Interaction between Occupational and Non-Occupational Arsenic Exposure and Tobacco Smoke on Lung Cancerogenesis: A Systematic Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. Identification of Studies
2.2. Inclusion Criteria
2.3. Exclusion Criteria
2.4. Data Extraction
2.5. Quality Assessment
3. Results
3.1. Study Selection
3.2. Characteristics of the Included Studies
Author (Year) | Study Design | Subjects | Country | Age (Years) | Exposed Study Period | Data Collection | NOS * |
---|---|---|---|---|---|---|---|
Su Z. et al., 2022 [30] | Cohort | M/W (1215/405) | Taiwan | ≥40 | 1992–2019 | Baseline questionnaire and face to face interview | 9 |
Fan Y. et al., 2016 [44] | Prospective occupational-based cohort | M/W (8696/599) | China | 40–59; 60–69; >70 | 1992–2001 | Personal interview | 5 |
Steinmaus C.M. et al., 2015 [29] | Case-control | M/W (637/298) Cases: 301 Controls: 634 | Chile | Case: 65.9 ± 10.2 Control: 66.3 ± 11.3 | 2007–2009 | Standardized study questionnaire and government agencies, research studies | 6 |
D’Ippoliti D. et al., 2015 [42] | Population-based | M/W (82,169/83,440) | Italy | ≤35; 36–64; >65 | 1990–2010 | Population registries | 4 |
Steinmaus C.M. et al., 2014 [35] | Case-control | M/W (257/123) Cases: 92 Controls: 288 | Chile | 25–65 | 2007–2010 | Face to face interview and questionnaire | 8 |
Steinmaus C.M. et al., 2013 [36] | Case-control | M/W (601/271) Cases: 306 Controls: 640 | Chile | 30–39; 40–49; 50–59; 60–69; 70+ | 1958–1970 | Standardized questionnaire | 8 |
Hsu L. et al., 2013 [31] | Cohort | M/W (1231/1216) | Taiwan | 30–49; 50–59; 60–69; ≥70 | 1985–1989 | Interviewed at homewith a structured questionnaire | 5 |
Ferreccio C. et al., 2013 [37] | Case-control | M/W (646/300) Cases: 306 Controls: 640 | Chile | 30–39; 40–49; 50–59; 60–69; 70+ | 2007–2010 | Standardized study questionnaire and government agencies, research studies | 6 |
Dauphiné D.C. et al., 2013 [38] | Case-control | M/W (237/318) Cases: 196 Controls: 359 | Nevada and California (USA) | Case: mean 70.2 ± 10 Control: mean 69.0 ± 8.6 | 2002–2005 | Standardized study questionnaire by telephone | 8 |
Chen C. et al., 2010 [32] | Cohort | M/W (3481/3407) | Taiwan | ≤50; 50–54.9; 55–59.9; ≥60 | 1991–2002 | Home interview with a questionnaire | 7 |
Paul S. et al., 2013 [41] | Cross-sectional | 2005–2006 88 M, unexposed 83 W, unexposed 94 M, exposed 95, W exposed 2010–2011 87 M, unexposed 83 W, unexposed 85 M, exposed 91 W, exposed | India | 2005–2006 34.76 ± 9.52 unexposed 34.62 ± 12.93 exposed 2010–2011 39.05 ± 9.08 unexposed 38.65 ± 13.09 exposed | 2005–2010 | Expert physician screening | 4 |
Marano K.M. et al., 2012 [43] | Review of epidemiological data | Cigarette smokers, n = 991 Smokeless tobacco (SLT) consumers, n = 90 Non-consumers of tobacco n = 3385 | USA | ≥20 | 2003–2008 | Database (NHANES: National Health and Nutrition Examination Survey) | 2 |
Wadhwa S.K. et al., 2011 [39] | Case–control | Exposed subjects 98 M, referents without cancer 52 M, with lung cancer Non-exposed subjects 95 M, referents without cancer 55 M, with lung cancer | Pakistan | median 47 (range 35–65) | 2007–2009 | Face to face interview and medical database | 4 |
Olsson A.C. et al., 2011 [33] | Multicenter case-control | M/W (4054/1260) Cases: 2624 Controls:2690 M/W exposed (91/5) Exposed cases: 60 Exposed controls:36 | Czech Republic, Hungary, Poland, Romania, Russia and Slovakia | <45; 45 to 49; 50 to 54; 55 to 59; 60 to 64; 65 to 69; 70 to 74; 75+ | 1998–2002 | Face to face interview and questionnaire | 7 |
’t Mannetje A. et al., 2014 [34] | Multicenter case-control | M/W (4492/1464) Cases: 2852 Controls: 3104 Exposed cases: 70 Exposed controls:43 | Romania, Hungary, Poland, Russia, Slovakia, Czech Republic and UK | 25–45; 45–55; 55–65; 65 or older | 1998–2003 | Face to face interview and questionnaire | 7 |
Melak D. et al., 2014 [40] | Case-control | Cases: 94 Controls: 347 | Chile | >25 | 2007–2010 | Face to face interview, questionnaire and medical database | 8 |
3.3. Risk of Bias in Included Studies
3.4. Arsenic–Smoking Interaction
3.5. Outcome Measures
4. Discussion
4.1. Summary of Findings
- Five studies have identified a synergism between arsenic dose and cigarette smoking in the induction of lung carcinoma [30,32,36,37,39]. In particular, Su et al. [30] found a sub-multiplicative interaction and Ferreccio et al. [37] referred to a “greater than additive effects”, while the others defined a synergistic interaction.
- Synergism with smoking significantly changed the lung cancer risk when exposed to higher versus lower concentrations of arsenic.
- Some studies did not have complete quantitative characterization of exposure [34]. Conversely, Ferreccio et al. [37] asserted that “his study took place in an area with a history of high concentrations of arsenic in drinking water and good data on past exposure”. Moreover, detailed tobacco consumption was sometimes missing; for example, D’ippoliti et al. [42] reported indirect data on cigarette sales in different municipalities as an indicator of smoking status.
4.2. Strengths and Limitations of This Systematic Review
4.3. Interaction between Arsenic and Tobacco Smoke and Determination of Estimate Effect Values
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Author (Year) | Type of Exposure | Smoking Status | Estimate Effect Type | Estimate Effect Value | Type of Interaction | ||
---|---|---|---|---|---|---|---|
Su Z. et al., 2022 [30] | Occupational: tin miners (Chinese Yunnan tin corporation) | Never smoker Current smoker | ERR | Mean cumulative arsenic exposure: 83.6 mg/m3 | Sub-multiplicative | ||
Cumulative arseinc exposure < 3 mg/m3 * | |||||||
0.0033 (95% CI: 0.0014–0.0045) | |||||||
Cumulative arseinc exposure ≥ 3 mg/m3 * | |||||||
0.0056 (95% CI: 0.0035–0.0073) | |||||||
* Adjusted for smoking | |||||||
Fan Y. et al., 2016 [44] | Occupational: tin miners | Never smokers Former smoker Current smoker | HR | Cumulative arsenic exposure between 0 and 17,435 mg/m3 | Not reported | ||
1.00 | Never smokers * | ||||||
1.31 (95% CI: 0.77–2.24) | Former smokers * | ||||||
1.53 (95% CI: 0.95–2.44) | Current smokers * | ||||||
* adjusted for all prior lung diseases and different carcinogenic compounds exposure | |||||||
Steinmaus C.M. et al., 2015 [29] | Non-occupational: arsenic drinking water | Never smokers Ever smokers Heavier smokers (smoking > 20 cigs/day) | OR | LOW BMI, Unadjusted | Not reported | ||
1.00 | [<100 μg/L] | ||||||
1.24 (95% CI: 0.84–1.82) | [100–800 μg/L] | ||||||
2.47 (95% CI: 1.75–3.49) | [>800 μg/L] | ||||||
LOW BMI, Adjusted * | |||||||
1.00 | [<100 μg/L] | ||||||
1.17 (95% CI: 0.79–1.73) | [100–800 μg/L] | ||||||
2.31 (95% CI: 1.63–3.29) | [>800 μg/L] | ||||||
HIGH BMI, Unadjusted | |||||||
1.00 | [<100 μg/L] | ||||||
1.52 (95% CI: 0.56–4.15) | [100–800 μg/L] | ||||||
5.83 (95% CI: 1.73–19.64) | [>800 μg/L] | ||||||
HIGH BMI, Adjusted * | |||||||
1.00 | [<100 μg/L] | ||||||
1.48 (95% CI: 0.53–4.14) | [100–800 μg/L] | ||||||
6.98 (95% CI: 1.84–26.56) | [>800 μg/L] | ||||||
* Adjusted for age, sex and smoking | |||||||
D’Ippoliti D. et al., 2015 [42] | Non-occupational: arsenic drinking water | Not directly determined (used tobacco sales from municipal level assumption) | HR | Arsenic (10–20 μg/L) * | Not reported (dose response relationship) | ||
1.27 (95% CI: 1.18–1.38) | Natural causes, males | ||||||
1.47 (95% CI: 1.17–1.86) | Tracheas, bronchus and lung, males | ||||||
1.14 (95% CI: 1.05–1.24) | Natural causes, females | ||||||
1.80 (95% CI: 1.23–2.66) | Tracheas, bronchus and lung, females | ||||||
Cumulative Arsenic dose (CAI; 204.9–804.0 μg) * | |||||||
1.59 (95% CI: 1.45–1.74) | Natural causes, males | ||||||
2.03 (95% CI: 1.48–2.79) | Tracheas, bronchus and lung, males | ||||||
1.45 (95% CI: 1.32–1.58) | Natural causes, females | ||||||
1.66 (95% CI: 0.93–2.95) | Tracheas, bronchus and lung, females | ||||||
* Adjusted for age, calendar period, socio economic level, occupation in the ceramic industry, smoking sales and radon exposure | |||||||
Steinmaus C.M. et al., 2014 [35] | Non-occupational: arsenic drinking water | Never smokers Ever smokers Smoker > 10 cigs/day | OR | Unadjusted | Not reported | ||
1.00 | [<10 μg/L] | ||||||
1.46 (90% CI: 0.88–2.43) | [10–59.9 μg/L] | ||||||
1.90 (90% CI: 1.16–3.13) | [>59.9 μg/L] | ||||||
Adjusted * | |||||||
1.00 | [<10 μg/L] | ||||||
1.43 (90% CI: 0.82–2.52) | [10–59.9 μg/L] | ||||||
2.01 (90% CI: 1.14–3.52) | [>59.9 μg/L] | ||||||
* Adjusted for age, sex and smoking behavior | |||||||
Steinmaus C.M. et al., 2013 [36] | Non-occupational: arsenic drinking water | Never smoker Ever smoker | OR | Adjusted for smoking | Synergistic | ||
1.00 | [<11 μg/L] | ||||||
1.27 (95% CI: 0.81–1.98) | [11–90 μg/L] | ||||||
2.00 (95% CI: 1.24–3.24) | [91–335 μg/L] | ||||||
4.32 (95% CI: 2.60–7.17) | [>335 μg/L] | ||||||
Hsu L. et al., 2013 [31] | Non-occupational: arsenic drinking water | Non-smokers Smokers | HR | Non-smokers * | Not reported | ||
1.00 | Group 1 (no arsenical skin lesions) | ||||||
0.24 (95% CI: 0.03–1.79) | Group 2 (hyperpigmentation only) | ||||||
0.58 (95% CI: 0.08–4.26) | Group 3 (hyperkeratosis with or without hyperpigmentation) | ||||||
3.24 (95% CI: 1.54–6.80) | Group 4 (skin cancer without hyperkeratosis) | ||||||
2.22 (95% CI: 0.76–6.48) | Group 5 (skin cancer and hyperkeratosis) | ||||||
Smokers * | |||||||
2.20 (95% CI: 1.05–4.63) | Group 1 (no arsenical skin lesions) | ||||||
1.69 (95% CI: 0.46–6.20) | Group 2 (hyperpigmentation only) | ||||||
12.34 (95% CI: 4.79–31.75) | Group 3 (hyperkeratosis with or without hyperpigmentation) | ||||||
12.04 (95% CI: 5.12–28.31) | Group 4 (skin cancer without hyperkeratosis) | ||||||
23.54 (95% CI: 9.39–59.00) | Group 5 (skin cancer and hyperkeratosis) | ||||||
* Hazard ratios were adjusted for age, sex, body mass index, educational level and cumulative arsenic exposure | |||||||
Ferreccio C. et al., 2013 [37] | Non-occupational: arsenic drinking water | Never smokers Ever smoker Heavier smokers (smoking > 10 cigs/day) | OR | Never smoker * | Greater than additive | ||
1.00 | [0–34 μg/L] | ||||||
0.87 (95% CI: 0.42–1.81) | [35–260 μg/L] | ||||||
1.67 (95% CI: 0.78–3.56) | [>260 μg/L] | ||||||
Smoked > 10 cigs/day * | |||||||
4.36 (95% CI: 2.12–8.99) | [0–34 μg/L] | ||||||
6.94 (95% CI: 3.48–13.83) | [35–260 μg/L] | ||||||
20.80 (95% CI: 9.03–47.91) | [>260 μg/L] | ||||||
* Adjusted for age, sex, socioeconomic status, and second-hand tobacco smoke exposure. | |||||||
Dauphiné D.C. et al., 2013 [38] | Non-occupational: arsenic drinking water | Never smoker Ever smoker | OR | All subjects | Not reported | ||
1.00 | [≤10 μg/L] | ||||||
0.84 (95% CI:0.40–1.79) | [11–84 μg/L] | ||||||
1.39 (95% CI: 0.55–3.53) | [>85 µg/L] | ||||||
Smokers | |||||||
1.00 | [≤10 μg/L] | ||||||
0.66 (95% CI:0.30–1.44) | [11–84 μg/L] | ||||||
1.61 (95% CI: 0.59–4.38) | [>85 µg/L] | ||||||
Chen C. e al., 2010 [32] | Non-occupational: arsenic drinking water | Never smokers Current smokers (<25 cigs/day) Current smokers (≥25 cigs/day) | RR | Never smokers | Synergistic for squamous and small cell lung cancer | ||
1.00 | [<10 µg/L] | ||||||
1.22 (95% CI: 0.64–2.32) | [10–99.9 µg/L] | ||||||
1.32 (95% CI: 0.64–2.74) | [≥100 µg/L] | ||||||
Current smokers (<25 cigs/day) | |||||||
2.14 (95% CI: 0.79–5.79) | [<10 µg/L] | ||||||
1.52 (95% CI: 0.56–4.15) | [10–99.9 µg/L] | ||||||
5.30 (95% CI: 2.19–12.8) | [≥100 µg/L] | ||||||
Current smokers (≥25 cigs/day) | |||||||
4.08 (95% CI: 1.83–9.10) | [<10 µg/L] | ||||||
4.19 (95% CI: 1.92–9.14) | [10–99.9 µg/L] | ||||||
8.17 (95% CI: 3.74–17.9) | [≥100 µg/L] | ||||||
Paul S. et al., 2013 [41] | Non-occupational: arsenic drinking water | 2005–2006 63 M, unexposed 34 W, unexposed 57 M, exposed 31 W, exposed 2010–2011 69 M, unexposed 39 W, unexposed 53 M, exposed 33 W, exposed | Lung cancer death (number) | 2010–2011 * | Not reported | ||
1 individual among the unexposed died due to natural cause | |||||||
3 males, exposed | |||||||
0 female, exposed | |||||||
* tobacco consumption were matched between unexposed and exposed subjects | |||||||
Marano K.M et al., 2012 [43] | Occupational and non-occupational | Cigarette smokers Smokeless tobacco (SLT) consumers Non-consumers of tobacco | Geometric mean of urine arsenic (μg/g creatinine) | 39.1 for lung cancer Vs | Not reported | ||
7.98 (95% CI: 7.08–9.00) | Cigarette smokers * | ||||||
6.14 (95% CI: 4.86–7.74) | SLT consumers * | ||||||
9.56 (95% CI: 8.92–10.27) | Non-consumers of tobacco * | ||||||
* without lung cancer | |||||||
Wadhwa S.K. et al., 2011 [39] | Non-occupational: water, food and fish; locally made cigarette | 100% smokers | OR | Arsenic concentrations 3–15 fold higher than the permissible level (< 10 µg/L) 3.05 (95% CI: 1.26–7.36) (for lung cancer mortality among exposed lung cancer patients as compared to non-exposed lung cancer patients) | Synergistic | ||
Olsson A.C. et al., 2011 [33] | Occupational: different kinds of industries, e.g., wood work and painting | Never smoker Former smoker Current smoker | OR | Arsenic < 50% TLV (2011) = low; 50–150% TLV (2011) = medium; >150% TLV (2011) = high Adjusted for smoking (tobacco pack years) Men: 1.92 (95% CI: 1.15–3.20) Women: 1.05 (95% CI: 0.11–9.89) | Not reported | ||
’t Mannetje A. et al., 2014 [34] | Occupational: agriculture, miners and different kinds of industries | Never smokers Ex-smokers Ever smokers | OR | Arsenic concentration values not reported (low, medium and high exposure). Adjusted * 1.65 (95% CI: 1.05–2.58) * adjusted for age, center, sex, tobacco consumption and for other occupational exposures including metals | Not reported | ||
Melak D. et al., 2014 [40] | Non-occupational: arsenic drinking water | Never smokers Smokers | OR | Water arsenic < 200 µg/L | Not reported | ||
Crude | Adjusted * | ||||||
1.00 | 1.00 | %MMA < 12.5% | |||||
2.65 (95% CI: 1.18–5.94) | 2.48 (95% CI: 1.08–5.68) | %MMA ≥ 12.5% | |||||
Water arsenic ≥ 200 µg/L | |||||||
Crude | Adjusted * | ||||||
3.05 (95% CI: 1.56–5.95) | 3.16 (95% CI: 1.59–6.32) | %MMA < 12.5% | |||||
6.94 (95% CI:3.39–14.22) | 6.81 (95% CI:3.24–14.31) | %MMA ≥ 12.5% | |||||
* Odds ratios adjusted for age, gender and smoking | |||||||
%MMA = % monomethylarsenic in urine; the cut-off value of 12.5% divided the upper from the two lower tertiles |
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Folesani, G.; Galetti, M.; Petronini, P.G.; Mozzoni, P.; La Monica, S.; Cavallo, D.; Corradi, M. Interaction between Occupational and Non-Occupational Arsenic Exposure and Tobacco Smoke on Lung Cancerogenesis: A Systematic Review. Int. J. Environ. Res. Public Health 2023, 20, 4167. https://doi.org/10.3390/ijerph20054167
Folesani G, Galetti M, Petronini PG, Mozzoni P, La Monica S, Cavallo D, Corradi M. Interaction between Occupational and Non-Occupational Arsenic Exposure and Tobacco Smoke on Lung Cancerogenesis: A Systematic Review. International Journal of Environmental Research and Public Health. 2023; 20(5):4167. https://doi.org/10.3390/ijerph20054167
Chicago/Turabian StyleFolesani, Giuseppina, Maricla Galetti, Pier Giorgio Petronini, Paola Mozzoni, Silvia La Monica, Delia Cavallo, and Massimo Corradi. 2023. "Interaction between Occupational and Non-Occupational Arsenic Exposure and Tobacco Smoke on Lung Cancerogenesis: A Systematic Review" International Journal of Environmental Research and Public Health 20, no. 5: 4167. https://doi.org/10.3390/ijerph20054167