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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: an updated analysis of data from 127 countries

Country Study period Study design Exposure status Inclusion of cigarette/alcohol users Outcome Odds ratio/relative risk (95% CIs) Comments Quality assessment (NOS)a Reference
Cancers
 India 2001–2004 Case–control SLT with or without additives No/no Oral cancer 0.49 (0.32–0.75) Exclusive SLT users Selection****
Comparability**
Exposure*
[36]
 India 1996–1999 Case–control Ever SLT users Yes/yes Oral cancer 7.31 (3.79–14.1) Never drinkers adjusted for smoking Selection****
Comparability**
Exposure*
[37]
9.19 (4.38–19.28) Never smokers adjusted for alcohol
 India 1982–1992 Case–control Tobacco quid chewing Yes/no Oral cancer 5.80 (3.60–9.34) Adjusted for smoking Selection***
Comparability*
Exposure*
[38]
Pharyngeal cancer 1.20 (0.80–1.80)
Lung cancer 0.70 (0.40–1.22)
 India Not clear Case–control Chewing tobacco No/no Oral cancer 10.75 (6.58–17.56) Exclusive SLT users Selection**
Comparability*
Exposure0
[39]
 India 1990–1997 Cohort Current SLT users No/no Oral cancer 5.50 (3.30–9.17) Exclusive SLT users Selection****
Comparability*
Outcome**
[40]
Former SLT users 9.20 (4.60–18.40)
 India 1990–1997 Cohort Current SLT user Yes/yes Oral cancer 2.40 (1.70–3.39) Adjusted for smoking and alcohol Selection****
Comparability*
Outcome***
[41]
Former SLT users 2.10 (1.30–3.39)
 India Not clear Case–control Ever SLT users No/no Oral cancer 4.23 (3.11–5.75) Exclusive SLT users Selection***
Comparability**
Exposure0
[42]
Pharyngeal cancer 2.42 (1.74–3.37)
Laryngeal cancer 2.80 (2.07–3.79)
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***
Comparability**
Exposure0
[43]
Pharyngeal cancer 3.09 (2.31–4.13)
Laryngeal cancer 2.29 (1.72–3.05)
Oesophageal cancer 3.82 (2.84–5.13)
 India 2005–2006 Case–control Tobacco flakes Yes/yes Oral cancer 7.60 (4.90–11.79) Adjusted for smoking and alcohol Selection****
Comparability**
Exposure*
[44]
Gutkha 12.70 (7.00–23.04)
Mishiri 3.00 (1.90–4.74)
 India Not clear Case–control Chewing tobacco Yes/yes Oral cancer 5.00 (3.60–6.94) Adjusted for smoking and alcohol Selection****
Comparability*
Exposure*
[45]
 India 1982–1984 Case–control Chewing tobacco Yes/no Oral cancer 10.20 (2.60–40.02) Adjusted for smoking Selection***
Comparability**
Exposure*
[46]
 India 1980–1984 Case–control SLT users No/no Oral cancer 1.99 (1.41–2.81) Exclusive SLT users Selection**
Comparability0
Exposure*
[47]
 India 1952–1954 Case–control Chewing tobacco No/no Oral cancer 4.85 (2.32–10.14) Exclusive SLT users Selection***
Comparability**
Exposure0
[48]
Pharyngeal cancer 2.02 (0.94–4.33)
Laryngeal cancer 0.76 (0.37–1.56)
 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***
Comparability0
Exposure*
[49]
 India Not given Case–control Tobacco chewing Yes/yes Oropharyngeal cancer 7.98 (4.11–13.58)b Adjusted for smoking and alcohol Selection***
Comparability**
Exposure0
[50]
 India 1991–2003 Case–control Chewing tobacco No/no Oral cancer 5.88 (3.66–7.93) Exclusive SLT users Selection****
Comparability**
Exposure**
[51]
 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; data of habit was not available for the whole cohort Selection**
Comparability**
Exposure0
[52]
 Pakistan 1996–1998 Case–control Naswar Yes/yes Oral cancer 9.53 (1.73–52.50) Adjusted for smoking and alcohol Selection***
Comparability**
Exposure*
[53]
Paan with tobacco 8.42 (2.31–30.69)
 Sweden 1973–2002 Cohort Snus Yes/yes Oral and pharyngeal cancer combined 3.10 (1.50–6.41) Adjusted for smoking and alcohol Selection**
Comparability**
Outcome***
[54]
 India 1993–1999 Case–control Chewing tobacco Yes/yes Oral cancer 5.05 (4.26–5.99) Adjusted for smoking and alcohol Selection***
Comparability**
Exposure*
[55]
Pharyngeal cancer 1.83 (1.43–2.34)
Oesophageal cancer 2.06 (1.62–2.62)
 Norway 1966–2001 Cohort Chewing tobacco plus oral snuff No/no Oral cancer 1.10 (0.50–2.42) Adjusted for smoking, might be confounded by alcohol use Selection***
Comparability*
Outcome***
[56]
Oesophageal cancer 1.40 (0.61–3.21)
Pancreatic cancer 1.67 (1.12–2.49)
Lung cancer 0.80 (0.61–1.05)
 Sweden 1988–1991 Case–control Oral snuff Yes/yes Oral cancer 1.40 (0.80–2.45) Adjusted for smoking and alcohol Selection**
Comparability**
Exposure*
[57]
Laryngeal cancer 0.90 (0.50–1.62)
Oesophageal cancer 1.20 (0.70–2.06)
Pharyngeal cancer 0.70 (0.40–1.22)
 Sweden 1969–1992 Cohort Snus No/no Oral cancer 0.80 (0.40–1.60) Exclusive SLT users Selection***
Comparability*
Outcome***
[58]
Lung cancer 0.80 (0.50–1.28)
Pancreatic cancer 2.00 (1.20–3.33)
 Sweden 2000–2004 Case–control Oral snuff Yes/yes Oral cancer 0.70 (0.30–1.63) Adjusted for smoking and alcohol Selection***
Comparability**
Exposure**
[59]
 Sweden 1980–1989 Case–control Oral snuff Yes/yes Oral cancer 0.80 (0.50–1.28) Adjusted for smoking and alcohol Selection**
Comparability**
Exposure***
[60]
 USA 1972–1983 Case–control Oral snuff Yes/yes Oral cancer 0.80 (0.40–1.60) Not clear if adjusted for smoking and alcohol Selection**
Comparability0
Exposure*
[61]
Chewing tobacco 1.00 (0.70–1.43)
 USA Not given Case–control SLT use Yes/yes Oral cancer 0.90 (0.38–2.13) Adjusted for smoking and alcohol Selection***
Comparability**
Exposure*
[10]
Pharyngeal cancer 1.59 (0.84–3.01)
Laryngeal cancer 0.67 (0.19–2.36)
 India 2001–2004 Case–control Chewing tobacco No/no Pharyngeal cancer 3.18 (1.92–5.27) Exclusive SLT users Selection***
Comparability**
Exposure*
[62]
Laryngeal cancer 0.95 (0.52–1.74)
 Pakistan 1998–2002 Case–control Snuff dipping No/no Oesophageal cancer 4.10 (1.30–12.93) Adjusted for areca nut Selection***
Comparability**
Exposure**
[63]
Quid with tobacco 14.20 (6.40–31.50)
 India 2008–2012 Case–control Nass chewing No/no Oesophageal cancer 2.88 (2.06–4.03) Exclusive SLT users Selection***
Comparability**
Exposure**
[64]
Gutkha chewing 2.87 (0.87–9.47)
 India 2007–2011 Case–control Oral snuff Yes/yes Oesophageal cancer 3.86 (2.46–6.06) Adjusted for smoking and alcohol Selection**
Comparability**
Exposure*
[65]
 India 2011–2012 Case–control Chewing tobacco Yes/yes Oesophageal cancer 2.63 (1.53–4.52) Adjusted for smoking and alcohol Selection***
Comparability**
Exposure*
[66]
 Sweden 1995–1997 Case–control Oral snuff Yes/yes Oesophageal adenocarcinoma 1.20 (0.70–2.06) Adjusted for smoking and alcohol Selection***
Comparability**
Exposure*
[67]
Squamous cell carcinoma 1.40 (0.90–2.18)
 Sweden 1969–1993 Cohort Oral snuff Yes/no Oesophageal adenocarcinoma 1.30 (0.80–2.11) Adjusted for smoking Selection**
Comparability*
Outcome**
[68]
Squamous cell carcinoma 1.20 (0.80–1.80)
 Sweden 1974–1985 Cohort SLT users No/NA Lung cancer 0.90 (0.20–4.05) Adjusted for age, region of origin Selection***
Comparability*
Outcome**
[69]
 Morocco 1996–1998 Case–control SLT users Yes/no Lung cancer 1.05 (0.28–3.94) Adjusted for smoking Selection**
Comparability**
Exposure**
[70]
 USA 1977–1984 Case–control SLT users Yes/no Oesophageal cancer 1.20 (0.10–14.40) Adjusted for smoking Selection***
Comparability**
Exposure**
[71]
 USA 1986–1989 Case–control SLT users Yes/no Pancreatic cancer 1.40 (0.50–3.92) Adjusted for smoking Selection***
Comparability*
Exposure**
[72]
 USA 2000–2006 Case–control Chewing tobacco Yes/yes Pancreatic cancer 0.60 (0.30–1.20) Adjusted for smoking and alcohol Selection****
Comparability**
Exposure*
[73]
Oral snuff 0.50 (0.10–2.50)
 Pakistan 2014–2015 Case–control Ever use of naswar Yes/yes Oral cancer 21.20 (8.40–53.8) Adjusted for smoking; restricted control for alcohol due to cultural sensitivity Selection****
Comparability**
Exposure***
[74]
 India March–July, 2013 Case–control Gutkha Yes/yes Oral cancer 5.10 (2.00–10.30) Adjusted for smoking and alcohol Selection***
Comparability*
Exposure**
[75]
Chewing tobacco 6.00 (2.30–15.70)
Supari with tobacco 11.40 (3.40–38.20)
Quid with tobacco 6.40 (2.60–15.50)
 Pakistan 1996–1998 Case–control Quid with tobacco Yes/yes Oral cancer 15.68 (3.00–54.90) Adjusted for smoking and alcohol Selection**
Comparability*
Exposure***
[76]
Cardiovascular diseases (ischaemic heart disease and stroke)
 52 countries 1999–2003 Case–control Chewing tobacco Yes/yes Myocardial infarction 1.57 (1.24–1.99) Adjusted for smoking, diet, diabetes, abdominal obesity, exercise, hypertension Selection****
Comparability**
Exposure*
[35]
 Pakistan 2005–2011 Case–control Dippers (Naswar) No/NA Myocardial infarction 1.46 (1.21–1.78) Adjusted for age, gender, region, ethnicity, diet, socioeconomic status Selection****
Comparability**
Exposure**
[77]
Chewers (Paan/Supari/Gutkha) 1.71 (1.46–2.00)
 Bangladesh 2006–2007 Case–control Ever SLT users Yes/NA Myocardial infarction, angina pectoris 2.80 (1.10–7.30) Adjusted for age, gender, smoking, hypertension Selection** Comparability** Exposure** [78]
 Bangladesh 2010 Case–control Ever SLT users No/NA Myocardial infarction, angina pectoris 0.77 (0.52–1.13) Adjusted for age, gender, area of residence, hypertension, diabetes, stress Selection*** Comparability** Exposure* [79]
 India 2013 Case–control Current SLT users Yes/yes Stroke 1.50 (0.80–2.79) Adjusted for age, smoking, alcohol, diabetes, hypertension Selection** Comparability** Exposure* [80]
 Sweden 1989–1991 Case–control Current snuff users No/NA Myocardial infarction 0.89 (0.62–1.29) Adjusted for age Selection**** Comparability** Exposure* [81]
 Sweden 1991–1993 Case–control Current snuff users No/NA Myocardial infarction 0.58 (0.35–0.94) Adjusted for heredity, education, marital status, hypertension, diabetes, cholesterol Selection**** Comparability** Exposure** [82]
 Sweden 1985–2000 Case–control Current snuff users No/NA Stroke 0.87 (0.41–1.83) Adjusted for education, marital status, diabetes, hypertension, cholesterol Selection**** Comparability** Exposure** [83]
 Sweden 1998–2005 Case–control Current snuff users No/NA Myocardial infarction 0.73 (0.35–1.50) Adjusted for age, hospital catchment area Selection*** Comparability** Exposure** [84]
Former snuff users 1.20 (0.46–3.10)
 Sweden 1988–2003 Cohort Current use of snuff No/NA Ischaemic heart disease 0.77 (0.51–1.15) Adjusted for age, socioeconomic status, residential area, self-reported health, longstanding illnesses, physical activity Selection*** Comparability** Outcome*** [85]
Stroke 1.07 (0.65–1.77)
 Sweden 1978–2004 Cohort Ever snuff users No/NA Myocardial infarction 0.99 (0.90–1.10) Adjusted for age, BMI, region of residence Selection** Comparability** Outcome*** [86]
 Sweden 1985–1999 Case–control Current snuff users No/NA Myocardial infarction 0.82 (0.46–1.43) Adjusted for BMI, leisure time, physical activity, education, cholesterol Selection**** Comparability** Exposure* [87]
Former snuff users 0.66 (0.32–1.34)
 Sweden 1978–2003 Cohort Ever snuff users No/NA Stroke 1.02 (0.92–1.13) Adjusted for age, BMI, region of residence Selection** Comparability** Outcome*** [88]
 Sweden 1998–2005 Cohort Current snuff users No/NA Ischaemic heart disease 0.85 (0.51–1.42) Adjusted for age, hypertension, diabetes, cholesterol Selection*** Comparability** Outcome* [89]
Former snuff users 1.07 (0.56–2.04)
Current snuff users Stroke 1.18 (0.67–2.08)
Former snuff users 1.35 (0.65–2.82)
 Sweden 1991–2004 Cohort Current snuff users No/NA Myocardial infarction 0.75 (0.30–1.87) Adjusted for age, marital status, occupation, diabetes, BMI, hypertension, physical activity Selection*** Comparability** Outcome** [90]
Stroke 0.59 (0.20–1.50)
  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
  3. bEffect sizes are for oral and pharyngeal cancers combined and were included in the meta-analysis for oral cancer only