Hostname: page-component-669899f699-tpknm Total loading time: 0 Render date: 2025-04-30T15:47:10.472Z Has data issue: false hasContentIssue false

Association of dietary manganese intake and the IL1R1 rs3917225 polymorphism with thyroid cancer risk: a prospective cohort study in Korea

Published online by Cambridge University Press:  13 November 2024

Tao Thi Tran
Affiliation:
Department of Cancer AI and Digital Health, Graduate School of Cancer Science and Policy, Goyang-si, Republic of Korea Faculty of Public Health, University of Medicine and Pharmacy, Hue University, Hue city, Vietnam
Ha Thi Mien Nguyen
Affiliation:
Department of Cancer Control and Population Health, Graduate School of Cancer Science and Policy, Goyang-si, Republic of Korea
Madhawa Gunathilake
Affiliation:
Department of Cancer AI and Digital Health, Graduate School of Cancer Science and Policy, Goyang-si, Republic of Korea
Jeonghee Lee
Affiliation:
Department of Cancer AI and Digital Health, Graduate School of Cancer Science and Policy, Goyang-si, Republic of Korea
Jeongseon Kim*
Affiliation:
Department of Cancer AI and Digital Health, Graduate School of Cancer Science and Policy, Goyang-si, Republic of Korea
*
*Corresponding author: Dr Jeongseon Kim, email [email protected]

Abstract

Dietary Mn intake may have a beneficial effect in reducing cancer risk; however, its association with thyroid cancer (TC) risk remains inadequately understood. Additionally, Mn was associated with inflammation markers. Thus, we examined whether dietary Mn intake emerges a protective role against TC and whether this preventative effect has an interaction with IL1 receptor type 1 (IL1R1) rs3917225. The prospective study was designed at National Cancer Center in Korea between October 2007 and December 2020 including 17 754 participants. We identified TC cases by following participants until December 2020. Mn intake was collected using a semiquantitative food frequency questionnaire (SQFFQ). Genotyping was performed to determine IL1R1 rs3917225. The hazard ratios (HR) and 95 % confidence interval (CI) were calculated with a Cox proportional hazards model. We ascertained 108 incident TC cases throughout follow-up duration. Dietary Mn intake was found to be inversely associated with TC risk (HR (95 % CI)=0·64 (0·44, 0·95)). However, IL1R1 rs3917225 seemed to modify this association; the protective effect was limited to G-allele carriers (HR = 0·30 (0·11, 0·86), P interaction=0·028). A higher dietary Mn was suggested to be a protective factor against TC. Additionally, we drew a potential biological interaction between Mn intake and IL1R1 rs3917225 with a greater effect among individuals with a minor allele. This implies that when considering the cancer-preventive role of Mn, it is important to account for the influence of inflammatory gene participation.

Type
Research Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

Footnotes

These authors have contributed equally to this work and share first authorship.

References

Sung, H, Ferlay, J, Siegel, RL, et al. (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA:Cancer J Clin 71, 209249.Google ScholarPubMed
Kang, MJ, Jung, KW, Bang, SH, et al. (2023) Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2020. Cancer Res Treat 55, 385399.CrossRefGoogle ScholarPubMed
Wiltshire, JJ, Drake, TM, Uttley, L, et al. (2016) Systematic review of trends in the incidence rates of thyroid cancer. Thyroid 26, 15411552.CrossRefGoogle ScholarPubMed
Kim, J, Gosnell, JE & Roman, SA (2020) Geographic influences in the global rise of thyroid cancer. Nat Rev Endocrinol 16, 1729.CrossRefGoogle ScholarPubMed
Barrea, L, Pugliese, G, Frias-Toral, E, et al. (2021) Diet as a possible influencing factor in thyroid cancer incidence: the point of view of the nutritionist. Panminerva Med 63, 349360.CrossRefGoogle ScholarPubMed
Fiore, M, Cristaldi, A, Okatyeva, V, et al. (2020) Dietary habits and thyroid cancer risk: a hospital-based case–control study in Sicily (South Italy). Food Chem Toxicol 146, 111778.CrossRefGoogle Scholar
Choi, WJ & Kim, J (2014) Dietary factors and the risk of thyroid cancer: a review. Clin Nutr Res 3, 7588.CrossRefGoogle ScholarPubMed
D’Avanzo, B, Ron, E, La Vecchia, C, et al. (1997) Selected micronutrient intake and thyroid carcinoma risk. Cancer 79, 21862192.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Chen, P, Bornhorst, J & Aschner, M (2018) Manganese metabolism in humans. Front Biosci (Landmark Ed) 23, 16551679.CrossRefGoogle ScholarPubMed
Soldin, OP & Aschner, M (2007). Effects of manganese on thyroid hormone homeostasis: potential links. NeuroToxicology 28, 951956.CrossRefGoogle ScholarPubMed
Wróblewski, M, Wróblewska, J, Nuszkiewicz, J, et al. (2023) The role of selected trace elements in oxidoreductive homeostasis in patients with thyroid diseases. Int J Mol Sci 24, 4840.CrossRefGoogle ScholarPubMed
Obsekov, V, Ghassabian, A, Mukhopadhyay, S, et al. (2023) Manganese and thyroid function in the national health and nutrition examination survey, 2011–2012. Environ Res 222, 115371.CrossRefGoogle ScholarPubMed
Liu, M, Song, J, Jiang, Y, et al. (2021) A case-control study on the association of mineral elements exposure and thyroid tumor and goiter. Ecotoxicol Environ Saf 208, 111615.CrossRefGoogle ScholarPubMed
Liotti, F, Visciano, C & Melillo, RM (2012) Inflammation in thyroid oncogenesis. Am J Cancer Res 2, 286297.Google ScholarPubMed
Xiong, Z, Sun, Y, Wu, J, et al. (2019) Genetic polymorphisms in IL1R1 and IL1R2 are associated with susceptibility to thyroid cancer in the Chinese Han population. J Gene Med 21, e3093.CrossRefGoogle ScholarPubMed
Park, SW, Kim, MK, Kwon, KH, et al. (2012) Association between a promoter polymorphism (rs2192752, -1028A/C) of interleukin 1 receptor, type I (IL1R1) and location of papillary thyroid carcinoma in a Korean population. Int J Immunogenet 39, 501507.CrossRefGoogle Scholar
Tian, Y, Sun, Y, Wu, J, et al. (2020) Impact of IL1R1 polymorphisms on the risk of head and neck cancer in Chinese Han population. Gene 757, 144927.CrossRefGoogle ScholarPubMed
Chang, NC, Yang, HL, Dai, CY, et al. (2020) The association of genetic polymorphisms in interleukin-1 receptors type 1 and type 2 with age-related hearing impairment in a Taiwanese population: a case control study. J Otolaryngol Head Neck Surg 49, 16.CrossRefGoogle Scholar
Gong, JH, Lo, K, Liu, Q, et al. (2020) Dietary manganese, plasma markers of inflammation, and the development of type 2 diabetes in postmenopausal women: findings from the women’s health initiative. Diabetes Care 43, 13441351.CrossRefGoogle Scholar
Kresovich, JK, Bulka, CM, Joyce, BT, et al. (2018) The inflammatory potential of dietary manganese in a cohort of elderly men. Biol Trace Elem Res 183, 4957.CrossRefGoogle Scholar
Kim, J (2014) Cancer screenee cohort study of the national cancer center in South Korea. Epidemiol Health 36, e2014013.CrossRefGoogle ScholarPubMed
Nguyen, LTD, Gunathilake, M, Lee, J, et al. (2023) Association between dietary habits and incident thyroid cancer: a prospective cohort study. Front Nutr 10, 1104925.CrossRefGoogle ScholarPubMed
Ho, D, Imai, K, King, G, et al. (2011) MatchIt: nonparametric preprocessing for parametric causal inference. J Stat Software 42, 128 CrossRefGoogle Scholar
Ahn, Y, Kwon, E, Shim, JE, et al. (2007) Validation and reproducibility of food frequency questionnaire for Korean genome epidemiologic study. Eur J Clin Nutr 61, 14351441.CrossRefGoogle ScholarPubMed
Oh, JY, Yang, YJ, Kim, BS, et al. (2007) Validity and reliability of Korean version of international physical activity questionnaire (IPAQ) short form. J na Acad Fam Med 28, 532541.Google Scholar
Lu, Y, Kweon, SS, Cai, Q, et al. (2020) Identification of novel loci and new risk variant in known loci for colorectal cancer risk in East Asians. Cancer Epidemiol Biomarkers Prev 29, 477486.CrossRefGoogle ScholarPubMed
Van Gerwen, M, Alerte, E, Alsen, M, et al. (2022) The role of heavy metals in thyroid cancer: a meta-analysis. J Trace Elem Med Biol 69, 126900.CrossRefGoogle ScholarPubMed
Zhou, Q, Xue, S, Zhang, L, et al. (2022) Trace elements and the thyroid. Front Endocrinol 13, 904889.CrossRefGoogle ScholarPubMed
Lv, M, Chen, M, Zhang, R, et al. (2020) Manganese is critical for antitumor immune responses via cGAS-STING and improves the efficacy of clinical immunotherapy. Cell Res 30, 966979.CrossRefGoogle ScholarPubMed
Kasai, F, Eshak, ES, Tamakoshi, A, et al. (2023) Dietary manganese intake and risk of liver cancer in Japanese men and women: the JACC Study. Nutr Cancer 75, 154163.CrossRefGoogle ScholarPubMed
Ma, X, Yang, Y, Li, HL, et al. (2017) Dietary trace element intake and liver cancer risk: results from two population-based cohorts in China. Int J Cancer 140, 10501059.CrossRefGoogle ScholarPubMed
Yeo, Y, Shin, DW, Han, K, et al. (2022) Smoking, alcohol consumption, and the risk of thyroid cancer: a population-based Korean cohort study of 10 million people. Thyroid 32, 440448.CrossRefGoogle ScholarPubMed
Lee, JH, Chai, YJ & Yi, KH (2021) Effect of cigarette smoking on thyroid cancer: meta-analysis. Endocrinol Metab (Seoul, Korea) 36, 590598.CrossRefGoogle ScholarPubMed
Kitahara, CM, Linet, MS, Beane Freeman, LE, et al. (2012) Cigarette smoking, alcohol intake, and thyroid cancer risk: a pooled analysis of five prospective studies in the United States. Cancer Causes Control 23, 16151624.CrossRefGoogle Scholar
Anagianni, S & Tuschl, K (2019) Genetic disorders of manganese metabolism. Curr Neurol Neurosci Rep 19, 33.CrossRefGoogle ScholarPubMed
Maouche, N, Meskine, D, Alamir, B, et al. (2015) Trace elements profile is associated with insulin resistance syndrome and oxidative damage in thyroid disorders: manganese and selenium interest in Algerian participants with dysthyroidism. J Trace Elem Med Biol 32, 112121.CrossRefGoogle ScholarPubMed
Li, L & Yang, X (2018) The essential element manganese, oxidative stress, and metabolic diseases: links and interactions. Oxid Med Cell Longev 2018, 7580707.CrossRefGoogle ScholarPubMed
Coelho, RG, Fortunato, RS & Carvalho, DP (2018) Metabolic reprogramming in thyroid carcinoma. Front Oncol 8, 82.CrossRefGoogle ScholarPubMed
Owumi, SE & Dim, UJ (2019) Manganese suppresses oxidative stress, inflammation and caspase-3 activation in rats exposed to chlorpyrifos. Toxicol Rep 6, 202209.CrossRefGoogle ScholarPubMed
Li, C & Zhou, HM (2011) The role of manganese superoxide dismutase in inflammation defense. Enzyme Res 2011, 387176.CrossRefGoogle ScholarPubMed
Aung, MT, Meeker, JD, Boss, J, et al. (2020) Manganese is associated with increased plasma interleukin-1β during pregnancy, within a mixtures analysis framework of urinary trace metals. Reprod Toxicol (Elmsford, NY) 93, 4353.CrossRefGoogle ScholarPubMed
Supplementary material: File

Tran et al. supplementary material

Tran et al. supplementary material
Download Tran et al. supplementary material(File)
File 15.6 KB