Bezroukov V, Infirri JS. Guide to epidemiology and diagnosis of oral mucosal diseases and conditions: World Health Organization. Community Dent Oral Epidemiol 1980:8(1):1–26.[Medline]

  8. National Center for Health Statistics. National Health and Nutrition Examination Survey III oral examination component. Hyattsville, Md.: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Health Statistics; 1992:5-23–5-35.




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