ORIGINAL Yadav ARTICLE et al
Influence of Environmental Tobacco Smoke on Gingival Pigmentation in Schoolchildren Rajendra Yadava/Vikas Deob/Pradeep Kumarc/Amit Hedad Purpose: To examine the relationship between environmental tobacco smoke (ETS) and oral pigmentation in schoolchildren. Materials and Methods: Oral photographs of 117 systemically healthy, nonsmoking children and young adults (aged 10 to 21 years) were randomly selected from two rural schools. Closed-ended questionnaires were designed for this age group and used to record answers given by the subjects. The subjects were divided into two groups based on age: group 1 (10 to 14 years) and group 2 (15 to 21 years). There were 58 subjects in group 1 and 59 in group 2. Gingival pigmentation was classified using the Melanin Index Score (MIS) into MIS-0 (no pigmentation), MIS-1 (solitary unit(s) of pigmentation in papillary gingiva) and MIS-2 (continuous band extending from 2 neighbouring solitary units). Results: In group 1, 17.24% of subjects displayed MIS-0 compared to only 5.08% in group 2. The difference between the groups was found to be statistically significant according to Student’s t-test (p < 0.001). In group 2, 38.98% of subjects showed MIS-2 as compared to only 17.24% subjects in group 1. Conclusion: Despite the relatively small sample size, the results of the present study confirmed previously reported findings that ETS has an influence on both the prevalence and the severity of gingival pigmentation. Key words: children, gingival pigmentation, tobacco smoke Oral Health Prev Dent 2015;13:407-410 doi: 10.3290/j.ohpd.a33918
M
elanin pigmentation is the most common form of discolouration of the oral mucosa and may have a negative impact on the appearance.13 Several local and systemic causes of gingival pigmentation have been recognised and broadly classified into localised and generalised pigmentations. The latter may be further subclassified on the basis of its association with genetic conditions, drugs, endocrine conditions and postinflammatory conditions.8 A high prevalence of oral pigmentation has been observed in Indians (89%), whereas low prevalences have been reported in Europeans (15%).16,19 The intensity and distribution of racial pigmentation of the oral mucosa is variable, not only between races, but also between different individuals of the same race.21 a
Periodontologist in Private Practice, Jaipur, India. Performed the experiments in partial fulfillment of requirements for a degree.
b
Assistant Professor, Government Medical College, Jodhpur, India. Designed the study, prepared and proofread the manuscript.
c
Reader, Rajasthan Dental College and Hospital, Jaipur, India. Helped with the introduction and discussion.
d
Reader, Teerthanker Mahaveer Dental College and Research Centre, Moradabad, India. Performed statistical analysis.
Correspondence: Assistant Professor Vikas Deo, Government Medical College, Jodhpur, 224, Padmawati B, Kings Road, Jaipur, India. Tel: +91-995-099-1918. Email: [email protected]
Vol 13, No 5, 2015
Submitted for publication: 04.10.13; accepted for publication: 05.10.13
Physiological pigmentation is probably genetically determined, but the degree of pigmentation is also partially related to mechanical, chemical and physical stimulation.10 In darker skinned people, oral pigmentations are more prevalent, but there is no difference in the number of melanocytes between fair-skinned and dark-skinned individuals. The variation is related to differences in the activity of melanocytes.21 Previous epidemiological investigations on oral melanin pigmentation in dark-skinned ethnic groups have been undertaken without any consideration of tobacco habits,16 although tobacco smoking has been found to be associated with oral melanin pigmentation.23,28 In an epidemiological study, 21.5% of the smokers had clinically visible melanin pigmentation as compared to only 3% among nonsmokers.5 Gingival pigmentation has also been examined in terms of its association with smoking in different populations and ethnicities, e.g. in Turkey,28 Sweden,23 Israel,25 Japan and3,15 Thailand and Malaysia.16 In these studies, excessive melanin pigmentation was found to be related to smoking. Thus, smoking may stimulate melanin production in gingival tissue. The stimulatory effect could be instigated by a high affinity of melanin to nicotine9 and benzopyrene22 in tobacco smoke. Additionally, a
407
Yadav et al
Fig 1 MIS score 1.
Fig 2 MIS score 2.
dose-response relationship has also been observed between smoking and gingival pigmentation3,5 and the disappearance of gingival pigmentation following reduction in smoking has also been reported.18 These findings suggest a causal relationship between smoking and gingival pigmentation. A relationship between passive smoking and some side effects such as appearance of childhood asthma,11 caries,1 spontaneous abortion,12 periodontal disease,4 children’s behavioural problems and childhood cancers6 has been extensively reported. Thus, children may suffer from environmental tobacco smoke (ETS); the home is the most important site of this exposure.6 Recently, researchers have also focused on increased prevalence of melanin pigmentation in children whose parents (fathers, mothers or both) are smokers.24 The aim of the present study was therefore to assess the relationship between passive smoking/ETS and oral pigmentation in children and young adults in a rural population.
with gingival pigmentation (minocycline, anti-malarials etc) within the past 6 months. Two hundred six subjects were initially evaluated. Of these, 131 subjects had parents (fathers, mothers or both) who smoked and were included in the study. However, 14 subjects were excluded based on the exclusion criteria mentioned above, thereby leaving a final study sample of 117 subjects. The study protocol was approved by the ethics committee of Rajasthan Dental College, Jaipur. The subjects were divided into two groups on the basis of age: group 1 (10 to 14 years) and group 2 (15 to 21 years). Out of the final study sample of 117 subjects, 58 subjects were in group 1 and 59 subjects in group 2.
MATERIALS AND METHODS Oral photographs of 206 systemically healthy, nonsmoking children and young adults (aged 10 to 21 years) were taken randomly from two rural government schools. Every effort was taken to recruit the children with similar skin colour based on the skin index.20 All the subjects included were from the same ethnicity, race and socioeconomic group. Closed-ended questionnaires designed for this age group were used to record answers given by the subjects. Intraoral photographs of the gingiva were taken in a standardised manner after adjusting for white balance using a Sony DSC-T 700 camera (Sony Electronics; San Diego, CA, USA) in pre-set automatic macro-mode to evaluate gingival pigmentation. The exclusion criteria were: gingival pigmentation of haemoglobin, melanoid, carotene or any other systemic cause; amalgam restoration adjacent to gingiva; a history of drugs that may interfere
408
Evaluation of melanin pigmentation Gingival pigmentation was assessed using standardised oral photographs. Brownish or black pigmentation in gingiva was classified using the Melanin Index Score (MIS).19 The scoring system was as follows: MIS-0: no pigmentation; MIS-1: solitary unit(s) of pigmentation in papillary gingiva without formation of continuous band between solitary units (Fig 1); MIS2: at least one unit of formation of continuous band extending from 2 neighbouring solitary units (Fig 2). The reliability of this method was evaluated on the basis of inter-examiner agreement. Two examiners who did not know about the passive smoking status of the subjects independently reviewed the same photographs. There was no statistically significant disagreement between examiners.
RESULTS In group 1, 17.2% of subjects did not show any type of pigmentation as compared to only 5.1% in group 2. The difference between the groups was found to be statistically significant as assessed by Stu-
Oral Health & Preventive Dentistry
Yadav et al
dent’s t-test (p < 0.001). Similarly, in group 2, 39% of subjects showed a continuous band of pigmentation as compared to only 17.2% of subjects in group 1. Again, the difference between the groups was found to be statistically significant (p < 0.001). However, when individuals with solitary units were compared, there was no statistically significant difference between the groups (65.5% in group 1 vs 55.9% in group 2). It was observed that 15.4% (n = 2) of the subjects with MIS-0 were exposed to smoke from > 5 packs per day, whereas 53.8% (n = 7) of MIS-0 were exposed to smoke from ≤ 2 packs per day. 30.8% (n = 4) of the subjects with MIS-0 were exposed to smoke from 3 to 5 packs per day. Among subjects with MIS-1, 15.5% (n = 11) were exposed to smoke from ≤ 2 packs per day, 53.5% (n = 28) were exposed to smoke from 3–5 packs/day and 45.1% (n = 32) were exposed to > 5 packs/day. Of subjects with MIS-2, 51.5% (n = 17) of were exposed to smoke from > 5 packs per day, whereas only 15.6% (n = 5) were exposed to smoke from ≤ 2 packs per day. 33.3% (n = 11) of the subjects with MIS-2 were exposed to smoke from 3–5 packs per day.
DISCUSSION Melanin pigmentation is caused by melanin granules – produced in melanosomes of melanocytes – in gingival tissue.17 Melanin is synthesised from tyrosine and dihydroxyphenylalanine (DOPA) via dopaquinone by the oxidation of tyrosinase.14 To date, there are few reports in the literature regarding potential stimulants of melanin production in gingiva; for instance, a high affinity of tobacco constituents such as nicotine9 and benzopyrene22 to melanin could be one factor. In the oral mucosa, polycyclic amines present in tobacco (benzopyrene, nicotine) as well as free radicals produced by the use of tobacco stimulate the melanocytes to produce melanin.26 Two pathways exist by which stimulatory substances from ETS may enter melanocytes in the gingiva of children. One route involves penetration through oral mucosa: stimulatory agents derived from ETS can be carried by saliva and might reach melanocytes through the gingival epithelium. However, the majority of ETS is aspirated through the nose and may reach the gingival tissue via the bloodstream. As breathing in children has a higher frequency than in adults, this may explain why ETS is more harmful to children.27 Although melanin pigmentation varies in prevalence among different races and ethnic groups –
Vol 13, No 5, 2015
for example, the prevalence is higher in Asian populations (34.6%)15 than in Jews (11.1%)25 – clinically visible oral melanin pigmentation is most frequent in dark-skinned ethnic groups. Among Australian Aborigines and dark-skinned Brazilians, nearly all individuals show oral melanin pigmentation, sometimes already in early childhood.2,7 This brown or black pigmentation has been considered to be due solely to genetic factors. However, studies performed during the last decade in more light-skinned adult populations have shown that the main cause of oral melanin pigmentation in Sweden and Japan is tobacco smoking.3,5 Gingival pigmentation in Japanese children has also been described,15 and melanin pigmentation of oral mucosa was detected in 13.5% of Israeli children 6 to 10 years of age.2 In the present study, the duration of direct exposure to cigarette smoke was not possible to determine (it could not be determined with certainty that the children knew or would be able to report the exact duration they had seen their parents smoking), but in all cases of the passive smoker group there was at least one person who smoked in the presence of the child. Therefore, the assumption was that these children had been affected by smoke at home for a long time. A cause-and-effect relationship seems to exist between cigarette smoke and pigmentation; for instance, the more time elapsed since quitting smoking, the more pigmentation disappears. In the present study, the duration of smoke exposure was found to be directly related to the prevalence and severity of the pigmentation. The observed dose-response relationship may also indicate high sensitivity of melanocytes in gingival tissue to tobacco smoking. In spite of the fact that melanocytes are normal cells in the human gingiva and that a relationship exists between skin colour and gingival pigmentation, gingival pigmentation in children is not necessarily a sign of their parents smoking. However, gingival pigmentation in children may serve as an alarm to parents who smoke. Because parents may perceive a social stigma associated with smoking, they may underreport it; however, it has been suggested that 10- to 11-yearold children may be more reliable than the parents in terms of providing truthful information on parental smoking.13 The present findings confirm that the severity of pigmentation is directly related to the number of packs of cigarettes smoked per day by the parents/ people in the subjects’ environment. The results are comparable to those observed in an Indian
409
Yadav et al
population survey.24 Another study15 that examined the relationship between melanin pigmentation in the gingiva of children and exposure to ETS also yielded similar results. The study had some limitations as well. The sample size was small, considering that it was an epidemiologic study. Biochemical analysis (level of continine in urine) would have provided a more objective variable of ETS, as it could be argued that the parents’ report of their smoking habits is to a large extent unreliable.
CONCLUSION Despite relatively small sample size, the results of the present study confirmed the previously reported findings that environmental tobacco smoke has an influence on both the prevalence and the severity of gingival pigmentation.
ACKNOWLEDGEMENT The authors wish to thank the children who helped us by participating in this study.
REFERENCES 1. Aligne CA, Moss ME, Auinger P, Weitzman M. Association of pediatric dental caries with passive smoking. JAMA 2003;289:1258–1264. 2. Amir E, Gorsky M, Muchner A, Sarnat H, Gat H. Physiologic pigmentation of oral mucosa in Israeli children. Oral Surg Oral Med Oral Pathol 1991;71:396–398. 3. Araki S, Murata K, Ushio K, Sakai R. Dose-response relationship between tobacco consumption and melanin pigmentation in the attached gingiva. Arch Environ Health 1983; 38:375–378. 4. Arbes SJ Jr, Agustsdottir H, Slade GD. Enviromental tobacco smoke and periodontal disease in the United States. Am J Public Health 2001;91:253–257. 5. Axéll T, Hedin CA. Epidemiologic study of excessive oral melanin pigmentation with special reference to the influence of tobacco habits. Scand J Dent Res1982;90:434–442. 6. Boyaci H, Etiler N, Duman C, Basyigit I, Pala A. Enviromental tobacco smoke exposure in school children: parent report and urine cotinine measures. Pediatr Int 2006;48: 382–389. 7. Brown T. Oral pigmentation in the Aborigines of Kalumbura, northwest Australia. Arch Orat Biol 1964;9:555–564. 8. Ciçek Y, Ertaş U. The normal and pathological pigmentation of oral mucous membrane: a review. J Contemp Dent Pract 2003;4:76–86. 9. Claffey DJ, Stout PR, Ruth JA. 3H-nicotine, 3H-flunitrazepam, and 3H-cocaine incorporation into melanin: a model for the examination of drug-melanin interactions. J Anal Toxicol 2001;25:607–611.
410
10. Dummett CO. Clinical observation on pigment variations in healthy oral tissues in the Negro. J Dent Res 1945;24:7–13. 11. Fernando D, Martinez MD, Cline M. Increase incidence of asthma in children of smoking mothers. Pediatrics 1992;89:21–28. 12. George L, Granath F, Johansson AL, Annerén G, Cnattingius S. Enviromental tobacco smoke and risk of spontaneous abortion. Epidemiology 2006;17:500–505. 13. Hajifattahi F, Azarshab M, Haghgoo R, Lesan S. Evaluation of the relationship between passive smoking and oral pigmentation in children. J Dent (Tehran) 2010;7:119–123. 14. Halaban R, Cheng E, Svedine S, Aron R, Hebert DN. Proper folding and endoplasmic reticulum to golgi transport of tyrosinase are induced by its substrates, DOPA and tyrosine. J Biol Chem 2001;276 (15):11933–8. Epub 2000 Dec 20. 15. Hanioka T, Tanaka K, Ojima M, Yuuki K. Association of melanin pigmentation in the gingiva of children with parents who smoke. Pediatrics 2005;116:e186–190. 16. Hedin CA, Axéll T. Oral melanin pigmentation in 467 Thai and Malaysian people with special emphasis on smoker‘s melanosis. J Oral Pathol Med 1991;20:8–12. 17. Hedin CA, Larsson A. The ultrastructure of the gingival epithelium in smokers‘ melanosis. J Periodontal Res 1984; 19:177–190. 18. Hedin CA, Pindborg JJ, Axéll T. Disappearance of smoker’s melanosis after reducing smoking. J Oral Pathol Med 1993;22:228–230. 19. Hedin CA. Smokers’ melanosis. Occurrence and localization in the attached gingiva. Arch Dermatol 1977;113: 1533–1538. 20. Jahangiri L, Reinhardt SB, Mehra RV, Matheson PB. Relationship between tooth shade value and skin color: an observational study. J Prosthet Dent 2002;87:149–152. 21. Özbayrak S, Dumlu A, Ercalik-Yalcinkaya S. Treatment of melanin-pigmented gingiva and oral mucosa by CO2 laser. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90:14–15. 22. Roberto A, Larsson BS, Tjälve H. Uptake of 7, 12dimethylbenz(a)anthracene and benzo(a)pyrene in melanin-containing tissues. Pharmacol Toxicol 1996;79:92–99. 23. Salonen L, Axéll T, Helldén L. Occurrence of oral mucosal lesions, the influence of tobacco habits and an estimate of treatment time in an adult Swedish population. J Oral Pathol Med 1990;19:170–176. 24. Sridharan S, Ganiger K, Satyanarayana A, Rahul A, Shetty S. Effect of environmental tobacco smoke from smoker parents on gingival pigmentation in children and young adults: a cross-sectional study. J Periodontol 2011;82: 956–962. 25. Steigmann S. The relationship between physiologic pigmentation of the skin and oral mucosa in Yemenite Jews. Oral Surg Oral Med Oral Pathol 1965;19:32–38. 26. Szüts T, Olsson S, Lindquist NG, Ullberg S, Pilotti A, Enzell C. Long-term fate of [14C] nicotine in the mouse: retention in the bronchi, melanin-containing tissues and urinary bladder wall. Toxicology 1978;10:207–220. 27. Thaqi A, Franke K, Merkel G, Wichmann HE, Heinrich J. Biomarkers of exposure to passive smoking of school children: frequency and determinants. Indoor Air 2005;15:302–310. 28. Unsal E, Paksoy C, Soykan E, Elhan AH, Sahin M. Oral melanin pigmentation related to smoking in a Turkish population. Community Dent Oral Epidemiol 2001;29:272–277.
Oral Health & Preventive Dentistry
Influence of Environmental Tobacco Smoke on Gingival Pigmentation in Schoolchildren Rajendra Yadava/Vikas Deob/Pradeep Kumarc/Amit Hedad Purpose: To examine the relationship between environmental tobacco smoke (ETS) and oral pigmentation in schoolchildren. Materials and Methods: Oral photographs of 117 systemically healthy, nonsmoking children and young adults (aged 10 to 21 years) were randomly selected from two rural schools. Closed-ended questionnaires were designed for this age group and used to record answers given by the subjects. The subjects were divided into two groups based on age: group 1 (10 to 14 years) and group 2 (15 to 21 years). There were 58 subjects in group 1 and 59 in group 2. Gingival pigmentation was classified using the Melanin Index Score (MIS) into MIS-0 (no pigmentation), MIS-1 (solitary unit(s) of pigmentation in papillary gingiva) and MIS-2 (continuous band extending from 2 neighbouring solitary units). Results: In group 1, 17.24% of subjects displayed MIS-0 compared to only 5.08% in group 2. The difference between the groups was found to be statistically significant according to Student’s t-test (p < 0.001). In group 2, 38.98% of subjects showed MIS-2 as compared to only 17.24% subjects in group 1. Conclusion: Despite the relatively small sample size, the results of the present study confirmed previously reported findings that ETS has an influence on both the prevalence and the severity of gingival pigmentation. Key words: children, gingival pigmentation, tobacco smoke Oral Health Prev Dent 2015;13:407-410 doi: 10.3290/j.ohpd.a33918
M
elanin pigmentation is the most common form of discolouration of the oral mucosa and may have a negative impact on the appearance.13 Several local and systemic causes of gingival pigmentation have been recognised and broadly classified into localised and generalised pigmentations. The latter may be further subclassified on the basis of its association with genetic conditions, drugs, endocrine conditions and postinflammatory conditions.8 A high prevalence of oral pigmentation has been observed in Indians (89%), whereas low prevalences have been reported in Europeans (15%).16,19 The intensity and distribution of racial pigmentation of the oral mucosa is variable, not only between races, but also between different individuals of the same race.21 a
Periodontologist in Private Practice, Jaipur, India. Performed the experiments in partial fulfillment of requirements for a degree.
b
Assistant Professor, Government Medical College, Jodhpur, India. Designed the study, prepared and proofread the manuscript.
c
Reader, Rajasthan Dental College and Hospital, Jaipur, India. Helped with the introduction and discussion.
d
Reader, Teerthanker Mahaveer Dental College and Research Centre, Moradabad, India. Performed statistical analysis.
Correspondence: Assistant Professor Vikas Deo, Government Medical College, Jodhpur, 224, Padmawati B, Kings Road, Jaipur, India. Tel: +91-995-099-1918. Email: [email protected]
Vol 13, No 5, 2015
Submitted for publication: 04.10.13; accepted for publication: 05.10.13
Physiological pigmentation is probably genetically determined, but the degree of pigmentation is also partially related to mechanical, chemical and physical stimulation.10 In darker skinned people, oral pigmentations are more prevalent, but there is no difference in the number of melanocytes between fair-skinned and dark-skinned individuals. The variation is related to differences in the activity of melanocytes.21 Previous epidemiological investigations on oral melanin pigmentation in dark-skinned ethnic groups have been undertaken without any consideration of tobacco habits,16 although tobacco smoking has been found to be associated with oral melanin pigmentation.23,28 In an epidemiological study, 21.5% of the smokers had clinically visible melanin pigmentation as compared to only 3% among nonsmokers.5 Gingival pigmentation has also been examined in terms of its association with smoking in different populations and ethnicities, e.g. in Turkey,28 Sweden,23 Israel,25 Japan and3,15 Thailand and Malaysia.16 In these studies, excessive melanin pigmentation was found to be related to smoking. Thus, smoking may stimulate melanin production in gingival tissue. The stimulatory effect could be instigated by a high affinity of melanin to nicotine9 and benzopyrene22 in tobacco smoke. Additionally, a
407
Yadav et al
Fig 1 MIS score 1.
Fig 2 MIS score 2.
dose-response relationship has also been observed between smoking and gingival pigmentation3,5 and the disappearance of gingival pigmentation following reduction in smoking has also been reported.18 These findings suggest a causal relationship between smoking and gingival pigmentation. A relationship between passive smoking and some side effects such as appearance of childhood asthma,11 caries,1 spontaneous abortion,12 periodontal disease,4 children’s behavioural problems and childhood cancers6 has been extensively reported. Thus, children may suffer from environmental tobacco smoke (ETS); the home is the most important site of this exposure.6 Recently, researchers have also focused on increased prevalence of melanin pigmentation in children whose parents (fathers, mothers or both) are smokers.24 The aim of the present study was therefore to assess the relationship between passive smoking/ETS and oral pigmentation in children and young adults in a rural population.
with gingival pigmentation (minocycline, anti-malarials etc) within the past 6 months. Two hundred six subjects were initially evaluated. Of these, 131 subjects had parents (fathers, mothers or both) who smoked and were included in the study. However, 14 subjects were excluded based on the exclusion criteria mentioned above, thereby leaving a final study sample of 117 subjects. The study protocol was approved by the ethics committee of Rajasthan Dental College, Jaipur. The subjects were divided into two groups on the basis of age: group 1 (10 to 14 years) and group 2 (15 to 21 years). Out of the final study sample of 117 subjects, 58 subjects were in group 1 and 59 subjects in group 2.
MATERIALS AND METHODS Oral photographs of 206 systemically healthy, nonsmoking children and young adults (aged 10 to 21 years) were taken randomly from two rural government schools. Every effort was taken to recruit the children with similar skin colour based on the skin index.20 All the subjects included were from the same ethnicity, race and socioeconomic group. Closed-ended questionnaires designed for this age group were used to record answers given by the subjects. Intraoral photographs of the gingiva were taken in a standardised manner after adjusting for white balance using a Sony DSC-T 700 camera (Sony Electronics; San Diego, CA, USA) in pre-set automatic macro-mode to evaluate gingival pigmentation. The exclusion criteria were: gingival pigmentation of haemoglobin, melanoid, carotene or any other systemic cause; amalgam restoration adjacent to gingiva; a history of drugs that may interfere
408
Evaluation of melanin pigmentation Gingival pigmentation was assessed using standardised oral photographs. Brownish or black pigmentation in gingiva was classified using the Melanin Index Score (MIS).19 The scoring system was as follows: MIS-0: no pigmentation; MIS-1: solitary unit(s) of pigmentation in papillary gingiva without formation of continuous band between solitary units (Fig 1); MIS2: at least one unit of formation of continuous band extending from 2 neighbouring solitary units (Fig 2). The reliability of this method was evaluated on the basis of inter-examiner agreement. Two examiners who did not know about the passive smoking status of the subjects independently reviewed the same photographs. There was no statistically significant disagreement between examiners.
RESULTS In group 1, 17.2% of subjects did not show any type of pigmentation as compared to only 5.1% in group 2. The difference between the groups was found to be statistically significant as assessed by Stu-
Oral Health & Preventive Dentistry
Yadav et al
dent’s t-test (p < 0.001). Similarly, in group 2, 39% of subjects showed a continuous band of pigmentation as compared to only 17.2% of subjects in group 1. Again, the difference between the groups was found to be statistically significant (p < 0.001). However, when individuals with solitary units were compared, there was no statistically significant difference between the groups (65.5% in group 1 vs 55.9% in group 2). It was observed that 15.4% (n = 2) of the subjects with MIS-0 were exposed to smoke from > 5 packs per day, whereas 53.8% (n = 7) of MIS-0 were exposed to smoke from ≤ 2 packs per day. 30.8% (n = 4) of the subjects with MIS-0 were exposed to smoke from 3 to 5 packs per day. Among subjects with MIS-1, 15.5% (n = 11) were exposed to smoke from ≤ 2 packs per day, 53.5% (n = 28) were exposed to smoke from 3–5 packs/day and 45.1% (n = 32) were exposed to > 5 packs/day. Of subjects with MIS-2, 51.5% (n = 17) of were exposed to smoke from > 5 packs per day, whereas only 15.6% (n = 5) were exposed to smoke from ≤ 2 packs per day. 33.3% (n = 11) of the subjects with MIS-2 were exposed to smoke from 3–5 packs per day.
DISCUSSION Melanin pigmentation is caused by melanin granules – produced in melanosomes of melanocytes – in gingival tissue.17 Melanin is synthesised from tyrosine and dihydroxyphenylalanine (DOPA) via dopaquinone by the oxidation of tyrosinase.14 To date, there are few reports in the literature regarding potential stimulants of melanin production in gingiva; for instance, a high affinity of tobacco constituents such as nicotine9 and benzopyrene22 to melanin could be one factor. In the oral mucosa, polycyclic amines present in tobacco (benzopyrene, nicotine) as well as free radicals produced by the use of tobacco stimulate the melanocytes to produce melanin.26 Two pathways exist by which stimulatory substances from ETS may enter melanocytes in the gingiva of children. One route involves penetration through oral mucosa: stimulatory agents derived from ETS can be carried by saliva and might reach melanocytes through the gingival epithelium. However, the majority of ETS is aspirated through the nose and may reach the gingival tissue via the bloodstream. As breathing in children has a higher frequency than in adults, this may explain why ETS is more harmful to children.27 Although melanin pigmentation varies in prevalence among different races and ethnic groups –
Vol 13, No 5, 2015
for example, the prevalence is higher in Asian populations (34.6%)15 than in Jews (11.1%)25 – clinically visible oral melanin pigmentation is most frequent in dark-skinned ethnic groups. Among Australian Aborigines and dark-skinned Brazilians, nearly all individuals show oral melanin pigmentation, sometimes already in early childhood.2,7 This brown or black pigmentation has been considered to be due solely to genetic factors. However, studies performed during the last decade in more light-skinned adult populations have shown that the main cause of oral melanin pigmentation in Sweden and Japan is tobacco smoking.3,5 Gingival pigmentation in Japanese children has also been described,15 and melanin pigmentation of oral mucosa was detected in 13.5% of Israeli children 6 to 10 years of age.2 In the present study, the duration of direct exposure to cigarette smoke was not possible to determine (it could not be determined with certainty that the children knew or would be able to report the exact duration they had seen their parents smoking), but in all cases of the passive smoker group there was at least one person who smoked in the presence of the child. Therefore, the assumption was that these children had been affected by smoke at home for a long time. A cause-and-effect relationship seems to exist between cigarette smoke and pigmentation; for instance, the more time elapsed since quitting smoking, the more pigmentation disappears. In the present study, the duration of smoke exposure was found to be directly related to the prevalence and severity of the pigmentation. The observed dose-response relationship may also indicate high sensitivity of melanocytes in gingival tissue to tobacco smoking. In spite of the fact that melanocytes are normal cells in the human gingiva and that a relationship exists between skin colour and gingival pigmentation, gingival pigmentation in children is not necessarily a sign of their parents smoking. However, gingival pigmentation in children may serve as an alarm to parents who smoke. Because parents may perceive a social stigma associated with smoking, they may underreport it; however, it has been suggested that 10- to 11-yearold children may be more reliable than the parents in terms of providing truthful information on parental smoking.13 The present findings confirm that the severity of pigmentation is directly related to the number of packs of cigarettes smoked per day by the parents/ people in the subjects’ environment. The results are comparable to those observed in an Indian
409
Yadav et al
population survey.24 Another study15 that examined the relationship between melanin pigmentation in the gingiva of children and exposure to ETS also yielded similar results. The study had some limitations as well. The sample size was small, considering that it was an epidemiologic study. Biochemical analysis (level of continine in urine) would have provided a more objective variable of ETS, as it could be argued that the parents’ report of their smoking habits is to a large extent unreliable.
CONCLUSION Despite relatively small sample size, the results of the present study confirmed the previously reported findings that environmental tobacco smoke has an influence on both the prevalence and the severity of gingival pigmentation.
ACKNOWLEDGEMENT The authors wish to thank the children who helped us by participating in this study.
REFERENCES 1. Aligne CA, Moss ME, Auinger P, Weitzman M. Association of pediatric dental caries with passive smoking. JAMA 2003;289:1258–1264. 2. Amir E, Gorsky M, Muchner A, Sarnat H, Gat H. Physiologic pigmentation of oral mucosa in Israeli children. Oral Surg Oral Med Oral Pathol 1991;71:396–398. 3. Araki S, Murata K, Ushio K, Sakai R. Dose-response relationship between tobacco consumption and melanin pigmentation in the attached gingiva. Arch Environ Health 1983; 38:375–378. 4. Arbes SJ Jr, Agustsdottir H, Slade GD. Enviromental tobacco smoke and periodontal disease in the United States. Am J Public Health 2001;91:253–257. 5. Axéll T, Hedin CA. Epidemiologic study of excessive oral melanin pigmentation with special reference to the influence of tobacco habits. Scand J Dent Res1982;90:434–442. 6. Boyaci H, Etiler N, Duman C, Basyigit I, Pala A. Enviromental tobacco smoke exposure in school children: parent report and urine cotinine measures. Pediatr Int 2006;48: 382–389. 7. Brown T. Oral pigmentation in the Aborigines of Kalumbura, northwest Australia. Arch Orat Biol 1964;9:555–564. 8. Ciçek Y, Ertaş U. The normal and pathological pigmentation of oral mucous membrane: a review. J Contemp Dent Pract 2003;4:76–86. 9. Claffey DJ, Stout PR, Ruth JA. 3H-nicotine, 3H-flunitrazepam, and 3H-cocaine incorporation into melanin: a model for the examination of drug-melanin interactions. J Anal Toxicol 2001;25:607–611.
410
10. Dummett CO. Clinical observation on pigment variations in healthy oral tissues in the Negro. J Dent Res 1945;24:7–13. 11. Fernando D, Martinez MD, Cline M. Increase incidence of asthma in children of smoking mothers. Pediatrics 1992;89:21–28. 12. George L, Granath F, Johansson AL, Annerén G, Cnattingius S. Enviromental tobacco smoke and risk of spontaneous abortion. Epidemiology 2006;17:500–505. 13. Hajifattahi F, Azarshab M, Haghgoo R, Lesan S. Evaluation of the relationship between passive smoking and oral pigmentation in children. J Dent (Tehran) 2010;7:119–123. 14. Halaban R, Cheng E, Svedine S, Aron R, Hebert DN. Proper folding and endoplasmic reticulum to golgi transport of tyrosinase are induced by its substrates, DOPA and tyrosine. J Biol Chem 2001;276 (15):11933–8. Epub 2000 Dec 20. 15. Hanioka T, Tanaka K, Ojima M, Yuuki K. Association of melanin pigmentation in the gingiva of children with parents who smoke. Pediatrics 2005;116:e186–190. 16. Hedin CA, Axéll T. Oral melanin pigmentation in 467 Thai and Malaysian people with special emphasis on smoker‘s melanosis. J Oral Pathol Med 1991;20:8–12. 17. Hedin CA, Larsson A. The ultrastructure of the gingival epithelium in smokers‘ melanosis. J Periodontal Res 1984; 19:177–190. 18. Hedin CA, Pindborg JJ, Axéll T. Disappearance of smoker’s melanosis after reducing smoking. J Oral Pathol Med 1993;22:228–230. 19. Hedin CA. Smokers’ melanosis. Occurrence and localization in the attached gingiva. Arch Dermatol 1977;113: 1533–1538. 20. Jahangiri L, Reinhardt SB, Mehra RV, Matheson PB. Relationship between tooth shade value and skin color: an observational study. J Prosthet Dent 2002;87:149–152. 21. Özbayrak S, Dumlu A, Ercalik-Yalcinkaya S. Treatment of melanin-pigmented gingiva and oral mucosa by CO2 laser. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90:14–15. 22. Roberto A, Larsson BS, Tjälve H. Uptake of 7, 12dimethylbenz(a)anthracene and benzo(a)pyrene in melanin-containing tissues. Pharmacol Toxicol 1996;79:92–99. 23. Salonen L, Axéll T, Helldén L. Occurrence of oral mucosal lesions, the influence of tobacco habits and an estimate of treatment time in an adult Swedish population. J Oral Pathol Med 1990;19:170–176. 24. Sridharan S, Ganiger K, Satyanarayana A, Rahul A, Shetty S. Effect of environmental tobacco smoke from smoker parents on gingival pigmentation in children and young adults: a cross-sectional study. J Periodontol 2011;82: 956–962. 25. Steigmann S. The relationship between physiologic pigmentation of the skin and oral mucosa in Yemenite Jews. Oral Surg Oral Med Oral Pathol 1965;19:32–38. 26. Szüts T, Olsson S, Lindquist NG, Ullberg S, Pilotti A, Enzell C. Long-term fate of [14C] nicotine in the mouse: retention in the bronchi, melanin-containing tissues and urinary bladder wall. Toxicology 1978;10:207–220. 27. Thaqi A, Franke K, Merkel G, Wichmann HE, Heinrich J. Biomarkers of exposure to passive smoking of school children: frequency and determinants. Indoor Air 2005;15:302–310. 28. Unsal E, Paksoy C, Soykan E, Elhan AH, Sahin M. Oral melanin pigmentation related to smoking in a Turkish population. Community Dent Oral Epidemiol 2001;29:272–277.
Oral Health & Preventive Dentistry
