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Table 2.

Summary of studies to define human buccal cell changes associated with smokeless tobacco and similar-use substances

No.First author (year) (ref.)Tobacco used or chewing behaviorBuccal cell change*,Remarks
Goral (1999) (64) Moist snuff Yes Significant buccal cell alterations were recorded in a study of buccal cells of smokeless tobacco users. 
  Chewing tobacco Yes  
  Dip tobacco Yes  
Ramaesh (1999) (65) Smoked tobacco Yes The effect of tobacco use on buccal mucosa was assessed by cytomorphometry of buccal cells. A significant increase was discovered for cells in all habit groups. There was a significant reduction in the cell diameter of the chewing group and the combined habit group compared with the control nonuser group. 
  Betel chewers with tobacco Yes  
  Smoke and chew Yes  
  Nontobacco users No  
Ozkul (1997) (66) Chewed maras powder Yes There was no difference in the micronuclei of buccal cells of subjects who smoked or chewed smokeless tobacco (maras powder). Buccal cells of both groups showed a higher frequency of micronuclei than nonusers (nonsmokers, nonchewers). 
  Smokers, no maras No  
  Nonsmokers, no maras Yes  
Roberts (1997) (67) Snuff Yes Comparative cytology of the oral cavity was conducted to define the effects of snuff users. The regular use of snuff caused an increase in the incidence of buccal cell micronuclei, loss of cell cohesion, and hyperkeratosis. 
Desai (1996) (68) Betel nut Yes The exfoliated oral mucosal cells had significantly higher numbers of micronuclei compared with those of healthy normal subjects having no chewing or smoking habit. 
  Pan masala Yes  
  Mava Yes  
Ghose (1995) (69) Tobacco smokers with Pika habit Yes In India, tobacco smokers with Pika habit showed higher frequency of micronuclei of buccal cells than tobacco chewers with Dungia habit. 
  Tobacco chewers with Dungia habit Yes  
Kayal (1993) (70) Areca nut Yes All groups studied (see listing) had a significantly higher frequency of micronuclei of buccal cells than nonusers from different parts of India. Patients with oral leukoplakia had a high incidence of micronucleated cells in spite of the fact they had stopped chewing months before collection of the oral mucosa cells. 
  Mava Yes  
  Tamol Yes  
  Tobacco with lime Yes  
  Dry snuff Yes  
  Masheri Yes  
  Tobacco Yes  
Stich (1992) (71) Reverse cigar smokers Yes An elevated frequency of micronuclei of buccal cells was documented for reverse cigar smokers and Khaini-tobacco chewers; no increase was observed for gudakhu users. 
  Khaini-tobacco chewers Yes  
  Gudakhu users No  
Das (1992) (72) Gudakhu Yes The incidence of micronuclei was increased in users, and the increased incidence was correlated with the period of use. There were no significant differences between men and women. 
10 Dave (1992) (73) Areca nut Yes A clinical study in India showed statistically significant increases in the frequencies of micronuclei among of chewers compared with controls. 
11 Adhvaryu (1991) (74) Mava Yes When compared with healthy controls, a clinical study showed a significant increase in micronuclei of buccal cells for all three groups studied (chewers free of oral disease, chewers with oral submucous fibrosis, and chewers with oral cancer). 
12 Dave (1991) (75) Pan masala Yes Buccal cells collected from the site where the pan masala was placed showed a statistically significant (P < 0.001) increase in micronuclei of buccal cells compared with nonconsuming controls. 
  Pan masala with tobacco Yes  
13 Nair (1991) (76) Betel quid with tobacco Yes Significantly elevated micronuclei frequencies of buccal cells were observed in the exposed groups compared with the control group. No correlation was seen among age, duration, and frequency of habits. 
  Tobacco with lime Yes  
14 Tolbert (1991) (77) Snuff Yes A study was conducted of subjects who use snuff at levels known to be associated with a significant increase in cancer risk. The prevalence of micronuclei was elevated in the snuff users compared with the nonusers (prevalence ratio = 2.4) and, to a lesser extent, at the contact site compared with a distal buccal site in the snuff users (prevalence ratios = 2-13). 
15 Livingston (1990) (78) Smokeless tobacco Yes Cytologic and cytogenetic studies were done to assess the prevalence of somatic cell genetic damage in 48 young adults (college students) equally divided into users and nonusers of smokeless tobacco. The frequency of micronuclei of buccal cells was significantly higher in users than nonusers (P = <0.01). 
16 Stich (1988) (79) Betel quid with tobacco Yes Remission of oral leukoplakias and micronuclei in tobacco/betel quid chewers treated with β-carotene and with β-carotene plus vitamin A. Remission and inhibition of new oral leukoplakias and reduction of micronuclei of mucosal cells occurred in the groups receiving β-carotene and β-carotene plus vitamin A during the continuous presence of carcinogens derived from tobacco and areca nut. 
17 Stich (1985a) (80) Snuff Yes A pilot β-carotene intervention trial with inuits using smokeless tobacco. β-Carotene seemed to be an efficient inhibitor of micronuclei formation in buccal cells of snuff users who do not suffer from any vitamin A deficiency and who had normal levels of retinol. 
18 Stich (1985b) (81) Areca nut Yes Defined the frequency of micronuclei of buccal cells from areca nut and/or tobacco users. When compared with subjects who used areca nut only, all others (see listing to left) showed a significant increase in micronuclei frequency. Authors review critical buccal cell assay variables and statistical methodologies to be used in future large-scale screening programs. 
  Areca nut + lime + betel leaf Yes  
  Areca nut + lime + betel leaf + tobacco Yes  
  Tobacco + lime + ash + oil Yes  
  Tobacco + lime Yes  
  Snuff Yes  
19 Stich (1984a) (82) Betel (areca) nut/tobacco chewers Yes The frequency of exfoliated cells with micronuclei in buccal mucosa swabs was used to estimate the protective effect of vitamin A, β-carotene, and canthaxanthin on the buccal mucosa of betel (areca) nut/tobacco chewers. The betel (areca) nut/tobacco chewers served as their own controls. Following a 9-week ingestion of vitamin A and β-carotene the frequency of micronuclei-positive cells decreased significantly. 
20 Stich (1984b) (83) Betel nut and tobacco Yes Reduction with vitamin A and β-carotene administration of proportion of micronuclei in Asian betel nut and tobacco chewers. 
21 Stich (1983) (84) Betel nut (“pan”) Yes The frequency of micronuclei of buccal cells was significantly elevated in all examined betel quid chewers. The betel nut/tobacco mixture of a “pan” seems to be more genotoxic than the chewing of raw betel nut alone. Khaini tobacco only produced less micronuclei in cells than the betel nut with or without tobacco. 
  Betel nut and tobacco Yes  
  Khaini tobacco only Yes  
22 Stich (1982a) (85) Betel quid Yes Elevated frequency of micronuclei in buccal cells of individuals at high risk for oral cancer-betel quid chewers. The micronuclei frequency was lower among individuals chewing a raw betel nut, betel leaf, and lime mixture compared with those using quids with tobacco, betel nut, lime, or betel leaf. 
23 Stich (1982b) (86) Betel quid Yes The frequency of micronuclei of buccal cells in all three groups of chewers compared with a group of nonchewing subjects. 
  Khaini (tobacco and lime) Yes  
  Raw betel nut Yes  
No.First author (year) (ref.)Tobacco used or chewing behaviorBuccal cell change*,Remarks
Goral (1999) (64) Moist snuff Yes Significant buccal cell alterations were recorded in a study of buccal cells of smokeless tobacco users. 
  Chewing tobacco Yes  
  Dip tobacco Yes  
Ramaesh (1999) (65) Smoked tobacco Yes The effect of tobacco use on buccal mucosa was assessed by cytomorphometry of buccal cells. A significant increase was discovered for cells in all habit groups. There was a significant reduction in the cell diameter of the chewing group and the combined habit group compared with the control nonuser group. 
  Betel chewers with tobacco Yes  
  Smoke and chew Yes  
  Nontobacco users No  
Ozkul (1997) (66) Chewed maras powder Yes There was no difference in the micronuclei of buccal cells of subjects who smoked or chewed smokeless tobacco (maras powder). Buccal cells of both groups showed a higher frequency of micronuclei than nonusers (nonsmokers, nonchewers). 
  Smokers, no maras No  
  Nonsmokers, no maras Yes  
Roberts (1997) (67) Snuff Yes Comparative cytology of the oral cavity was conducted to define the effects of snuff users. The regular use of snuff caused an increase in the incidence of buccal cell micronuclei, loss of cell cohesion, and hyperkeratosis. 
Desai (1996) (68) Betel nut Yes The exfoliated oral mucosal cells had significantly higher numbers of micronuclei compared with those of healthy normal subjects having no chewing or smoking habit. 
  Pan masala Yes  
  Mava Yes  
Ghose (1995) (69) Tobacco smokers with Pika habit Yes In India, tobacco smokers with Pika habit showed higher frequency of micronuclei of buccal cells than tobacco chewers with Dungia habit. 
  Tobacco chewers with Dungia habit Yes  
Kayal (1993) (70) Areca nut Yes All groups studied (see listing) had a significantly higher frequency of micronuclei of buccal cells than nonusers from different parts of India. Patients with oral leukoplakia had a high incidence of micronucleated cells in spite of the fact they had stopped chewing months before collection of the oral mucosa cells. 
  Mava Yes  
  Tamol Yes  
  Tobacco with lime Yes  
  Dry snuff Yes  
  Masheri Yes  
  Tobacco Yes  
Stich (1992) (71) Reverse cigar smokers Yes An elevated frequency of micronuclei of buccal cells was documented for reverse cigar smokers and Khaini-tobacco chewers; no increase was observed for gudakhu users. 
  Khaini-tobacco chewers Yes  
  Gudakhu users No  
Das (1992) (72) Gudakhu Yes The incidence of micronuclei was increased in users, and the increased incidence was correlated with the period of use. There were no significant differences between men and women. 
10 Dave (1992) (73) Areca nut Yes A clinical study in India showed statistically significant increases in the frequencies of micronuclei among of chewers compared with controls. 
11 Adhvaryu (1991) (74) Mava Yes When compared with healthy controls, a clinical study showed a significant increase in micronuclei of buccal cells for all three groups studied (chewers free of oral disease, chewers with oral submucous fibrosis, and chewers with oral cancer). 
12 Dave (1991) (75) Pan masala Yes Buccal cells collected from the site where the pan masala was placed showed a statistically significant (P < 0.001) increase in micronuclei of buccal cells compared with nonconsuming controls. 
  Pan masala with tobacco Yes  
13 Nair (1991) (76) Betel quid with tobacco Yes Significantly elevated micronuclei frequencies of buccal cells were observed in the exposed groups compared with the control group. No correlation was seen among age, duration, and frequency of habits. 
  Tobacco with lime Yes  
14 Tolbert (1991) (77) Snuff Yes A study was conducted of subjects who use snuff at levels known to be associated with a significant increase in cancer risk. The prevalence of micronuclei was elevated in the snuff users compared with the nonusers (prevalence ratio = 2.4) and, to a lesser extent, at the contact site compared with a distal buccal site in the snuff users (prevalence ratios = 2-13). 
15 Livingston (1990) (78) Smokeless tobacco Yes Cytologic and cytogenetic studies were done to assess the prevalence of somatic cell genetic damage in 48 young adults (college students) equally divided into users and nonusers of smokeless tobacco. The frequency of micronuclei of buccal cells was significantly higher in users than nonusers (P = <0.01). 
16 Stich (1988) (79) Betel quid with tobacco Yes Remission of oral leukoplakias and micronuclei in tobacco/betel quid chewers treated with β-carotene and with β-carotene plus vitamin A. Remission and inhibition of new oral leukoplakias and reduction of micronuclei of mucosal cells occurred in the groups receiving β-carotene and β-carotene plus vitamin A during the continuous presence of carcinogens derived from tobacco and areca nut. 
17 Stich (1985a) (80) Snuff Yes A pilot β-carotene intervention trial with inuits using smokeless tobacco. β-Carotene seemed to be an efficient inhibitor of micronuclei formation in buccal cells of snuff users who do not suffer from any vitamin A deficiency and who had normal levels of retinol. 
18 Stich (1985b) (81) Areca nut Yes Defined the frequency of micronuclei of buccal cells from areca nut and/or tobacco users. When compared with subjects who used areca nut only, all others (see listing to left) showed a significant increase in micronuclei frequency. Authors review critical buccal cell assay variables and statistical methodologies to be used in future large-scale screening programs. 
  Areca nut + lime + betel leaf Yes  
  Areca nut + lime + betel leaf + tobacco Yes  
  Tobacco + lime + ash + oil Yes  
  Tobacco + lime Yes  
  Snuff Yes  
19 Stich (1984a) (82) Betel (areca) nut/tobacco chewers Yes The frequency of exfoliated cells with micronuclei in buccal mucosa swabs was used to estimate the protective effect of vitamin A, β-carotene, and canthaxanthin on the buccal mucosa of betel (areca) nut/tobacco chewers. The betel (areca) nut/tobacco chewers served as their own controls. Following a 9-week ingestion of vitamin A and β-carotene the frequency of micronuclei-positive cells decreased significantly. 
20 Stich (1984b) (83) Betel nut and tobacco Yes Reduction with vitamin A and β-carotene administration of proportion of micronuclei in Asian betel nut and tobacco chewers. 
21 Stich (1983) (84) Betel nut (“pan”) Yes The frequency of micronuclei of buccal cells was significantly elevated in all examined betel quid chewers. The betel nut/tobacco mixture of a “pan” seems to be more genotoxic than the chewing of raw betel nut alone. Khaini tobacco only produced less micronuclei in cells than the betel nut with or without tobacco. 
  Betel nut and tobacco Yes  
  Khaini tobacco only Yes  
22 Stich (1982a) (85) Betel quid Yes Elevated frequency of micronuclei in buccal cells of individuals at high risk for oral cancer-betel quid chewers. The micronuclei frequency was lower among individuals chewing a raw betel nut, betel leaf, and lime mixture compared with those using quids with tobacco, betel nut, lime, or betel leaf. 
23 Stich (1982b) (86) Betel quid Yes The frequency of micronuclei of buccal cells in all three groups of chewers compared with a group of nonchewing subjects. 
  Khaini (tobacco and lime) Yes  
  Raw betel nut Yes  
*

For all reports, buccal cell changes were evaluated using the micronuclei assay.

Statistically significant association identified between buccal cell changes and chewing: positive (yes) or negative (no) association.

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