|TOBACCO CONTROL ISSUE - ORIGINAL ARTICLE
|Year : 2014 | Volume
| Issue : 5 | Page : 67-72
Rising incidence of oral cancer in Ahmedabad city
PC Gupta1, CS Ray1, PR Murti1, DN Sinha2
1 Healis Sekhsaria Institute for Public Health, Belapur, Navi Mumbai, Maharashtra, India
2 World Health Organization, Regional Office for South-East Asia, New Delhi, India
|Date of Web Publication||19-Dec-2014|
C S Ray
Healis Sekhsaria Institute for Public Health, Belapur, Navi Mumbai, Maharashtra
Source of Support: None, Conflict of Interest: None
Context: In 1999, an increase in mouth cancer incidence among young men (<50 years) in urban Ahmedabad was reported to be occurring along with decreasing mouth cancer incidence in older age groups and increasing oral submucous fibrosis incidence associated with areca nut consumption among young men in Gujarat. The aim was to investigate whether the increase in the incidence mouth cancer that had started among young men in the 1990s was continuing. Settings and Design: Ahmedabad urban population, comparison of reported mouth cancer cases in the population across four time period. Methods: Age-specific incidence rates of mouth cancer (International Classification of Diseases [ICD]-9:143-5; ICD-10:C03-06) in five year age groups among men aged ≥15 years for the city of Ahmedabad for years 1985, 1995, 2007 and 2010 were extracted from published reports. For comparison, lung cancer (ICD-9:169; ICD-10:C33-C34) rates were also abstracted. Statistical Analysis Used: A cohort approach was used for further analysis of mouth cancer incidence. Age adjusted incidence rates of mouth and lung cancer for men aged ≥15 years were calculated and compared. Results: The age specific incidence rates of mouth cancer among men increased over the 25-year period while lung cancer rates showed a net decrease. Using a cohort approach for mouth cancer, a rapid increase in younger age cohorts was found. Conclusions: Mouth cancer incidence increased markedly among men in urban Ahmedabad between 1985 and 2010, apparently due to increasing consumption of areca nut products, mawa and gutka. Gutka has now been banned all over India, but a more vigorous implementation is necessary.
Keywords: Areca nut smokeless tobacco, gutka, mawa, mouth cancer, submucous fibrosis
|How to cite this article:|
Gupta P C, Ray C S, Murti P R, Sinha D N. Rising incidence of oral cancer in Ahmedabad city. Indian J Cancer 2014;51, Suppl S1:67-72
| » Introduction|| |
In the late 1990s, an increasing occurrence of oral submucous fibrosis (OSF) was reported in young men in Gujarat  against a backdrop of decreasing or stable oral cancer incidence (mouth and tongue) in Ahmedabad and India's other population based cancer registries (PBCRs). ,, The possibility of an incipient increase in the incidence of mouth cancer (International Classification of Diseases [ICD]-9: 143-5) among young persons was investigated from the data of Ahmedabad (urban) PBCR for the two time period 1983-1987 and 1995. A significant increase in the incidence of mouth cancer in men in younger age groups (<50 years) emerged.  Since then, more recent data from the same registry has become available, and the current study was undertaken with the aim of investigating whether this increase in mouth cancer was continuing.
| » Methods|| |
Published reports of cancer incidence from the population-based cancer registry of urban Ahmedabad were used for analysis. Like the earlier study,  this study was also confined to men. The earliest dataset corresponded to the period 1983-1987 and the average age-specific annual incidence rates for this five year period were considered representative of the mid-year, 1985,  which was taken as the baseline year for comparison. Henceforth, for cancer incidence rates in this article, the period 1983-1987 is considered as 1985.
Curves of the five year age specific incidence rates of mouth cancer (ICD-9: 143-145; ICD-10: C03-06) for the male population aged ≥15 years of the city of Ahmedabad for years 1995,  2006-2008 (considered as representing 2007 incidence rates)  and 2010  were compared to those in the baseline year (1985).  The curves of age specific lung cancer incidence rates in males were similarly compared.
Since the denominator for all incidence rates was the population of Ahmedabad, the entire denominator was assumed to age according to calendar time. The incidence rates were available after approximately every five or 10-year and were computed for each five year age group. Thus, the cohort in each age group with the incidence rate in one time period corresponded to the cohort in the next higher age-group with the incidence rate in the next time period. In this manner, in a second analysis, the cohort approach was used in which the incidence rates were plotted for successive age cohorts over calendar time.
Finally, the age adjusted incidence rates for men ≥15 years over time were computed and compared for cancers of the mouth and lung.
| » Results|| |
The distribution of the numbers of incident cases of mouth cancer in men in each of the four time periods by five year age group is shown in [Table 1]. Also, the descriptives shown are the total numbers of men aged ≥15 years residing in Ahmedabad city and the crude incidence rate for this age range for each period. The trend in crude incidence is clearly an increase, but the values cannot be directly compared as their denominators, the population of the city of Ahmedabad, increased over time.
|Table 1: Incident mouth cancer cases among males in Ahmedabad Urban Agglomeration for four periods, during 1985-2010 and total male population (≥ 15 years of age) for each period |
Click here to view
[Figure 1] shows the comparison of the percentage age distribution of the male population (aged ≥15 years) in the base year (1985) and in the final year (2010). Over the years, the proportion of men in the mid-range age groups (40-45 years and 50-54 years) had increased slightly, but the size of the younger age groups (15-19 years to 35-39 years) had decreased.
|Figure 1: Age distribution of male population (aged ≥15 years) of Ahmedabad city in the base year (1985) and the most recent year (2010)|
Click here to view
[Figure 2] shows the distribution of the age-specific incidence rates in the four time periods. A shift toward a higher incidence in successive years is clearly seen. The increase is discernible even in very young age groups (<35 years). The peak incidence has also shifted downward from 70 to 74 years or above in 1985 to 55-59 years in 2010.
|Figure 2: A comparison of age-specific incidence rates of mouth cancer (International Classification of Diseases 143-5; C03-C06) in men ≥15 years (per 100,000), for years 1985, 1995, 2007 and 2010 in the city of Ahmedabad|
Click here to view
[Figure 3] shows the cohort analysis for age cohorts from 15 to 19 years to 45-49 years starting from the base year 1985 over the three successive time periods. The data points of age-specific incidence rates in 1985 have been joined for ease of comparison. A very steep increase in the incidence is apparent in each of the age cohorts over the successive time periods.
|Figure 3: Mouth cancer incidence rates in cohorts of men ≥15 years (per 100,000) by 5-year age cohort from 1985 onward in the city of Ahmedabad|
Click here to view
[Figure 4] shows the age-specific lung cancer incidence rates in Ahmedabad city for the same time periods. Clearly, the pattern of lung cancer incidence appears entirely different from the pattern of mouth cancer. Over the same period, a decrease in lung cancer incidence in Ahmedabad during the first to the third period was followed by an apparent increase.
|Figure 4: A comparison of age-specific incidence rates of lung cancer (International Classification of Diseases 162; C033-C034) in men ≥15 years (per 100,000 population), for years 1985, 1995, 2007 and 2010 in the city of Ahmedabad|
Click here to view
[Figure 5] shows that the age-standardized incidence rates of men ≥15 years of age for cancers of mouth and lung during three time period. The age standardization procedure permits direct comparison of the rates. From the beginning of the second time period in 1995, the incidence of mouth cancer increased by >2½ times by 2010, while the incidence of lung cancer decreased by half in the first and second time periods (from 1985 to 2007) before increasing in the third time period (2007-2010).
|Figure 5: Trends in age adjusted incidence rates of mouth and lung cancer in men ≥15 years (per 100,000) for years 1985, 1995, 2007 and 2010 in the city of Ahmedabad ASR(W) = Age standardized rate (to the standard world population)|
Click here to view
| » Discussion and Conclusion|| |
The most important causal factor for oral cancer in India is the use of tobacco. Tobacco use has been estimated to be responsible for 90% of oral cancers in India. Specifically, 30% of oral cancer cases have been attributed to chewing (betel quid with tobacco) without smoking, 50% to chewing with smoking.  An estimate from more recent studies in India was that 52% of oral cancers in both men and women were attributable to smokeless tobacco (mainly chewing of betel quid with tobacco) with smoking (the estimates without smoking were unstable). 
Like most other cancers, oral cancer is considered as a disease of the elderly. The age-specific incidence of this disease rises rapidly with age everywhere including in India. , Oral cancer does get diagnosed among young persons (≤45 years) and an increase in the incidence among them has been receiving global attention. , This is of particular importance in India where there is a widespread general impression of increasing incidence of oral cancer among young persons accompanied by a lot of anecdotal, and some case-series evidence from various parts of India, including Gujarat  Maharashtra, , Karnataka , and Uttar Pradesh. 
These observations of increasing incidence of oral cancer among young persons have resulted in considerable public health concern, which has led to cancer surgeons taking help from young oral cancer patients for nationwide awareness and advocacy campaigns to advance tobacco control. 
In India, the suspicion of increasing incidence of oral cancer is bolstered by a well-documented increase in OSF among young persons that began in the 1990s in Bhavnagar, Gujarat, Hyderabad, Andhra Pradesh and Mumbai, Maharashtra. ,,,, The OSF epidemic was first noted in Bhavnagar district in Gujarat state in the late 1980s, where a case-control study was conducted. Of 60 consecutive cases of OSF included in the study, 59 were using areca nut in some form every day, and one was occasionally using . In addition, 50 of them were using mawa, a vendor made mixture of areca nut pieces and a small amount of tobacco with slaked lime that had become very popular. As many as 58 out of all the cases were males and 57 of them were below 45-years of age. Users of only mawa had a very high relative risk for OSF (109.6). The largest group (37 out of 59 cases or 63%) of OSF cases had used the products six or more times a day and had more than twice the risk of those who had used the products five or fewer times a day. Although the risk increased with duration of use, it was noted that 29% of cases had used the products for <5-years. 
To ascertain the real nature of the epidemic of OSF, in 1993-1994, results from a house-to-house survey in part of Bhavnagar district were reported. This survey was conducted among 5018 tobacco and/or areca nut users age ≥15 years, and it found 164 cases of OSF, resulting in a prevalence of 3.2% among tobacco/areca nut users. Of the 164 cases, 160 were currently using areca nut, mostly in the form of mawa. Some of the 84% of the cases were under 35-year of age, and all were males. These results contrasted with an earlier survey in 1967 of similar size in which no OSF case was found among males, but some were found among females. By the late 1980s, gutka, another name for pan masala with tobacco, and pan masala itself, both areca nut products, were being intensely advertised on television all over India and sold in highly affordable single portion sachets, although less readily available in rural areas.  There seemed to be a connection between these products and the OSF epidemic in the early 1990s.
The early age at which OSF was also occurring prompted a case series study at a hospital in Hyderabad. Among the 50 OSF patients studied, those who chewed pan masala or gutka had presented with OSF after 2.7 ± 0.6 years of use while betel quid chewers came with OSF for diagnosis after 8.6 ± 2.3 years of use (P < 0.05). 
A case-control study was undertaken in Nagpur, Maharashtra, at the Government Dental College and Hospital with 200 consecutive cases of OSF diagnosed during June 1996 to May 1997 and outpatients roughly matched on age. Almost all participants were in the age range of 15-54 years, and all were interviewed about their areca nut and tobacco use. The odds ratio for the use of areca nut products increased from 10.1 for their use once a day to 255.2 for their use six or more times a day. 
That areca nut causes OSF had been clearly established by 1990.  Depending on where the quid is kept, OSF typically occurs at the site of the buccal mucosa, but may occur at other sites in the mouth  and may even involve the tongue. , The phenomenon of increased OSF prevalence in association with the use of areca nut products is currently being reported from virtually all parts of India ,,, The increasing prevalence of OSF is, therefore, clearly linked to increasing use of areca nut products, especially pan masala with tobacco, gutka and mawa, which are mainly used by young persons. 
OSF exhibits a high potential for cancer development. In one cohort study of 12,212 tobacco users, followed-up for eight years, the relative risk for cancer compared to tobacco users without any precancerous lesion was 397.3.  In a 17-year follow-up of 66 OSF patients in Kerala, five developed oral cancer, yielding a malignant transformation rate of 7.6%. 
Gutka use has been found to carry a high risk of oral cancer. A case-control study conducted during 2005-2006 in Pune, Maharashtra, with 350 oral cancer cases and 350 controls reported adjusted odds ratios with 95% confidence intervals for the use of various tobacco products: Gutka chewing showed the highest risk (12.3 [7.0-23.7]), followed by tobacco chewing (8.3 [5.4-13.0]), areca nut chewing (6.6 [3.0-14.8]), bidi smoking (4.1 [2.4-6.9]) and mishri use (3.3 [2.1-5.4]). 
The present analysis shows that incidence rates of mouth cancer among men from the urban population of Ahmedabad have increased markedly from 1985 to 2010. It is interesting that the increase is not confined to any specific age-group; however, the magnitude of the increase differs considerably by age-group. The youngest age-group (<35 years), which had low mouth cancer incidence rates to begin with in 1985, had the largest increase - of over 30 times by 2010. Even the mid-range age-groups (35-39 and 40-45 years), had 10-fold increases in the incidence and the age-group 45-49 had a five-fold increase. Considering that the total time period of observation was <30-years, this is an explosive increase in the incidence unprecedented in India and perhaps globally, for any cancer.
Although only Ahmedabad data are analyzed here, it is worth noting that the increase in mouth cancer incidence is not confined to the city of Ahmedabad. In a recent report on time trends in cancer incidence in 13 registries of the National Cancer Registry Program, highly significant increases in age adjusted rates of mouth cancer incidence in men were found in the older registries of Bhopal, Madhya Pradesh (5.9 in 1988-11.2 in 2010), Mumbai, Maharashtra (5.5 in 1998-8.3 in 2010) and Delhi (3.0 in 1988-7.1 in 2008) as well as in newer registries in Ahmedabad (rural), (6.5 in 2004-12.7 in 2010) and in Dibrugarh, Assam (5.7 in 2003-10.2 in 2011). 
This increase in the incidence of mouth cancer in Ahmedabad and several other registries in recent years points toward a virtually pan-Indian increase in exposure to a specific causal factor especially in the younger age-groups. The Global Adult Tobacco Survey (GATS), conducted in India in 2009-2010 reported the highest prevalence of use of areca nut based tobacco products (which include gutka) was among men in Madhya Pradesh (26.7%), followed by Gujarat (21.7%), also Maharashtra (13.4%) and Delhi (13.2%).  In some states, prevalence of using betel quid with tobacco among men is also high, as in Assam (17.4%), Madhya Pradesh (9.7%) and several other states. The clearest pointer toward the responsible causal factor is the fact that the three cancer registries (Bhopal, Mumbai and Delhi) that have reported an increase in mouth cancer are located in states with a high prevalence of use of areca nut and tobacco mixtures and/or betel quid with tobacco. ,
Although smoking is also a causal factor for mouth cancer, smoking does not seem to have played any major role in the increase reported here. Smoking is strongly related to lung cancer, and if smoking had increased, lung cancer would have also shown an increase. That has clearly not happened. Therefore, almost, all increase in mouth cancer is probably attributable to increase in smokeless tobacco use.
The increased incidence of mouth cancer seen in Ahmedabad and in other registries where the use of areca nut products like mawa and gutka is highly prevalent can be explained by the evidence on the carcinogenicity of these products. An evaluation by the International Agency for Research on Cancer had concluded that there is sufficient evidence for the carcinogenicity of areca nut with or without tobacco toward causing mouth cancer with high relative risks. Areca nut use can also induce a dependence syndrome or addiction, which is consonant with its alkaloid content. The dependence promotes a high level of continued use.  This is apart from the additional carcinogenicity and addictiveness due to the tobacco content of commonly used products like mawa and gutka. 
The GATS report also shows that among men, gutka and other areca nut and tobacco mixtures are used mainly by individuals below the age of 45-years, whereas for other smokeless tobacco products, prevalence is larger in higher age-groups.  Hence, the younger age of incidence of mouth cancer is clearly related to the young age of most users of the areca nut-tobacco products.
It is concluded that the rapid increase in mouth cancer among men has occurred in the city of Ahmedabad. This is most likely due to the widespread and increasing popularity and use of areca nut and tobacco mixtures, mawa and gutka, which came into wide use in the decade of 1980s and later. The marketing of gutka has been intense and especially targeted toward adolescents. The size of gutka industry starting from almost nothing prior to 1980s increased to billions of dollars (several thousand crore rupees) by the first decade of 21 st century. The correspondence of high prevalence of use of these products in other states with increasing oral cancer incidence as a whole further confirms that the sale of these products, whether packaged or not, constitutes a serious public health problem, especially among young men.
A regulation dated 1 st August 2011 notified under the Food and Safety and Standards Act, 2006, prohibited the manufacture, sale and storage of packaged food products that contain tobacco.  Under Indian laws and as per the judgment of the Supreme Court, gutka is a food product. Taking the help of this food law, starting from March 2012, by mid-2014, all States in India have banned gutka, and some have banned other flavored smokeless tobacco products as well.  Maharashtra has banned pan masala without tobacco and flavored areca nut products as well.
There have been some initial evaluations of the gutka bans. In a preliminary evaluation of the effectiveness of the ban in Maharashtra, a focus group discussion conducted with eleven men aged 19-43 years, who were former gutka users revealed they were all aware of the ban and hoped it would remain in force so that they would not start using gutka again. Three men stopped consuming any form of tobacco while eight switched to other tobacco products. Of these, one switched to mawa, a vendor made product. 
A rapid surveillance study performed soon after the gutka ban in a low-income community of Mumbai found that gutka was much less available, less in demand and its use bore a social stigma. Commonly, gutka users were switching to other tobacco products and some new products similar to gutka with different names were now available. The conclusion was that the gutka ban had had an effect but that more efforts at creating awareness about the harmfulness of gutka and other tobacco products would be necessary.  Thus, although efforts toward curbing the epidemic of oral cancer have started, they clearly require vigorous implementation of the ban on gutka and related tobacco control measures.
| » Acknowledgments|| |
This work was supported by the South East Asia Office of the World Health Organization.
The author alone is responsible for the views expressed in this article and they do not necessarily represent the views, decisions or policies of the institutions with which they are affiliated.
| » References|| |
Gupta PC, Sinor PN, Bhonsle RB, Pawar VS, Mehta HC. Oral submucous fibrosis in India: A new epidemic? Natl Med J India 1998;11:113-6.
Sankaranarayanan R, Masuyer E, Swaminathan R, Ferlay J, Whelan S. Head and neck cancer: A global perspective on epidemiology and prognosis. Anticancer Res 1998;18:4779-86.
Yeole BB. Trends and predictions of cancer incidence cases by site and sex for Mumbai. Indian J Cancer 1999;36:163-78.
Yeole BB. Trends in incidence of head and neck cancers in India. Asian Pac J Cancer Prev 2007;8:607-12.
Gupta PC. Mouth cancer in India: A new epidemic? J Indian Med Assoc 1999;97:370-3.
Parkin DM, Muir CS, Whelan SL, Gao YT, Ferlay J, Powell J, editors. Cancer Incidence in Five Continents. Vol. VI. Lyon: World Health Organization, International Agency for Research on Cancer (IARC) and International Association of Cancer Registries. IARC Scientific Publication No. 120; 1992.
Population Based Cancer Registry, (Ahmedabad Urban Agglomeration Area) and Hospital Based Cancer Registry. Report of 1995. Ahmedabad: The Gujarat Cancer and Research Institute; 1999. p. 14, 8.
Population Based Cancer Registry, Ahmedabad District (Other than Ahmedabad Urban) and Ahmedabad Urban Agglomeration Area. Individual Registry Write-up. In: Three Three-Year Report of Population Based Cancer Registries: 2006-2008. First Report of 20 PBCRs in India. Bangalore: National Cancer Registry Programme, Indian Council for Medical Research; 2010. p. 420, 2. Available from: http://www.ncrpindia.org/Reports/PBCR_2006_2008.aspx
. [Last accessed on 2014 Jun 03].
Population Based Cancer Registry (Ahmedabad Urban Agglomeration Area), and Hospital Based Cancer Registry. Report of 2010. Ahmedabad: The Gujarat Cancer and Research Institute; 2013. p. 32, 5.
Control of oral cancer in developing countries. A WHO meeting. Bull World Health Organ 1984;62:817-30.
Boffetta P, Hecht S, Gray N, Gupta P, Straif K. Smokeless tobacco and cancer. Lancet Oncol 2008;9:667-75.
Daftary DK, Murti PR, Bhonsle RB, Gupta PC, Mehta FS, Pindborg JJ. In: Prabhu SR, Wilson DF, Daftary DK, Johnson NW, editors. Oral Squamous cell Carcinoma. Oral Diseases in the Tropics. Oxford (UK): Oxford University Press; 1992. p. 429-48.
Macfarlane TV, Macfarlane GJ, Oliver RJ, Benhamou S, Bouchardy C, Ahrens W, et al.
The aetiology of upper aerodigestive tract cancers among young adults in Europe: The ARCAGE study. Cancer Causes Control 2010;21:2213-21.
Warnakulasuriya S. Global epidemiology of oral and oropharyngeal cancer. Oral Oncol 2009;45:309-16.
Patel MM, Pandya AN. Relationship of oral cancer with age, sex, site distribution and habits. Indian J Pathol Microbiol 2004;47:195-7.
Madani AH, Dikshit M, Bhaduri D. Risk for oral cancer associated to smoking, smokeless and oral dip products. Indian J Public Health 2012;56:57-60.
Chaturvedi P, Vaishampayan SS, Nair S, Nair D, Agarwal JP, Kane SV, et al.
Oral squamous cell carcinoma arising in background of oral submucous fibrosis: A clinicopathologically distinct disease. Head Neck 2013;35:1404-9.
Kalyani R, Das S, Kumar ML. Pattern of cancer in adolescent and young adults - A ten year study in India. Asian Pac J Cancer Prev 2010;11:655-9.
Aruna DS, Prasad KV, Shavi GR, Ariga J, Rajesh G, Krishna M. Retrospective study on risk habits among oral cancer patients in Karnataka Cancer Therapy and Research Institute, Hubli, India. Asian Pac J Cancer Prev 2011;12:1561-6.
Kumar V, Sindhu VA, Rathanaswamy S, Jain J, Pogal JR, Akhtar N, et al.
Cancers of upper gingivobuccal sulcus, hard palate and maxilla: A tertiary care centre study in North India. Natl J Maxillofac Surg 2013;4:202-5.
Murukutla N, Turk T, Prasad CV, Saradhi R, Kaur J, Gupta S, et al.
Results of a national mass media campaign in India to warn against the dangers of smokeless tobacco consumption. Tob Control 2012;21:12-7.
Sinor PN, Gupta PC, Murti PR, Bhonsle RB, Daftary DK, Mehta FS, et al.
A case-control study of oral submucous fibrosis with special reference to the etiologic role of areca nut. J Oral Pathol Med 1990;19:94-8.
Babu S, Bhat RV, Kumar PU, Sesikaran B, Rao KV, Aruna P, et al.
A comparative clinico-pathological study of oral submucous fibrosis in habitual chewers of pan masala and betelquid. J Toxicol Clin Toxicol 1996;34:317-22.
Chaturvedi P. Gutka or areca nut chewer′s syndrome. Indian J Cancer 2009;46:170-2.
Patil PB, Bathi R, Chaudhari S. Prevalence of oral mucosal lesions in dental patients with tobacco smoking, chewing, and mixed habits: A cross-sectional study in South India. J Family Community Med 2013;20:130-5.
Hazare VK, Goel RR, Gupta PC. Oral submucous fibrosis, areca nut and pan masala use: A case-control study. Natl Med J India 1998;11:299.
Murti PR, Bhonsle RB, Gupta PC, Daftary DK, Pindborg JJ, Mehta FS. Etiology of oral submucous fibrosis with special reference to the role of areca nut chewing. J Oral Pathol Med 1995;24:145-52.
Daftary DK, Murti PR, Bhonsle RB, Gupta PC, Mehta FS, Pindborg JJ. Oral precancerous lesions and conditions of tropical interest. In: Prabhu SR, Wilson DF, Daftary DK, Johnson NW, editors. Oral Diseases in the Tropics. Oxford (UK): Oxford University Press; 1992. p. 402-28.
Ali FM, Aher V, Prasant MC, Bhushan P, Mudhol A, Suryavanshi H. Oral submucous fibrosis: Comparing clinical grading with duration and frequency of habit among areca nut and its products chewers. J Cancer Res Ther 2013;9:471-6.
Deshpande A, Kiran S, Dhillon S, Mallikarjuna R. Oral submucous fibrosis: A premalignant condition in a 14-year-old Indian girl. BMJ Case Rep 2013;2013.
Bhatnagar P1, Rai S, Bhatnagar G, Kaur M, Goel S, Prabhat M. Prevalence study of oral mucosal lesions, mucosal variants, and treatment required for patients reporting to a dental school in North India: in accordance with WHO guidelines. J Family Community Med. 2013 Jan;20:41-8.
Gupta PC, Bhonsle RB, Murti PR, Daftary DK, Mehta FS, Pindborg JJ. An epidemiologic assessment of cancer risk in oral precancerous lesions in India with special reference to nodular leukoplakia. Cancer 1989;63:2247-52.
Murti PR, Bhonsle RB, Pindborg JJ, Daftary DK, Gupta PC, Mehta FS. Malignant transformation rate in oral submucous fibrosis over a 17-year period. Community Dent Oral Epidemiol 1985;13:340-1.
National Centre for Disease Informatics and Research (NCDIR)-National Cancer Registry Programme (NCRP). Time Trends in Cancer Incidence Rates, 1982-2010. Bangalore: NCDIR-NCRP (ICMR); 2013. p. 31-6.
International Agency for Research on Cancer (IARC). Monographs on the Evaluation of Carcinogenic Risks to Humans. Betel-Quid and Areca-Nut Chewing and Some Areca-Nut-Derived Nitrosamines. Vol. 85. Lyon: IARC; 2004.
IARC. Monographs on the Evaluation of the Carcinogenic risk of Chemicals to Humans. Smokeless Tobacco and Some Tobacco-specific N-Nitrosamines. Vol. 89. Lyon: IARC; 2007.
Dhumal GG, Gupta PC. Assessment of gutka ban in Maharashtra: Findings from a focus group discussion. Int J Head Neck Surg 2013;4:115-8.
Nair S, Schensul JJ, Bilgi S, Kadam V, D′Mello S, Donta B. Local responses to the Maharashtra gutka and pan masala ban: A report from Mumbai. Indian J Cancer 2012;49:443-7.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]