Lesions of the oral mucosa: an epidemiological study of 23785 Mexican patients

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Mexican patients

José L. Castellanos, DDS,aand Laura Díaz-Guzmán, DDS,bLeón, Guanajuato, Mexico

DE LA SALLE BAJÍO UNIVERSITY

This study is a cross-sectional report of oral mucosal lesions in 23785 patients more than 15 years of age who requested elective dental care in a dental school. Among the patients examined, the general lesion rate was 356.60 lesions per 1000 patients. Sixty-eight entities were identified, the lesions being more common among males.

White, red, and ulcerated lesions were seen to predominate, associated mostly with chronic irritative causative factors.

The prevalence rates of individual oral mucosal lesions ranged from 0.55 to 105.36 per 1000 patients examined. Age and sex assessment showed some differences in the type and presentation rates of the lesions. These and other epidemiological aspects are discussed. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105:79-85)

The present study reports the results of a cross-sectional evaluation of the permanent prospective registry of oral mucosal lesions of the Department of Oral Diagnosis and Medicine, Dental School, De La Salle Bajío Uni- versity, León, Guanajuato, Mexico, with the purpose of establishing the prevalence of oral mucosal lesions in a population of patients more than 15 years of age, of either sex, seeking elective dental care in a dental school.

While a dental school setting may differ from the situation found in the general population (because it is not open or randomized),1,2this may be a model indic- ative of general and daily dental practice, particularly compared with other settings that deal with rather se- lected populations such as those seen in specialty cen- ters,3-6 nursing homes and veterans facilities,7or oral mucosa disease prevalence established in biopsy ser- vices.8Such selected populations may also be considered to include either very young9,10or very old patients.11-14 Although such settings afford highly specific information, they necessarily introduce bias to the mucosal lesion prevalences and incidences found in the general popula- tion. Similar inconveniences are posed by small popula- tion samples.15-17

The present report includes 22 years of data on 23785 patients. A prior evaluation involved 7297 pa- tients, corresponding to a period of 7.5 years,18 to which 16488 observational subjects were added. The

increase in patients is expected to reinforce the reliabil- ity and validity of the study, to better define epidemi- ological aspects relating to pathological changes of the oral mucosa.

MATERIAL AND METHODS

We consecutively examined data of 23785 patients more than 15 years of age who requested elective dental care from January 1982 to December 2003. The guide to clinical procedures of the Department of Oral Diag- nosis and Medicine was used to this effect.19 Each suspect lesion was assessed clinically by qualified staff members who were assisting dental students, accompa- nied by a direct patient interview; where necessary, complementary studies were made (e.g., laboratory tests and histopathologic evaluation). Following confir- mation of the diagnosis, management and control mea- sures were defined. For the present study, the following patient data were collected from the corresponding clinical histories: identification of the lesion or condi- tion, the underlying etiology, and patient age and sex.

For presentation and analysis, lesion prevalence was reported as the number of lesions per 1000 patients, with distribution into the following categories: (1) clin- ical characteristics, (2) etiology, (3) general prevalence, with identification of the 30 most frequent lesions, (4) sex distribution and mean age, with identification of the 15 most frequent lesions per sex, and (5) major lesion groups and specific lesion prevalence, based on the etiology and prevalence of the total mucosal lesions recorded in the study (this aspect will be the subject of future reports).

RESULTS

Fig. 1 reports the general statistics of the study.

Among the 23785 patients examined, the general lesion rate was 356.60 lesions per 1000 patients. The age

aHead, Department of Periodontics, Dental School, De La Salle Bajío University.

bHead, Department of Oral Diagnosis and Oral Medicine, Dental School, De La Salle Bajío University.

Received for publication Jan 15, 2006; returned for revision Dec 29, 2006; accepted for publication Jan 29, 2007.

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ranged from 15 to 97 years, with a global average of 33.06 years (38.55 years for the patient subgroup with lesions). Lesions were more common among males (male:female ratio⫽ 1.4:1). As to morbidity (percent-

age of lesions in relation to the number of subjects in the corresponding subgroup), a three-fold greater risk of developing mucosal lesions was recorded among the males compared with the female population (6% in males vs. approximately 2% in females). Sixty-eight different lesions were identified.

Table Ireports the general clinical characteristics. The lesions identified were classified as (1) superficial changes, (2) soft tissue masses, and (3) miscellaneous.

The superficial changes included white lesions (keratotic and nonkeratotic), red lesions, and pigmented lesions de- fined by the presence of endogenous pigments such as melanin, or exogenous pigments such as amalgam, dyes, or graphite. This large group also comprised ulcers, ves- icles, and pits and fissures. The latter included deep linear infolding lesions such as fissured tongue. A pit was in turn defined as a hollow fovea or indentation, such as commis- sural lip pits. The masses were subclassified into nonneo- plastic volume increase (reactive, hyperplastic, hamar- tomatous, or cystic), and neoplastic (either benign or malignant). White, red, and ulcerated lesions were seen to predominate.Table IIshows the etiopathogenic distribu- tion of these lesions— of the 8 major groups identified, 76.99% corresponded to the first 3 groups: morphogenetic Fig. 1. General statistics of the lesions of the oral mucosa in 23785 patients.

Table I. Clinical appearance of lesions of the oral mucosa in 23785 patients

No. of lesions per 1,000

patients Average

Age (y) Male Female Total

Superficial changes

White nonkeratotic (4) 148.76 88.50 107.34 32.90

Red (12) 93.88 75.47 81.23 39.88

Ulcers/vesicles (9) 64.56 54.25 57.47 37.83 White keratotic (9) 67.11 29.11 40.99 42.59 Color (8): endogenous and

exogenous pigments

27.21 27.79 27.61 41.11

Fissure lesions and pits (6) 6.46 7.77 7.36 36.93 Soft tissue masses

Nonneoplastic (13) 34.70 40.73 34.64 36.98 Reactive, hyperplasic,

hamartomatous, and cystic

Neoplastic (6) 3.50 4.65 4.29 38.82

Miscellaneous (1) 0.00 0.06 0.04 36.00

Total 442.68 323.69 352.39 38.20

No. of lesions in the group are shown in parentheses.

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disorders, reactive lesions, and traumatic lesions (this in- formation will be discussed in more detail in a future publication).

Table IIIreports the 30 most frequent lesions found.

All were identified during the examination upon admis- sion—no alterations detected from anamnesis were in- cluded. These 30 lesions were 98.33% of all identified

lesions, with a rate of 0.80:105 per 1000. The remain- ing 38 lesion types had a rate per 1000 of less than 0.55.

Regarding patient age, the lesions most removed from the general mean of the study population, with presentation in subjects more than 50 years of age, were epulis fissuratum, chronic atrophic candidiasis, leuko- plakia, inflammatory papillary hyperplasia, and smok- Table II. Etiopathogenesis of lesions of the oral mucosa in 23785 patients

Catagory Etiopathogenesis No. lesions per 1000 patients Relative % Accumulative %

I Morphogenetic disorders 115.32 32.73

II Reactive 85.80 24.35 57.07

III Traumatic 70.17 19.91 76.99

IV Infectious 37.50 10.64 87.63

V Factitious 22.70 6.44 94.07

VI Growths and neoplasms 10.64 3.02 97.09

VII Immune 10.09 2.86 99.95

VIII Systemic diseases 0.17 0.05 100.00

352.39 100.00

TABLE III. Lesions of greatest prevalence in the oral mucosa of 23785 patients

Lesion

Male n⫽ 7435

No. of lesions per 1000 patients

Female n⫽ 16350

No. of lesions per 1000 patients

Total n⫽ 23785

No. of lesions per 1000 patients

Age (y)

Leukoedema 1086 146.07 1420 86.85 2506 105.36 32.50

Traumatic ulceration 333 44.79 624 38.17 957 40.24 31.64

Frictional keratosis 377 50.71 388 23.73 765 32.16 37.03

Traumatic erythema 245 32.95 435 26.61 680 28.59 32.90

Morsicatio buccarum 236 31.74 280 17.13 516 21.69 27.36

Chronic atrophic candidiasis 118 15.87 361 22.08 479 20.14 52.48

Melanotic maculae of the lip* 25 13.27 67 17.71 92 16.23 31.14

Inflammatory fibrous hyperplasia 92 12.37 285 17.43 377 15.85 42.51

Smoker melanosis* 25 13.27 34 8.99 59 10.41 49.46

Aphthous ulcer 68 9.15 136 8.32 204 8.58 30.45

Lip herpes 72 9.68 116 7.09 188 7.90 32.26

Benign migratory glossitis 70 9.41 111 6.79 181 7.61 31.97

Nicotinic stomatitis 72 9.68 28 1.71 100 4.20 47.88

Angular cheilitis 26 3.50 60 3.67 86 3.62 47.94

Nevi 23 3.09 52 3.18 75 3.15 36.63

Epulis fissuratum 15 2.02 59 3.61 74 3.11 59.61

Papilloma 14 1.88 55 3.36 69 2.90 38.67

Inflammatory papillary hyperplasia 21 2.82 38 2.32 59 2.48 50.58

Hemangioma 20 2.69 34 2.08 54 2.27 48.65

Erythema of unidentified cause 20 2.69 30 1.83 50 2.10 38.10

Gingival hyperplasia 15 2.02 30 1.83 45 1.89 39.64

Hairy tongue 20 2.69 20 1.22 40 1.68 38.13

Phenytoin gingival hyperplasia 11 1.48 23 1.41 34 1.43 28.82

Mucocele 12 1.61 22 1.35 34 1.43 28.68

Reticular lichen planus 8 1.08 21 1.28 29 1.22 44.31

Fibrosis and scar tissue 11 1.48 12 0.73 23 0.97 28.00

Leukoplakia 13 1.75 10 0.61 23 0.97 51.00

Chemical burns 7 0.94 14 0.86 21 0.88 32.10

Pyogenic granuloma 6 0.81 14 0.86 20 0.84 42.15

Verruca vulgaris 2 0.27 17 1.04 19 0.80 36.68

3063 431.78 4796 313.85 7859 350.71 38.98

M⫽ 1884.

F⫽ 3784.

*Rates based on 5668 patients. Those entities were considered after 1999 (M⫽ 1884, F ⫽ 3784).

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ing-associated melanosis. In comparison, the lesions associated with the youngest age intervals were morsi- catio buccarum, fibrosis and scars, and mucocele.

Table IVreflects morbidity and order of importance of the 15 most frequent lesions according to patient sex.

This differentiation was made on the grounds that sex may condition risk differences due to biologic factors, psychological aspects, or differences in social role.

These 15 lesions account for 91.24% of all lesions reported. The male:female proportion of the lesions found was 1.25:1 (1.4:1 for the total group). Morbidity risk (lesions vs. the number of patients within the group) was 2.15:1 (male:female ratio, 3.0:1 for the total group). Only one third of the lesions showed a higher incidence among females, with rates very similar to those found in males: chronic atrophic candidiasis, la- bial melanotic macule, traumatic fibroma, angular chei- litis, and melanocytic nevus. However, several sex con- trasts were noted, as an example, nicotinic stomatitis was almost 6 times more frequent in men than in women (5.1:1). Other lesions were approximately twice as com- mon in males, such as frictional keratoses (2.1:1), morsi- catio buccarum (1.8:1), and leukoedema (1.7:1). Regard- ing the order of these pathologies, only 2 lesions showed variations in ranking of more than 3 levels: morsicatio buccarum and nicotinic stomatitis.

DISCUSSION

Prior to discussing the results of the present study, it should be stressed that the findings are influenced by

the conditions under which the data were collected. If the operative and circumstantial particularities associ- ated with the geographic, social, and cultural setting are taken into consideration, the results obtained can be compared with those of similar studies. In the Depart- ment of Oral Diagnosis and Medicine, admission to clinical care is processed when patients request elective dental care by professionals assisting dental students.

This department usually does not deal with oral or dental emergencies, which are seen in the correspond- ing emergency service. Patients spontaneously present- ing for dental consultation exhibit an attitude that may differ from that found in an epidemiological survey of an open population. In numerical terms, most of our series is composed of females. We did not include lesions registered from the anamnesis or as result of interconsultation requested from other services in our dental school.

Considering the information presented in the afore- mentioned paragraph and in comparison with other studies carried out elsewhere in the world, it is seen that surveys such as that published by Bouquot20involve a sample size similar to our own, although the patients were older, because the services were offered in cancer detection clinics where the attended population is typ- ically of older age. This must be taken into consider- ation because the prevalences of both reactive and degenerative lesions increase with age,21frequently as a result of preexisting systemic diseases or risk factors that introduce some bias to the sampling procedure.22-24 TABLE IV. Characteristics by patient gender

Male Female

Lesion n⫽ 7435

No. of lesions per

1000 patients Lesion n⫽ 16350

No. of lesions per 1000 patients

Leukoedema 1086 146.07 Leukoedema 1420 86.85

Frictional keratosis 377 50.71 Traumatic ulcer 624 38.17

Traumatic ulcer 333 44.79 Traumatic erythema 435 26.61

Traumatic erythema 245 32.95 Frictional keratosis 388 23.73

Morsicatio buccarum 236 31.74 Chronic atrophic candidiasis 361 22.08

Chronic atrophic candidiasis 118 15.87 Melanotic maculae of the lip* 67 17.71

Melanotic maculae of the lip* 25 13.27 Inflammatory fibrous hyperplasia 285 17.43

Smoking melanosis* 25 13.27 Morsicatio buccarum 280 17.13

Inflammatory fibrous hyperplasia 92 12.37 Smoking melanosis* 34 8.99

Lip herpes 72 9.68 Aphthous ulcers 136 8.32

Nicotinic stomatitis 72 9.68 Lip herpes 116 7.09

Benign migratory glossitis 70 9.41 Benign migratory glossitis 111 6.79

Aphthous ulcers 68 9.15 Angular cheilitis 60 3.67

Angular cheilitis 26 3.50 Nevi 52 3.18

Nevi 23 3.09 Nicotinic stomatitis 28 1.71

2868 405.56 4397 289.44

Risk index 1.41 0.66

Risk index. M:F proportion 2.15

M⫽ 1884.

F⫽ 3784.

*On the basis of 5668 patients after the year 1999.

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The study of Axéll1is included as a solid reference for comparison purposes, for although it involves a smaller sample of patients, it exceeds the international stan- dards required of epidemiological studies.25While the report published by Shulman2involved an open popu- lation not requesting dental care (home visits), the large sample size of the study has led us to include it for comparison. In this sense,Table Vattempts to establish comparisons with studies similar to our own in terms of the population size evaluated and oral lesion classifi- cation.1,2,20 A comparison is made of the frequency with which the first 10 disease entities of this study coincide with the first 10 entities of other surveys, although the order of lesions and their prevalences may differ. The purpose is to determine whether any lesion or lesions are repeatedly cited as the most prevalent or common disorders in different parts of the world.

In the present report, and compared with our 1991 subset comprising 7297 patients,18 6 of the 10 most prevalent lesions in the initial survey were seen to remain the same: leukoedema, traumatic ulcer, fric- tional keratoses, chronic atrophic candidiasis, irritative hyperplasia, and minor recurrent aphthous ulcers. Fac- tors such as time and improvement in diagnostic quality observed in recent years may influence the registered prevalence of oral mucosal lesions. In effect, regarding the factor time, it is important to point out that there have been technological advances; social and ecologi- cal changes; modifications in the coverage, type, and speed of massive communications; population dis- placements; and pharmacological and medical ad- vances that influence population longevity and quality

of life. The increase in smoking among women during the 1980s, the influence of government antismoking campaigns over the last 10 years, increased sexual freedom, global emergence of the acquired immunode- ficiency syndrome, the increase in cases of anorexia, and the growing practice of oral piercing and cosmetic lip tattooing among young people are examples of lifestyle changes that will have an impact on study outcomes.

In the study of Axéll1involving 8698 patients, 5 of these same lesions were among the most frequent. In the series published by Bouquot20 comprising 23,616 patients, the same coincidence was established for 3 of the lesions—a situation that is seen to repeat in the report published by Shulman et al.2Thus, in these 4 surveys, each conducted in at least 7000 patients, the same lesions coincided in 50% to 100% of cases. Irri- tative keratosis ranked in the first 10 places in each of these studies. Traumatic ulcer and inflammatory fibrous hyperplasia were cited in 3 of 4 studies. Thus, it can be concluded that lesions of a traumatic origin are those most commonly reported in different parts of the world.

Only traumatic erythema, smoking-associated melano- sis, and minor recurrent aphthous ulcers were not cited among the 10 most common lesions in any of the 3-comparator reports. Labial melanotic macule, chronic atrophic candidiasis, and leukoedema likewise showed a high prevalence in 3 of the 4 studies compared. In relation to this latter entity, which is actually best regarded as a variant of normality, it is interesting to note that it is common in both northern European populations and in the mixed-race Latin American pop- TABLE V. Comparative analysis with other major epidemiological studies

Lesion

No. of lesions per 1000 patients

Coincidence among the 4 studies

I* II† III‡ IV§ Times %

Leukoedema 105.36 459.3 (1) 2 50

Traumatic ulcer 40.24 17.8 (10) 5.2 (4) 3 75

Irritative keratosis 32.16 43.7 (5) 4.7 (5) 26.7 (4) 4 100

Traumatic erythema 28.59

Morsicatio buccarum 21.69 30.5 (3) 2 50

Chronic atrophic candidiasis 20.14 36.0 (1) 2 50

Melanotic maculae of the lip 16.23 100.4 (2) 2 50

Inflammatory fibrous hyperplasia 15.85 20.7 (9) 12.0 (2) 3 75

Smoking associated melanosis 10.41 Minor recurrent aphthous ulcers 8.58

Coincidence with present study No. of rank in the study

Times (%) 5 3 3

Percent 50 30 30

*Present study.

†Axéll (1975).1

‡Bouquot (1986).20

§Shulman (2004).2

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ulation,1,18with higher prevalences than any patholog- ical change.

Other reports (not included in Table V) presenting age distribution characteristics15 or sampling condi- tions16 similar to those found in the dental school environment nevertheless failed to involve equivalent study population sizes. Even the study published by Knapp,10 which included 181 388 Army recruits, is limited to young adults between 18 and 22 years old.

On analyzing specific aspects of the present study, leukoedema is seen to be the most commonly recorded disorder, with a frequency twice that of the next rank- ing lesion (traumatic ulcers). Regarding the origin of the alterations, reactive and traumatic lesions showed the highest prevalence.Table IIshows that lesions of this kind account for almost half (44.26%) of the lesions reported (sum of relative percentages of categories II and III); on adding to this the factitious conditions (category V), those causative factors account for almost a half of the lesions found in this study. In addition, 7 of the first 10 lesions cited inTable III are associated with an irritative etiology: traumatic ulcer, irritative keratoses, traumatic erythema, morsicatio buccarum, labial melanotic macule, irritative hyperplasia, and smoking-associated melanosis. Assessment of irritative etiologies is of preventive importance, because ade- quate patient education and dental practice can help prevent many of these lesions. The control of local and external factors based on information, the elimination of local irritants, excellence in dental care for dental replacement, and adequate psychological and health orientation of compulsive habits and biologic and psy- chological dependencies such as tobacco smoking may contribute to the reduction of morbidity in these le- sions. Although minor recurrent aphthous ulcers affect a significant proportion of the population (8.58:1000 patients) and are intensely painful lesions, it is interest- ing to observe that minor recurrent aphthous ulcers do not seem to be a cause for dental consultation, because with the exception of our own series, such lesions are not among the most important disorders reported by the aforementioned epidemiological surveys. Although not included among the 10 most common lesions described by Shulman,2 the prevalence is similar, 8.9:1000 pa- tients.

Considering patient age or the chronology of lesion appearance, it is difficult to explain why some lesions such as morsicatio buccarum, irritative hyperplasia, or mucocele are prevalent at earlier ages— because the associated risk factors for the development of such lesions are not age dependent. Morsicatio buccarum, which was found to be the lesion with the youngest age index, can be attributable to psychological reactions to anxiety or self-aggression that are not necessarily char-

acteristic of any particular age group. In contrast, the lesions characteristic of older age ranges, such as those predominantly manifesting in patients more than 50 years of age, are associated with the wearing of partial or complete dentures, the latter in turn being related to tooth loss resulting from caries and periodontitis accu- mulating over time. Defects in the manufacture of partial or complete prostheses and the adaptive and progressive atrophic changes of the bone and mucosa of the maxillary processes explain the presence of epulis fissuratum, inflammatory papillary hyperplasia, and chronic atrophic candidiasis. Smoking also shows cu- mulative effects, resulting in melanosis in a percentage of cases proportional to the duration of the habit. Leu- koplakia, another lesion associated with smoking and other chronic irritants, also develops in proportion to the duration of exposure. Thus, it can be expected to be more common among older patients.

The results may be influenced by patient sex. In fact, some conditions are highly determined by sex.26In this report, the possibility of finding a lesion in males was 2 to 3 times greater than in females (Fig. 1andTable IV).

The analysis of this variable can be approached from different biologic, cultural, and social perspectives.

One possibility is that males are more exposed to risk factors, or alternatively, females may be genetically less susceptible to the development of oral lesions.

Another possible explanation is that males may be comparatively less sensitive to health matters, and their concept of well-being places little emphasis on oral or dental aspects. In contrast, women may be more health conscious and might extend such consciousness to younger family members, thus causing the lesions not to appear or advance as a result of earlier identification and treatment. An additional question is whether male adaptation to the environment leads to more manias, self-aggressive behavior, and neglect of oral health. It could also be that social, economic, and family roles prevent males from receiving care as often and timely as women, because the existing time availability may be different. Furthermore, although medical insurance and public health are available for covering the costs of health care, women may be more frequently benefited in that they combine opportunity with a positive atti- tude toward health and dental care. While the afore- mentioned observations are speculative, they may merit further study or clarification, with focused efforts on health attitudes generated by sex considerations and acknowledgment that there may be variations among different parts of the world or between countries.

Finally, it may be observed that from the public health care perspective, the majority of lesions identi- fied and their causes, in this and in other similar studies, are largely avoidable and can be controlled through

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education and measures targeted to both the general population and to dental professionals.

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Reprint requests:

José L. Castellanos, DDS Blvd. Campestre 506-301 Jardines del Moral León, Guanajuato, Mexico castellanosjose@hotmail.com

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