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ORIGINAL ARTICLE Biopsied Lesions of the Gingiva in a Southern Indian Population – A Retrospective Study Kavitha P. Kam...

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ORIGINAL ARTICLE

Biopsied Lesions of the Gingiva in a Southern Indian Population – A Retrospective Study Kavitha P. Kamatha/M. Vidyab/Pradeep S. Anandc Purpose: To retrospectively analyse the frequency and distribution of various biopsied lesions of the gingiva among patients attending a dental teaching institution in Karnataka state in India. Materials and Methods: Data collected from 153 gingival biopsies referred to the Department of Oral Pathology, Yenepoya Dental College in Mangalore, Karnataka state, India during a 5-year period from 2004–2008 were utilised for the purpose of this study. Lesions were categorised by their type and analysed for age, sex and location. Results: Non-neoplastic lesions accounted for 51% while neoplastic and potentially malignant lesions accounted for 49% of the lesions. The most common non-neoplastic lesion was pyogenic granuloma (42.3%), the most common benign neoplasm was fibroma (34.5%) and the most common malignant lesion was squamous cell carcinoma (82.6%). Among all the lesions, the most common was squamous cell carcinoma (24.8% of all the lesions). Conclusions: Unlike in previous studies, squamous cell carcinoma was the most common gingival lesion. The proportion of malignant and potentially malignant lesions was also higher among subjects in the present study than in other populations. Hence, public oral health programmes need to be formulated to better tackle the burden of these diseases. Key words: fibroma, gingiva, neoplasms, pyogenic granuloma, squamous cell carcinoma Oral Health Prev Dent 2013; 11: 71-79

T

he gingiva is a common site for various pathological conditions affecting the oral cavity. Although the most common lesions affecting the gingiva are inflammatory conditions induced by dental plaque, it is also a common site for both benign and malignant neoplasms as well as other tumour-like lesions (Bataineh and Al-Dwairi, 2005). As these lesions vary in their aetiology and clinical behaviour, which often dictates the line of treatment, accurate diagnosis is essential for proper management of these conditions. Although the clinical diagnosis of these various lesions is made based upon changes

a

Senior Lecturer, Department of Oral Pathology, People’s Dental Academy, Bhanpur, Bhopal, Madhya Pradesh State, India.

b

Professor, Department of Oral Pathology, A. B. Shetty Memorial Institute of Dental Sciences, Deralakatte, Mangalore, Karnataka State, India.

c

Reader, Department of Periodontics, People’s College of Dental Sciences and Research Centre, Bhanpur, Bhopal, Madhya Pradesh State, India.

Correspondence: Kavitha P. Kamath, Department of Oral Pathology, People’s Dental Academy, Karond-Bhanpur Bypass Road, Bhanpur, Bhopal, Madhya Pradesh State, 462037, India. Tel: +91-887-1721397. Email: [email protected]

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Submitted for publication: 19.07.11; accepted for publication: 30.04.12

observed in the clinical features of gingiva, information regarding the frequency and distribution of these lesions will certainly be helpful in the diagnosis. Few studies have reported the prevalence and distribution of gingival lesions among various populations (Eversole and Rovin, 1972; Kfir et al, 1980; Stablein and Silverglade, 1985; Zain and Fei, 1990; Ababneh, 2006; Zhang et al, 2007; Buchner et al, 2010). While some of these studies have considered only the reactive lesions of the gingiva (Eversole and Rovin, 1972; Kfir et al, 1980; Zhang et al, 2007; Buchner et al, 2010), others have analysed neoplastic as well non-neoplastic gingival lesions (Stablein and Silverglade, 1985; Ababneh, 2006; Shamim et al, 2008). However, the terminologies and classification of gingival lesions have been different in these studies. Lesions resembling peripheral ossifying fibroma (POF) have in the past been termed as ‘peripheral fibroma with calcification’ (Kfir et al, 1980) and ‘calcifying fibroblastic granuloma’ (Zain and Fei, 1990). It has been considered as a reactive lesion by some authors (Eversole and Rovin, 1972; Kfir et al, 1980; Zhang et al, 2007; Buchner et al, 2010), while others (Stablein and Sil-

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verglade, 1985; Ababneh, 2006; Shamim et al, 2008) have considered it a neoplastic lesion. While some investigators have considered pyogenic granuloma (PG) and fibrous epulis to be different lesions (Kfir et al, 1980), other investigators have used the term pyogenic granuloma/gingival fibromatoid lesions to describe lesions like PG, fibrous epulis, peripheral gingival fibroma and sclerosing PG (Eversole and Rovin, 1972), and terms such as fibrous epulis and fibroepithelial polyp have also been described as different lesions (Zain and Fei, 1990). At present, there is very little data regarding gingival lesions among Indian subjects. A recent study reported on the prevalence and distribution of biopsied gingival lesions among patients attending a dental teaching institution in the neighbouring state of Kerala (Shamim et al, 2008). The aim of the present study was to retrospectively analyse the frequency and distribution of various biopsied lesions of the gingiva among patients attending a dental teaching institution in Karnataka state in India.

30% (n=46) Malignant lesions 51% (n=78) Non-neoplastic lesions

19% (n=29) Benign neoplasms

Fig 1  Frequency of different types of biopsied gingival lesions.

MATERIALS AND METHODS Data collected from the records of gingival biopsies referred to the Department of Oral Pathology, Yenepoya Dental College in Mangalore, Karnataka state, India during a 5-year period from 2004 to 2008 were utilised for the purpose of this study. Only records with adequate case histories were considered for the study purpose. Thus, data collected from 153 biopsies were utilised for the final analysis. Based on the histopathological examination, the lesions were classified as neoplastic or nonneoplastic. Neoplastic lesions were further categorised as either benign neoplasms or malignant lesions. The latter category included malignant neoplasms, as well as potentially malignant lesions. The lesions were subsequently analysed for age and sex distribution as well as the location and type of the lesion. Data entry was done using Microsoft Excel and statistical analysis was performed using SPSS Version 10. The chi-square test was used to analyse the site and gender distribution of the lesions.

ing 49% (n = 75) (Fig 1). Ninety-four of the biopsied lesions were from female patients and 59 were from males (male to female ratio of 1:1.59). The age of the patients ranged from 10 to 75 years. Table 1 shows the age and sex distribution of different types of lesions. Non-neoplastic lesions showed a peak incidence among subjects in the age group of 20 to 29 years, benign lesions among subjects in the age range of 10 to 39 years, and malignant lesions among subjects in the age range of 50 to 69 years. Site distribution of the lesions is shown in Table 2. Non-neoplastic lesions were more commonly reported from the maxilla (59%) while the neoplastic lesions were more common in the mandible (57.3%). However, among the neoplastic lesions, the benign neoplasms were more common in the maxilla and the malignant neoplasms were more common in the mandible.

Non-neoplastic lesions

RESULTS Among the 153 biopsy specimens, 78 (51%) were non-neoplastic lesions, while neoplastic and potentially malignant lesions accounted for the remain-

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Non-neoplastic lesions accounted for 51% of all lesions. The 78 non-neoplastic lesions were categorised into 10 types. The most frequent lesions in this category were the PG (42.3%) followed by fibrous hyperplasia (26.9%) and inflammatory hyper-

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Table 1 Age and sex distribution of different types of lesions Age groups

Non-neoplastic

Neoplastic

Total

Benign

Malignant*

Males

Females

Males

Females

Males

Females

0–9

1

1

0

0

0

0

2

10–19

0

3

3

3

0

0

9

20–29

6

19

2

4

0

0

31

30–39

6

11

3

4

0

0

24

40–49

2

10

2

1

4

1

20

50–59

2

7

2

2

8

8

29

60–69

2

5

1

1

7

11

27

≥70

1

2

1

0

6

1

11

Total

20

58

14

15

25

21

153

*Includes malignant and potentially malignant lesions.

Table 2 Site distribution of different types of lesions Type of lesion

Maxilla

Mandible

Non-neoplastic

46

32

Neoplastic

32

43

Benign

20

9

Malignant*

12

34

Total

78

75

*Includes malignant and potentially malignant lesions.

plasia (17.9%) (Table 3). The peak incidence of the non-neoplastic lesions was observed in the age group of 20 to 29 years (32.1%) followed by the age group of 30 to 39 years (21.8%) (Table 1). PG and fibrous hyperplasia, which were the most common lesions in this category, showed a peak incidence among patients in the age group of 20 to 29 years (Fig 2). Table 4 shows the distribution of non-neo-

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Table 3 Frequency of different types of non-neoplastic lesions Type of lesion

Frequency

Percentage

Inflammatory lesion

2

2.6

Pyogenic granuloma

33

42.3

Inflammatory hyperplasia

14

17.9

Hyperkeratosis

1

1.3

Non-specific ulceration

1

1.3

Lichen planus

2

2.6

Pigmented lesions

1

1.3

Pemphigus

2

2.6

Fibrous hyperplasia

21

26.9

Pemphigoid

1

1.3

Total

78

100.0

plastic lesions by gender and site. Out of the 78 lesions, 58 (74.4%) were from female patients and 20 (25.6%) from male patients (P < 0.001). Regarding the site of the lesions, 46 of the 78 nonneoplastic lesions were from the maxilla and 32 were from the mandible. However, these differences were not statistically significant. The jaw distribution of the individual lesions followed a similar pattern.

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18 Squamous cell carcinoma Pyogenic granuloma Fibrous hyperplasia Inflammatory hyperplasia Fibroma

16 14

Number of lesions

12 10 8 6 4 2 0

0–9

10 – 19

20 – 29

30 – 39 40 – 49 Age (years)

50 – 59

60 – 69

≥ 70

Fig 2  Age distribution of the most common gingival lesions biopsied from the study population. Table 4 Distribution of non-neoplastic lesions by site and gender Type of lesion

Gender

Site

Male

Female

P-value

Maxilla

Mandible

P-value

Inflammatory lesion

1

1

ns

1

1

ns

Pyogenic granuloma

11

22

ns

18

15

ns

Inflammatory hyperplasia

3

11

0.033

8

6

ns

Hyperkeratosis

1

0

*

0

1

*

Non-specific ulceration

1

0

*

0

1

*

Lichen planus

1

1

ns

2

0

*

Pigmented lesions

0

1

*

1

0

*

Pemphigus

0

2

*

2

0

*

Fibrous hyperplasia

2

19

0.05).

from males and 15 were from females. Regarding the site of the benign neoplasms, 20 (69%) were from the maxilla and 9 (31%) were from the mandible (P = 0.041). Fibroma, which accounted for 34.5% of the benign neoplasms, was more common among males while lesions such as POF and capillary haemangioma were reported almost exclusively in females. Lesions such as fibroma and capillary haemangioma were reported almost exclusively from the maxilla, while the other benign neoplasms were almost equally distributed between the two arches. Malignant lesions included malignant neoplasms, as well as potentially malignant lesions. The potentially malignant lesions included lesions that were histopathologically diagnosed as epithelial dysplasia. Squamous cell carcinoma (SCC) was the most common malignant lesion (n = 38) accounting for 82.6% of malignant and potentially malignant lesions and 50.7% of all neoplastic lesions (Table 7). All the malignant and potentially malig-

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nant lesions were reported among patients above 40 years of age with a peak incidence among subjects in the age range of 50 to 69 years (Table 1). Table 8 shows the distribution of malignant and potentially malignant lesions by gender and site. Of the 46 malignant and potentially malignant lesions, 25 were from males and 21 from females. Regarding the site of the malignant and potentially malignant lesions, 34 (73.9%) were from the mandible and 12 (26.1%) were from the maxilla (P = 0.001). SCC and epithelial dysplasia were more common among males, while verrucous carcinoma was more common among females. Regarding the site, the malignant neoplasms (SCC and verrucous carcinoma) were more commonly reported from the mandible, while the potentially malignant lesions were equally distributed between the 2 arches. Of the 38 cases of SCC, 33 were of the well-differentiated type, 4 were of the moderately differentiated type, and 1 was of the poorly differentiated type. Twenty-one cases were reported from males,

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Table 7 Frequency of different malignant and potentially malignant lesions Type of lesion

Frequency

%

Squamous cell carcinoma (well differentiated)

33

71.7

Squamous cell carcinoma (moderately differentiated)

4

8.7

Squamous cell carcinoma (poorly differentiated)

1

2.2

Verrucous carcinoma

4

8.7

Epithelial dysplasia

4

8.7

Total

46

100.0

Table 8 Distribution of malignant and potentially malignant lesions by gender and site Type of lesion

Gender

Site

Male

Female

P-value

Maxilla

Mandible

P-value

WD-SCC

20

13

ns

10

23

0.024

MD-SCC

1

3

ns

0

4

*

PD-SCC

0

1

*

0

1

*

Verrucous carcinoma

1

3

ns

0

4

*

Epithelial dysplasia

3

1

ns

2

2

ns

Total

25

21

ns

12

34

0.001

WD-SCC = Well-differentiated squamous cell carcinoma; MD-SCC = Moderately differentiated squamous cell carcinoma; PD-SCC = Poorly differentiated squamous cell carcinoma. *= statistical tests could not be performed; ns=not statistically significant (P > 0.05).

of which 20 were of the well-differentiated type and 1 was of the moderately differentiated type. Out of the 17 cases in females, 13 were of the well-differentiated type, 3 were moderately differentiated, and 1 was poorly differentiated. All the 10 cases reported from the maxilla were of the well-differentiated type.

DISCUSSION In the present study, the nature, frequency and distribution of 153 biopsied gingival lesions among patients attending a dental teaching institution in the south Indian state of Karnataka was analysed. Of the 153 lesions, 51% were non-neoplastic, while neoplastic and potentially malignant lesions accounted for the remaining 49% of the lesions. The most commonly biopsied non-neoplastic lesion was PG while the most commonly biopsied malig-

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nant and benign neoplastic lesions were SCC and fibroma, respectively. When compared with other similar studies, it was observed that the proportion of neoplastic and potentially malignant lesions was higher in the present study population. Recently, in a similar study conducted among patients attending a dental teaching institution in the neighbouring state of Kerala, it was reported that neoplastic lesions accounted for 24.5% of the gingival lesions (Shamim et al, 2008). However, in another study conducted among northern Jordanians, the prevalence of neoplastic lesions was only 9% (Ababneh, 2006). Stablein and Silverglade (1985), in their study of lesions of gingiva and alveolar mucosa, reported that neoplastic lesions accounted for 15% of gingival lesions and 13% of lesions of the alveolar mucosa. However, the distribution of individual neoplastic lesions was not reported in that study. In the present study, females were more commonly affected, with a male to female ratio of

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1:1.59. When the different types of lesions were considered, non-neoplastic lesions were more common among females, while the neoplastic lesions were almost equally distributed between the sexes with a slightly higher occurrence of malignant neoplasms among males. Although the differences in the gender distribution of non-neoplastic lesions observed in the present study were statistically significant, the differences in the gender distribution of the malignant lesions were not statistically significant. This may be due to the low number of lesions in this category. In the study reported by Shamim et al (2008), both neoplastic (benign as well as malignant) and non-neoplastic lesions were higher among females. Stablein and Silverglade (1985) had also reported a similar trend for gingival lesions. However, Ababneh (2006), in a study among Jordanian subjects, reported a higher incidence of non-neoplastic lesions among females, a higher incidence of malignant lesions among males and an equal distribution of benign neoplasms between both of the sexes. It was also observed that the malignant and potentially malignant lesions were reported exclusively among patients above 40 years of age, with a peak incidence among subjects in the age range of 50 to 69 years. The benign neoplasms were more common in individuals in the age range of 10 to 39 years and non-neoplastic lesions among individuals in the age range of 20 to 49 years. Shamim et al (2008) reported a peak incidence of non-neoplastic lesions among patients aged 20 to 29 years, benign neoplasms among patients aged 10 to 19 years, and malignant neoplasms among patients aged 40 to 49 years. In the study by Stablein and Silverglade (1985), non-neoplastic gingival lesions showed a peak incidence in subjects in the age group of 20 to 59 years, benign neoplasms in the age range of 10 to 29 years, and malignant neoplasms were reported almost exclusively in subjects above 49 years. The study among Jordanian subjects reported a peak incidence of non-neoplastic lesions and benign neoplasms among patients aged 20 to 29 years while the malignant lesions were reported among patients aged 30 to 79 years (Ababneh, 2006). Unlike in earlier studies (Ababneh, 2006; Shamim et al, 2008) where PG was the most common lesion, the most frequent lesion among patients in the present study was SCC, which accounted for 24.8% of all the lesions. Of the 38 cases of SCC, 28 were reported from the mandible and 10 from the maxilla; 21 cases were among males and

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17 were among females (male to female ratio was 1.24:1). SCC was also found exclusively among patients above the age of 40 years, with more cases reported among patients in the age range of 50 to 69 years. SCC is the most common malignant lesion occurring in the oral cavity, accounting for 90% of all oral malignancies. Studies have shown that oral SCC is a disease seen more among males, particularly above 40 years of age (Sasaki et al, 2005; Misra et al, 2009; Sharma et al, 2010). This trend was also observed in the present study. Sharma et al (2010), in their study on the epidemiological aspects of oral SCC in a northern Indian state, observed that the lesion was more common among males, particularly in the fourth and fifth decades of life. Most common intra-oral sites for SCC have been reported to be gingiva, buccal mucosa, and tongue and this site predilection appears to be related to the age group of subjects studied. While buccal mucosa and gingiva are common sites for oral SCC among older age groups, the tongue is more often the affected site among individuals below 40 years of age (Kuriakose et al, 1992; Sharma et al, 2010; Marocchio et al, 2010; Falaki et al, 2011). Studies in northern Indian populations have shown that the use of smokeless tobacco is prevalent among subjects with oral SCC and potentially malignant lesions (Misra et al, 2009; Sharma et al, 2010). Although the tobacco-related habits of subjects was not recorded in the present study, data from a nationwide survey conducted during the period 2005 to 2006 have shown that the prevalence of use of smokeless tobacco among males in Karnataka state was 21.3%, which was the highest among the 4 southern Indian states (Rooban et al, 2010). Hence, the large number of cases of SCC observed among gingival lesions in the study population is alarming and a study is now in progress to determine the patterns of oral SCC in this southern Indian population. Among the benign neoplasms, fibroma was the most common, accounting for 34.5% (n = 10) of the 29 benign neoplastic lesions. Of the 10 lesions, 7 were reported in males and regarding the site, 9 out of the 10 lesions were reported from the maxilla. In their study on reactive gingival lesions in a western Chinese population, Zhang et al reported that peripheral fibroma was more common among females with a predilection for occurrence in the maxilla (Zhang et al, 2007). However, Shamim et al (2008) reported an almost equal distribution of fibroma in terms of site and gender. In the present

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study, fibroma was reported in all age groups above 9 years. While age distribution of fibroma among their patients was not reported by Shamim et al (2008), Zhang et al (2007) reported that the lesion showed a peak incidence among subjects in the fourth to seventh decade of life. In previous similar studies, POF was reported to be the most common benign neoplasm (Ababneh, 2006; Shamim et al, 2008). However, in the present study, POF was the second most common benign neoplasm (27.6%, n = 8). Some authors consider POF (Eversole and Rovin, 1972; Kfir et al, 1980; Buchner et al, 2010) and peripheral fibroma (Zhang et al, 2007) reactive lesions and it has been suggested that POF and other reactive lesions such as PG may be considered progressive stages of the same pathology (Prasad et al, 2008). However, in the present study, as in some previous studies (Stablein and Silverglade, 1985; Ababneh, 2006; Shamim et al, 2008), both fibroma and POF were considered as benign neoplasms. Among the 78 non-neoplastic lesions, the most common were PG and fibrous hyperplasia. As in the present study, PG has been reported as the most common reactive gingival lesion in some populations (Ababneh, 2006; Shamim et al, 2008). However, in some other studies, fibrous hyperplasia was reported as the most common reactive gingival lesion (Kfir et al, 1980; Buchner et al, 2010). In the present study, PG accounted for 42.3% of all non-neoplastic lesions, which was lower than the 52.7% reported by Shamim et al (2008), but higher than the 30% reported by Ababneh (2006), 29.1% reported by Buchner et al (2010), and 19.76% reported by Zhang et al (2007). However, in the studies by Buchner et al (2010) and Zhang et al (2007), lesions like POF and peripheral fibroma, which were included among benign neoplasms in the present study, were also included among reactive lesions. Moreover, the sample size in the present study was considerably smaller than those in the studies by Buchner et al (2010) and Zhang et al (2007). Had lesions like fibroma and POF been included among non-neoplastic lesions in the present study, then the proportion of cases of PG among non-neoplastic lesions would have been 34.3%. In the present study, both PG and fibrous hyperplasia were most common among patients in the age group of 20 to 29 years, more common among females, and showed a predilection for occurrence in the maxilla. A similar trend was reported in other studies as well (Kfir et al, 1980; Stablein and Silverglade, 1985; Ababneh, 2006;

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Shamim et al, 2008; Buchner et al, 2010). In the study by Zhang et al (2007), although a similar trend was observed regarding age and sex predilection, PG showed a slightly higher predilection for occurrence in the mandible. A few authors have also reported fibrous hyperplasia to occur more commonly in the mandible than in the maxilla (Shamim et al, 2008; Buchner et al, 2010) and show a peak incidence in the fifth decade of life (Buchner et al, 2010). In a recent review of 137 cases of PG in a southern Indian population, it was observed that gingiva, more commonly the maxillary gingiva, was the site of 83% of the lesions. It was also reported that the lesion was more common among females, with a peak incidence in the third decade of life (Saravana, 2009). Similar patterns of occurrence of PG have been reported in other populations as well (Torres-Domingo et al, 2008; Al-Khateeb, 2009). PG is a common tumour-like lesion of the oral mucosa, which is considered to be non-neoplastic in nature (Neville et al, 2009). It most commonly involves the gingiva; this predilection for gingival involvement has been considered to be related to the anatomical nature of the gingiva and occurrence of irritational factors at this site (Eversole and Rovin, 1972). Although it occurs most commonly in the second and third decades of life, it can occur at any age, and even congenital forms have been reported (Willies-Jacobo et al, 2000). The term ‘pyogenic’ is considered to be a misnomer, as the lesion does not produce any pus (Ababneh, 2006). It is characterised by a high vascular proliferation, which is sometimes organised as lobular aggregates. Based on the lobular arrangement of capillaries at the base of the lesion, Mills et al (1980) proposed the term ‘lobular capillary haemangioma’ for PG. On account of its vascularity, the term ‘telangiectatic granuloma’ has also been suggested as being a more appropriate term for PG (Holmstrup and Reibel, 2003). Researchers have reported two types of PG based on the histologic appearance: lobular capillary haemangioma (LCH) type and non-LCH type (Epivatianos et al, 2005; Rezvani et al, 2010). These two types of PGs differ in the luminal diameter and number of blood vessels (Epivatianos et al, 2005), as well as in the proliferative activity of the endothelial cells (Rezvani et al, 2010). Although PGs are considered to be non-neoplastic, the LCH type PGs are currently categorised as vascular tumours under the classification scheme of the International Society for the Study of Vascular Anomalies (Neville et al, 2009).

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CONCLUSION Although comparison with other studies is difficult due to variations in terminologies and classification of gingival lesions, findings in the present study suggest that, when compared with other populations, the trends of gingival lesions are different in the studied population. In the present study, unlike in previous similar studies, it was observed that SCC was the most commonly biopsied gingival lesion. The proportion of malignant and potentially malignant lesions was also higher among subjects in the present study than in other populations. Hence, public oral health programmes need to be formulated to better tackle the burden of these diseases. As in previous studies, a female preponderance was observed in the present study as well, and this calls for more attention in the areas of dental awareness and motivation of these patients. However, as this study has evaluated only the gingival lesions among patients from a single region, the results of the study need to be interpreted with caution. As India is a country with diverse socioeconomic and life-style characteristics, further studies are needed to better understand the trends of oral SCC and other oral mucosal lesions in the state, as well as in other parts of the country.

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