Abstract
Purpose
Gallbladder cancers (GBC), unique to certain geographical regions, are lethal digestive tract cancers, disproportionately affecting women, with limited information on risk factors.
Methods
We evaluated the association between household cooking fuel and GBC risk in a hospital-based case–control study conducted in the North-East and East Indian states of Assam and Bihar. We explored the potential mediation by diet, fire-vents, ‘daily exposure duration’ and parity (among women). We recruited biopsy-confirmed GBC (n = 214) men and women aged 30–69 years between 2019 and 2021, and controls frequency-matched by age, sex and region (n = 166). Information about cooking fuel, lifestyle, personal and family history, female reproductive factors, socio-demographics, and anthropometrics was collected. We tested associations using multivariable logistic regression analyses.
Results
All participants (73.4% women) were categorised based on predominant cooking fuel use. Group-1: LPG (Liquefied Petroleum Gas) users in the previous 20 years and above without concurrent biomass use (26.15%); Group-2: LPG users in the previous 20 years and above with concurrent secondary biomass use (15.9%); Group-3: Biomass users for ≥ 20 years (57.95%). Compared to group-1, accounting for confounders, GBC risk was higher in group-2 [OR: 2.02; 95% CI: 1.00–4.07] and group-3 [OR: 2.01; 95% CI: 1.08–3.73] (p-trend:0.020). These associations strengthened among women that attenuated with high daily consumption of fruits-vegetables but not with fire-vents, ‘daily exposure duration’ or parity.
Conclusion
Biomass burning was associated with a high-risk for GBC and should be considered as a modifiable risk factor for GBC. Clean cooking fuel can potentially mitigate, and a healthy diet can partially reduce the risk among women.
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Data availability
The data used for the study are available with the PI and can be obtained with reasonable request.
References
Health Effects Institute. State of Global Air. 2019-2020. Special Report. Boston, MA: Health Effects Institute. Available at https://www.stateofglobalair.org/; Accessed on 17th September 2023.
Global Burden of Disease Collaborative Network. Global Burden of Disease Study 2019 (GBD 2019) Results. Seattle, United States: Institute for Health Metrics and Evaluation (IHME), 2020. Available from http://ghdx.healthdata.org/gbd-results-tool.
IARCMonographs on the Identification of Carcinogenic hazards to Humans [Internet]. Last update: 30 November 2021 [cited 22 February 2022]. Available from: https://monographs.iarc.who.int/agents-classified-by-the-iarc/.
Sheikh M, Poustchi H, Pourshams A, Khoshnia M, Gharavi A, Zahedi M et al (2020) Household fuel use and the risk of gastrointestinal cancers: the Golestan cohort study. Environ Health Perspect 128(6):67002
Bruce N, Dherani M, Liu R, Hosgood HD 3rd, Sapkota A, Smith KR et al (2015) Does household use of biomass fuel cause lung cancer? A systematic review and evaluation of the evidence for the GBD 2010 study. Thorax 70(5):433–441
Josyula S, Lin J, Xue X, Rothman N, Lan Q, Rohan TE et al (2015) Household air pollution and cancers other than lung: a meta-analysis. Environ Health 14:24
Okello S, Akello SJ, Dwomoh E, Byaruhanga E, Opio CK, Zhang R et al (2019) Biomass fuel as a risk factor for esophageal squamous cell carcinoma: a systematic review and meta-analysis. Environ Health 18(1):60
White AJ, Sandler DP (2017) Indoor wood-burning stove and fireplace use and breast cancer in a prospective cohort study. Environ Health Perspect 125(7):077011
White AJ, Teitelbaum SL, Stellman SD, Beyea J, Steck SE, Mordukhovich I et al (2014) Indoor air pollution exposure from use of indoor stoves and fireplaces in association with breast cancer: a case-control study. Environ Health 13:108
Hundal R, Shaffer EA (2014) Gallbladder cancer: epidemiology and outcome. Clin Epidemiol 6:99–109
Dutta U, Bush N, Kalsi D, Popli P, Kapoor VK (2019) Epidemiology of gallbladder cancer in India. Chin Clin Oncol 8(4):33
Three-Year Report of Population Based Cancer Registries 2012–14. Indian Council of Medical Research. National Cancer Registry Programme. Available from: ICMR - National Centre for Disease Informatics and Research (ncdirindia.org) accessed [20-05-2022]
Ferlay J SH, Bray F, Forman D, Mathers C, Parkin DM. Ferlay J, Ervik M, Lam F, Colombet M, Mery L, Piñeros M, Znaor A, Soerjomataram I, Bray F (2018). Global Cancer Observatory: Cancer Today. Lyon, France: International Agency for Research on Cancer. Available from: https://gco.iarc.fr/today, accessed [20- 06- 2020]. 2010 ed. Lyon: International Agency for Research on Cancer; 2020.
Randi G, Franceschi S, La Vecchia C (2006) Gallbladder cancer worldwide: geographical distribution and risk factors. Int J Cancer 118(7):1591–1602
Pandey M. Environmental pollutants in gallbladder carcinogenesis. 2006(0022–4790 (Print)).
Lugo A, Peveri G, Gallus S (2020) Should we consider gallbladder cancer a new smoking-related cancer? A comprehensive meta-analysis focused on dose-response relationships. Int J Cancer 146(12):3304–3311
Liu T, Song Y, Chen R, Zheng R, Wang S, Li L (2020) Solid fuel use for heating and risks of breast and cervical cancer mortality in China. Environ Res 186:109578
Kayamba V, Heimburger DC, Morgan DR, Atadzhanov M, Kelly P (2017) Exposure to biomass smoke as a risk factor for oesophageal and gastric cancer in low-income populations: A systematic review. Malawi Med J 29(2):212–217
World Cancer Research Fund International. Diet, Nutrition, Physical Activity and Cancer: A Global Perspective. 2018.Available at: Gallbladder cancer | What causes gallbladder cancer? | WCRF International Accessed on:04 Junly 2023.
International Institute of Population Sciences. National Family Health Survey (NFHS-5); Available at http://rchiips.org/nfhs/; accessed on Feb1st 2022. Mumbai, India: IIPS; 2019–2021.
Shridhar K, Krishnatreya M, Sarkar S, Kumar R, Kondal D, Kuriakose S et al (2023) Chronic exposure to drinking water arsenic and gallbladder cancer risk: preliminary evidence from endemic regions of India. Cancer Epidemiol Biomarkers Prev 32(3):406–414
Bowen L, Bharathi AV, Kinra S, Destavola B, Ness A, Ebrahim S (2012) Development and evaluation of a semi-quantitative food frequency questionnaire for use in urban and rural India. Asia Pac J Clin Nutr 21(3):355–360
Ravindran RD, Vashist P, Gupta SK, Young IS, Maraini G, Camparini M et al (2011) Inverse association of vitamin C with cataract in older people in India. Ophthalmology 118(10):1958–65.e2
Ravindran RD, Vashist P, Gupta SK, Young IS, Maraini G, Camparini M et al (2011) Prevalence and risk factors for vitamin C deficiency in north and south India: a two centre population based study in people aged 60 years and over. PLoS ONE 6(12):e28588
Gopalan C (1971) Nutritive value of Indian foods. National Institute of Nutrition, Hyderabad
Department of Chronic Diseases and Health Promotion WHO. Global Physical Activity Questionaire 2.; Available at: http://www.who.int/chp/steps/GPAQ%20Instrument%20and%20Analysis%20Guide%20v2.pdf Last accessed: July 2018.
Hennessy S, Bilker WB, Berlin JA, Strom BL (1999) Factors influencing the optimal control-to-case ratio in matched case-control studies. Am J Epidemiol 149(2):195–197
Hodson KE, Bowman RJ, Mafwiri M, Wood M, Mhoro V, Cox SE (2011) Low folate status and indoor pollution are risk factors for endemic optic neuropathy in Tanzania. Br J Ophthalmol 95(10):1361–1364
Miller CN, Rayalam S (2017) The role of micronutrients in the response to ambient air pollutants: Potential mechanisms and suggestions for research design. J Toxicol Environ Health B Crit Rev 20(1):38–53
Reid BC, Ghazarian AA, DeMarini DM, Sapkota A, Jack D, Lan Q et al (2012) Research opportunities for cancer associated with indoor air pollution from solid-fuel combustion. Environ Health Perspect 120(11):1495–1498
Corraini P, Olsen M, Pedersen L, Dekkers OM, Vandenbroucke JP (2017) Effect modification, interaction and mediation: an overview of theoretical insights for clinical investigators. Clin Epidemiol 9:331–338
Mhatre S, Lacey B, Sherliker P, Chatterjee N, Rajaraman P, Goel M et al (2022) Reproductive factors and gall-bladder cancer, and the effect of common genetic variants on these associations: a case-control study in India. Int J Epidemiol 51(3):789–798
Fritz MS, Mackinnon DP (2007) Required sample size to detect the mediated effect. Psychol Sci 18(3):233–239
Shridhar K, Kinra S, Gupta R, Khandelwal S, Prabhakaran D, Cox SE et al (2019) Serum calcium concentrations, chronic inflammation and glucose metabolism: a cross-sectional analysis in the Andhra Pradesh Children and Parents Study (APCaPS). Curr Develop Nut. https://doi.org/10.1093/cdn/nzy085
Panda D, Sharma A, Shukla NK, Jaiswal R, Dwivedi S, Raina V et al (2013) Gall bladder cancer and the role of dietary and lifestyle factors: a case-control study in a North Indian population. Eur J Cancer Prev 22(5):431–437
Liu T, Chen R, Zheng R, Li L, Wang S (2021) Household air pollution from solid cooking fuel combustion and female breast cancer. Front Public Health 9:677851
Hvidtfeldt UA, Severi G, Andersen ZJ, Atkinson R, Bauwelinck M, Bellander T et al (2021) Long-term low-level ambient air pollution exposure and risk of lung cancer—A pooled analysis of 7 European cohorts. Environ Int 146:106249
Turner MC, Andersen ZJ, Baccarelli A, Diver WR, Gapstur SM, Pope CA 3rd et al (2020) Outdoor air pollution and cancer: An overview of the current evidence and public health recommendations. CA Cancer J Clin 70:460
Bai L, Shin S, Burnett RT, Kwong JC, Hystad P, van Donkelaar A et al (2020) Exposure to ambient air pollution and the incidence of lung cancer and breast cancer in the Ontario Population Health and Environment Cohort. Int J Cancer 146(9):2450–2459
Peluso M, Ceppi M, Munnia A, Puntoni R, Parodi S (2001) Analysis of 13 32P-DNA postlabeling studies on occupational cohorts exposed to air pollution. Am J Epidemiol 153(6):546–558
Ramesh A, Walker SA, Hood DB, Guillén MD, Schneider K, Weyand EH (2004) Bioavailability and risk assessment of orally ingested polycyclic aromatic hydrocarbons. Int J Toxicol 23(5):301–333
Behera D, Balamugesh T (2005) Indoor air pollution as a risk factor for lung cancer in women. J Assoc Physicians India 53:190–192
Das A, Krishnamurthy A, Ramshankar V, Sagar TG, Swaminathan R (2017) The increasing challenge of never smokers with adenocarcinoma lung: Need to look beyond tobacco exposure. Indian J Cancer 54(1):172–177
Acknowledgements
The authors thank Drs. Aastha Aggrawal, Ruby Gupta, Sumita Sarma Barthakur and Gayatri Bharali and Ms. Kritika Anand for their support during study inception.
Funding
This study was funded by the Public Health Foundation of India’s Centre for Environmental Health core funds to Dr. Krithiga Shridhar as part of her Research Development Grant Fellowship (2018–2021). Funders had no role in study design, data collection, analysis, or publication.
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Krithiga Shridhar: Conceptualization, Funding acquisition, Formal Analysis, Writing-Original Draft, Supervision, Resources, Project Administration. Manigreeva Krishnatreya: Resources, Supervision, Project Administration. review & editing Ranjit Kumar: Resources, Supervision, Project Administration, review & editing. Dimple Kondal: Formal Analysis, review & editing. Mouchumee Bhattacharyya: Resources, Project Administration. review & editing. Banti Kalita: Investigation, Data Curation, review & editing. Prakriti Snehil: Investigation, Data Curation, review & editing. Amulya K. Singh: Resources, Project Administration. review & editing. Amal Chandra Kataki: Resources, Supervision, review & editing. Ashok Ghosh: Resources, Supervision, review & editing. D. Prabhakaran: Resources, Supervision, review & editing. Poornima Prabhakaran: conceptualization, Resources, Supervision, review & editing. Preet K. Dhillon: Conceptualization, Methodology, supervision, review & editing.
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The authors declare no conflicts of interest. We declare the commercial affiliation of one of our authors (Genentech Roche, CA, USA). The funder provided support in the form of salary for the author (PKD) but did not have any additional role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
Ethical approval
Ethics committee approval was obtained from all participating institutions, which included the coordinating centre Public Health Foundation of India (TRC IEC-389/18), as well as from study hospitals (BBCI-TMC/Misc-119/MEC/231/2019; 09/RMRI/EC/2019; SSN/IEC/JAN/2019/29), and the procedures followed were in accordance with the ethical standards of the committee. All study participants provided informed consent. Information sheets in local language were given to the participants, and their signatures were obtained in the consent forms. Strict COVID control protocol as approved by the ethical committee was followed during COVID-Pandemic.
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Shridhar, K., Krishnatreya, M., Kumar, R. et al. Household cooking fuel and gallbladder cancer risk: a multi-centre case–control study in India. Cancer Causes Control 35, 281–292 (2024). https://doi.org/10.1007/s10552-023-01787-8
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DOI: https://doi.org/10.1007/s10552-023-01787-8