Global burden of disease due to smokeless tobacco consumption in adults: analysis of data from 113 countries

Siddiqi, Kamran; Shah, Sarwat; Abbas, Syed Muslim; Vidyasagaran, Aishwarya; Jawad, Mohammed; Dogar, Omara; Sheikh, Aziz

doi:10.1186/s12916-015-0424-2

Table 3 Smokeless tobacco use and risk of cancers, ischaemic heart disease, and stroke—studies included in meta-analysis

From: Global burden of disease due to smokeless tobacco consumption in adults: analysis of data from 113 countries

Country	Study period	Study design	Exposure status	Inclusion of cigarette/alcohol users	Outcome	Odds ratios/relative risks (95 % confidence intervals)	Comments	Quality assessment (NOS)^a	Reference
CANCERS
India	2001–2004	Case–control	Smokeless tobacco with or without additives	No/No	Oral cancer	0.49 (0.32–0.75)	Exclusive SLT users	Selection****	Anantharaman et al. 2007 [46]
								Comparability**
								Exposure/Outcome*
India	1996–1999	Case–control	Ever SLT users	Yes/Yes	Oral cancer	7.31 (3.79–14.1)	Never drinkers adjusted for smoking	Selection****	Balaram et al. 2002 [47]
						9.19 (4.38–19.28)	Never smokers adjusted for alcohol	Comparability**
						9.19 (4.38–19.28)	Never smokers adjusted for alcohol	Exposure/Outcome *
India	1982–1992	Case–control	Tobacco quid chewing	Yes/No	Oral cancer	5.8 (3.6–9.34)	Adjusted for smoking	Selection***	Dikshit & Kanhere 2000 [48]
					Pharyngeal cancer	1.2 (0.8–1.8)		Comparability*
					Lung cancer	0.7 (0.4–1.22)		Exposure/Outcome*
India	Unclear	Case–control	Chewing tobacco	No/No	Oral cancer	10.75 (6.58–17.56)	Exclusive SLT users	Selection**	Goud et al. 1990 [49]
								Comparability*
								Exposure/Outcome⁰
India	1990–1997	Cohort	Current SLT users	No/No	Oral cancer	5.5 (3.3–9.17)	Exclusive SLT users	Selection****	Jayalekshmi et al. 2009 [50]
			Former SLT users			9.2 (4.6–18.40)		Comparability*
			Former SLT users			9.2 (4.6–18.40)		Exposure/Outcome**
India	1990–1997	Cohort	Current SLT user	Yes/Yes	Oral cancer	2.4 (1.7–3.39)	Adjusted for smoking and alcohol	Selection****	Jayalekshmi et al. 2010 [51]
			Former SLT users			2.1 (1.3–3.39)		Comparability*
			Former SLT users			2.1 (1.3–3.39)		Exposure/Outcome***
India	May 2005	Case–control	Ever SLT users	No/No	Oral cancer	4.23 (3.11–5.75)	Exclusive SLT users	Selection***	Jayant et al. 1977 [52]
					Pharyngeal cancer	2.42 (1.74–3.37)		Comparability**
					Laryngeal cancer	2.8 (2.07–3.79)		Exposure/Outcome⁰
					Oesophageal cancer	1.55 (1.15–2.07)		Exposure/Outcome⁰
India	1968	Case–control	Tobacco	Yes/No	Oral cancer	4.63 (3.50–6.14)	Exclusive chewers and non-chewers data available	Selection***	Jussawalla & Deshpande 1971 [53]
					Pharyngeal cancer	3.09 (2.31–4.13)		Comparability**
					Laryngeal cancer	2.29 (1.72–3.05)		Exposure/Outcome⁰
					Oesophageal cancer	3.82 (2.84–5.13)		Exposure/Outcome⁰
India	2005–2006	Case–control	Tobacco flakes	Yes/Yes	Oral cancer	7.6 (4.9–11.79)	Adjusted for smoking and alcohol	Selection****	Madani et al. 2010 [54]
			Gutkha			12.7 (7–23.04)		Comparability**
			Mishiri			3.0 (1.9–4.74)		Exposure/Outcome*
India	Unclear	Case–control	Chewing tobacco	Yes/Yes	Oral cancer	5.0 (3.6–6.94)	Adjusted for smoking and alcohol	Selection****	Muwonge et al. 2008 [55]
								Comparability*
								Exposure/Outcome*
India	1982–1984	Case–control	Chewing tobacco	Yes/No	Oral cancer	10.2 (2.6–40.02)	Adjusted for smoking	Selection***	Nandakumar et al. 1990 [56]
								Comparability**
								Exposure/Outcome*
India	1980–1984	Case–control	SLT users	No/No	Oral cancer	1.99 (1.41–2.81)	Exclusive SLT users	Selection**	Rao et al. 1994 [57]
								Comparability⁰
								Exposure/Outcome*
India	1952–1954	Case–control	Chewing tobacco	No/No	Oral cancer	4.85 (2.32–10.14)	Exclusive SLT users	Selection***	Sanghvi et al. 1955 [58]
					Pharyngeal cancer	2.02 (0.94–4.33)		Comparability**
					Laryngeal cancer	0.76 (0.37–1.56)		Exposure/Outcome⁰
India	1983–1984	Case–control	Snuff (males only)	Yes/Yes	Oral cancer	2.93 (0.98–8.76)	Adjusted for smoking and alcohol; adjusted effect size is only among males	Selection***	Sankaranarayan et al. 1990 [59]
								Comparability⁰
								Exposure/Outcome*
India	Not given	Case–control	Tobacco chewing	Yes/Yes	Oropharyngeal cancer	7.98 (4.11–13.58)^b	Adjusted for smoking and alcohol	Selection***	Wasnik et al. 1998 [60]
								Comparability**
								Exposure/Outcome⁰
India	1991–2003	Case–control	Chewing tobacco	No/No	Oral cancer	5.88 (3.66–7.93)	Exclusive SLT users	Selection****	Subapriya e al. 2007 [61]
								Comparability**
								Exposure/Outcome**
India	1950–1962	Case–control	Tobacco with or without paan or lime	Yes/No	Oral and oropharyngeal cancer	41.90 (34.20–51.33)	Exclusive chewer data available	Selection**	Wahi et al. 1965 [62]
							Note: data of habit was not available for the whole cohort	Comparability**
							Note: data of habit was not available for the whole cohort	Exposure/Outcome⁰
Pakistan	1996–1998	Case–control	Naswar	Yes/Yes	Oral cancer	9.53 (1.73–52.50)	Adjusted for smoking and alcohol	Selection***	Merchant et al. 2000 [63]
			Paan with tobacco			8.42 (2.31–30.69)		Comparability**
			Paan with tobacco			8.42 (2.31–30.69)		Exposure/Outcome*
Sweden	1973–2002	Cohort	Snus	Yes/Yes	Oral and pharyngeal combined	3.10 (1.50–6.41)	Adjusted for smoking and alcohol	Selection**	Roosar et al. 2008 [64]
								Comparability**
								Outcome***
India	1993–1999	Case–control	Chewing tobacco	Yes/Yes	Oral cancer	5.05 (4.26–5.99)	Adjusted for smoking and alcohol	Selection***	Znaor et al. 2003 [65]
					Pharynx	1.83 (1.43–2.34)		Comparability**
					Oesophagus	2.06 (1.62–2.62)		Exposure/Outcome*
Norway	1966–2001	Cohort	Chewing tobacco plus oral snuff	No/No	Oral cancer	1.1 (0.5–2.42)	Adjusted for smoking, might be confounded by alcohol use	Selection***	Bofetta et al. 2005 [66]
					Oesophageal cancer	1.4 (0.61–3.21)		Comparability*
					Pancreatic cancer	1.67 (1.12–2.49)		Exposure/Outcome***
					Lung cancer	0.80 (0.61–1.05)		Exposure/Outcome***
Sweden	1988–1991	Case–control	Oral snuff	Yes/Yes	Oral cancer	1.4 (0.8–2.45)	Adjusted for smoking and alcohol	Selection**	Lewin et al. 1998 [67]
					Larynx	0.9 (0.5–1.62)		Comparability**
					Oesophagus	1.2 (0.7–2.06)		Exposure/Outcome*
					Pharynx	0.7 (0.4–1.22)		Exposure/Outcome*
Sweden	1969–1992	Cohort	Snus	No/No	Oral cancer	0.8 (0.4–1.60)	Exclusive SLT users	Selection***	Luo et al. 2007 [68]
					Lung cancer	0.8 (0.5–1.28)		Comparability*
					Pancreatic cancer	2 (1.20–3.33)		Exposure/Outcome***
Sweden	2000–2004	Case–control	Oral snuff	Yes/Yes	Oral	0.70 (0.3–1.63)	Adjusted for smoking and alcohol	Selection***	Rosenquist et al 2005 [69]
								Comparability**
								Exposure/Outcome**
Sweden	1980–1989	Case–control	Oral snuff	Yes/Yes	Oral cancer	0.8 (0.5–1.28)	Adjusted for smoking and alcohol	Selection**	Schildt et al. 1998 [70]
								Comparability**
								Exposure/Outcome***
USA	1972–1983	Case–control	Oral snuff	Yes/Yes	Oral cancer	0.8 (0.4–1.60)	Not clear if adjusted for smoking and alcohol	Selection**	Mashberg et al. 1993 [71]
			Chewing tobacco			1 (0.7–1.43)		Comparability⁰
			Chewing tobacco			1 (0.7–1.43)		Exposure/Outcome*
USA	Not given	Case–control	SLT use	Yes/Yes	Oral cancer	0.90 (0.38–2.13)	Adjusted for smoking and alcohol	Selection***	Zhou et al. 2013 [15]
					Pharyngeal cancer	1.59 (0.84–3.01)		Comparability**
					Laryngeal cancer	0.67 (0.19–2.36)		Exposure/Outcome*
India	2001–2004	Case–control	Chewing tobacco	No/No	Pharyngeal cancer	3.18 (1.92–5.27)	Exclusive SLT users	Selection***	Sapkota et al. 2007 [72]
					Laryngeal cancer	0.95 (0.52–1.74)		Comparability**
					Laryngeal cancer	0.95 (0.52–1.74)		Exposure/Outcome*
Pakistan	1998–2002	Case–control	Snuff dipping	No/No	Oesophageal cancer	4.1 (1.3–12.93)	Adjusted for areca nut	Selection***	Akhtar et al. 2012 [73]
			Quid with tobacco			14.2 (6.4–31.50)		Comparability**
			Quid with tobacco			14.2 (6.4–31.50)		Exposure/Outcome**
India	2008–2012	Case–control	Nass chewing	No/No	Oesophageal cancer	2.88 (2.06–4.03)	Exclusive SLT users	Selection***	Dar et al. 2012 [74]
			Gutkha chewing			2.87 (0.87–9.47)		Comparability**
			Gutkha chewing			2.87 (0.87–9.47)		Exposure/Outcome**
India	2007–2011	Case–control	Oral snuff	Yes/Yes	Oesophageal cancer	3.86 (2.46–6.06)	Adjusted for smoking and alcohol	Selection**	Sehgal et al. 2012 [75]
								Comparability**
								Exposure/Outcome*
India	2011–2012	Case–control	Chewing tobacco	Yes/Yes	Oesophageal cancer	2.63 (1.53–4.52)	Adjusted for smoking and alcohol	Selection***	Talukdar et al. 2013 [76]
								Comparability**
								Exposure/Outcome*
Sweden	1995–1997	Case–control	Oral snuff	Yes/Yes	Oesophageal cancer (adenocarcinoma)	1.2 (0.7–2.06)	Adjusted for smoking and alcohol	Selection***	Lagergren et al. 2000 [77]
					(Squamous cell carcinoma)	1.4 (0.9–2.18)		Comparability**
					(Squamous cell carcinoma)	1.4 (0.9–2.18)		Exposure/Outcome*
Sweden	1969–1993	Cohort	Oral snuff	Yes/No	Oesophageal cancer (Adenocarcinoma)	1.3 (0.8–2.11)	Adjusted for smoking	Selection**	Zendehdel et al. 2008 [78]
					(Squamous cell carcinoma)	1.2 (0.8–1.80)		Comparability*
					(Squamous cell carcinoma)	1.2 (0.8–1.80)		Exposure/Outcome**
Sweden	1974–1985	Cohort	SLT users	No/NA	Lung cancer	0.90 (0.20– 4.05)	Adjusted for age, region of origin	Selection***	Bolinder et al. 1994 [79]
								Comparability*
								Outcome**
Morocco	1996–1998	Case–control	SLT users	Yes/No	Lung cancer	1.05 (0.28–3.94)	Adjusted for smoking	Selection**	Sasco et al. 2002 [80]
								Comparability**
								Exposure/Outcome**
USA	1977–1984	Case–control	SLT users	Yes/No	Oesophageal cancer	1.2 (0.1–14.40)	Adjusted for smoking	Selection***	Brown et al. 1988 [81]
								Comparability**
								Exposure/Outcome**
USA	1986–1989	Case–control	SLT users	Yes/No	Pancreatic cancer	1.4 (0.5–3.92)	Adjusted for smoking	Selection***	Alguacil & Silverman 2004 [82]
								Comparability*
								Exposure/Outcome**
USA	2000–2006	Case–control	Chewing tobacco	Yes/Yes	Pancreatic cancer	0.6 (0.3–1.20)	Adjusted for smoking and alcohol	Selection****	Hassan et al. 2007 [83]
			Oral snuff			0.5 (0.1–2.5)		Comparability**
			Oral snuff			0.5 (0.1–2.5)		Exposure/Outcome*
CARDIOVASCULAR DISEASES (ischaemic heart disease and stroke)
52 countries	1999–2003	Case–control	Chewing tobacco	No/Yes	Myocardial infarction	1.57 (1.24–1.99)	Adjusted for diabetes, abdominal obesity, hypertension, exercise, diet	Selection****	Teo et al. 2006 [29]
								Comparability**
								Exposure/Outcome*
Pakistan	2005–2011	Case–control	Dippers only (Naswar)	No/NA	Myocardial infarction	1.46 (1.20–1.77)	Adjusted for age, sex, region, ethnicity	Selection****	Alexander 2013 [84]
			Chewers only (Paan/ Supari/ Gutkha)			1.71 (1.46–2.00)		Comparability**
			Chewers only (Paan/ Supari/ Gutkha)			1.71 (1.46–2.00)		Exposure/Outcome**
Bangladesh	2006–2007	Case–control	Ever SLT users	No/NA	Myocardial infarction, Angina pectoris	2.8 (1.1–7.13)	Adjusted for age, sex, hypertension	Selection***	Rahman & Zaman 2008 [85]
								Comparability**
								Exposure/Outcome*
Bangladesh	2010	Case–control	Ever SLT users	No/NA	Myocardial infarction, Angina pectoris	0.77 (0.52–1.14)	Adjusted for age, hypertension, diabetes, acute psycho-social stress	Selection****	Rahman et al. 2012 [86]
								Comparability**
								Exposure/Outcome*
Sweden	1998–2005	Case–control	Current SLT users	No/NA	Myocardial infarction	0.73 (0.35–1.52)	Exclusive SLT users	Selection***	Hergens et al. 2005 [87]
			Former SLT users			1.2 (0.46–3.13)		Comparability**
			Former SLT users			1.2 (0.46–3.13)		Exposure/Outcome**
Sweden	1978–2004	Cohort	Ever SLT users	No/NA	Myocardial infarction	0.99 (0.90–1.10)	Adjusted for age, BMI, region of residence	Selection**	Hergens et al. 2007 [88]
								Comparability**
								Exposure/Outcome***
Sweden	1989–1991	Case–control	Regular SLT users	Yes/NA	Myocardial infarction	1.01 (0.66–1.55)^c	Adjusted for age, education, smoking	Selection***	Huhtasaari et al. 1992 [89]
								Comparability**
								Exposure/Outcome*
Sweden	1991–1993	Case–control	Former SLT users	No/NA	Myocardial infarction	1.23 (0.54–2.82)	Exclusive SLT users	Selection****	Huhtasaari et al. 1999 [90]
								Comparability**
								Exposure/Outcome**
Sweden	1988–2000	Cohort	Daily SLT users	No/NA	Ischaemic heart disease	1.41 (0.61–3.28)	Adjusted for BMI, physical activity, diabetes, hypertension	Selection****	Johansson et al. 2005 [91]
								Comparability**
								Exposure/Outcome**
Sweden	1985–1999	Case–control	Current SLT users	No/NA	Myocardial infarction	0.82 (0.46–1.46)	Adjusted for BMI, physical activity, education, cholesterol	Selection****	Wennberg et al. 2007 [92]
			Former SLT users			0.66 (0.32–1.36)		Comparability**
			Former SLT users			0.66 (0.32–1.36)		Exposure/Outcome**
Sweden	1985–2000	Case–control	Regular SLT users	No/NA	Stroke	0.87 (0.41–1.83)	Adjusted for diabetes, hypertension, education, marital status, cholesterol	Selection****	Asplund et al. 2003 [93]
								Comparability**
								Exposure/Outcome**
Sweden	1978–2003	Cohort	Ever SLT users	No/NA	Stroke	1.02 (0.92–1.13)	Adjusted for age, BMI, region of residence	Selection**	Hergens et al. 2008 [94]
								Comparability**
								Exposure/Outcome***
Sweden	1998–2005	Cohort	Current SLT users	No/NA	Ischaemic heart disease	0.85 (0.51–1.42)	Adjusted for age, hypertension, diabetes, cholesterol	Selection***	Hansson et al. 2009 [95]
			Former SLT users		Stroke	1.07 (0.56–2.04)		Comparability**
						1.18 (0.67–2.08)		Exposure/Outcome**
						1.35 (0.65–2.82)		Exposure/Outcome**
Sweden	1991–2004	Cohort	SLT users	No/NA	Myocardial infarction	0.75 (0.3–1.87)	Adjusted for age, diabetes, occupation, hypertension, physical activity, BMI, marital status	Selection***	Janzon et al. 2009 [96]
					Stroke	0.59 (0.2–1.5)		Comparability**
					Stroke	0.59 (0.2–1.5)		Exposure/Outcome**

BMI body mass index, NA not applicable, NOS Newcastle-Ottawa Scale, SLT smokeless tobacco
^aNOS for assessing the quality of non-randomised studies in meta-analyses based on selection, comparability, and exposure/outcome. Number of stars (*) indicates the number of criteria met for each of these three categories [23]
^bEffect sizes are for oral and pharyngeal cancers combined and were included in the meta-analysis for oral cancer only
^cBased on parameter estimate and standard error reported in paper

Back to article page

ISSN: 1741-7015

Contact us

Submission enquiries: bmcmedicineeditorial@biomedcentral.com
General enquiries: info@biomedcentral.com

BMC Medicine

Contact us