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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**
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*
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*
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)
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)
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**
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**
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)
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)
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
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**
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**
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**
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**
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*
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**
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**
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**
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**
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)
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**
Exposure/Outcome**
  1. BMI body mass index, NA not applicable, NOS Newcastle-Ottawa Scale, SLT smokeless tobacco
  2. 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]
  3. bEffect sizes are for oral and pharyngeal cancers combined and were included in the meta-analysis for oral cancer only
  4. cBased on parameter estimate and standard error reported in paper
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