Heavy metals in biological samples of cancer patients: a systematic literature review.

Breast cancer Gastric cancer Heavy metals Lung cancer Prostate cancer Trace elements

Journal

Biometals : an international journal on the role of metal ions in biology, biochemistry, and medicine
ISSN: 1572-8773
Titre abrégé: Biometals
Pays: Netherlands
ID NLM: 9208478

Informations de publication

Date de publication:
12 Feb 2024
Historique:
received: 24 03 2023
accepted: 07 01 2024
medline: 13 2 2024
pubmed: 13 2 2024
entrez: 12 2 2024
Statut: aheadofprint

Résumé

The majority of the so-called heavy metals are suspected to be involved in a number of pathologies and play a role in human carcinogenesis. Some of them (i.e. arsenic (As), cadmium (Cd), chromium (Cr), lead (Pb), mercury (Hg) and nickel (Ni)) have been defined as carcinogens, increasing the susceptibility of tumor development and progression in humans. Moreover, Ni, Cr, Cd, Hg, and Pb together with zinc (Zn) and iron (Fe), may be capable of stimulating the progression of breast cancer and reducing a patient's sensitivity to treatment through alterations to DNA methylation. In patients with gastric cancers, levels of various heavy metals are augmented and hypothesized to amplify the expression of the human epidermal growth factor receptor type 2 gene. Cd may increase the risk of lung cancer development and have a negative impact on the overall survival of lung cancer patients. To investigate the relation between heavy metals in biological samples and risk, occurrence and survival cancer individuals, a comprehensive review work was performed, with a focus on breast, lung, prostate and gastric cancers. An extensive search strategy was devised to ensure relevant literature could be identified, with the PECO framework being adopted to facilitate this and identify key search terms. As evidenced in this review, there is substantial data to support the hypothesis that heavy metals influence tumor development and progression. Unluckily the number of papers dealing with the determination of metals directly in samples from cancer tissues is still rather limited, so we decided to expand the scope of this review also to analyses carried out on other biological samples, as urine, plasma, hair, nail, etc. The studies reviewed showed that several limitations and current knowledge gaps are present in the literature that require further investigation to improve our comprehension of the impact of different heavy metals on tumorigenesis.

Identifiants

pubmed: 38347295
doi: 10.1007/s10534-024-00583-4
pii: 10.1007/s10534-024-00583-4
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : This research was funded by FAR 2019 of Serenella Medici and Ciriaco Carru
ID : FAR 2019

Informations de copyright

© 2024. The Author(s).

Références

Peana M, Pelucelli A, Medici S, Cappai R, Nurchi VM, Zoroddu MA (2021) Metal toxicity and speciation: a review. Curr Med Chem 28:7190–7208
pubmed: 33761850 doi: 10.2174/0929867328666210324161205
Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7:60
pubmed: 26109881 pmcid: 4427717 doi: 10.2478/intox-2014-0009
Aaseth J, Gerhardsson L, Skaug MA, Alexander J (2016) General chemistry of metal toxicity and basis for metal complexation. Chelation therapy in the treatment of metal intoxication. Academic Press, pp 1–33
Jomova K, Makova M, Alomar SY, Alwasel SH, Nepovimova E, Kuca K, Rhodes CJ, Valko M (2022) Essential metals in health and disease. Chemico-Biol Interact. https://doi.org/10.1016/j.cbi.2022.110173
doi: 10.1016/j.cbi.2022.110173
Islam MR, Akash S, Jony MH, Alam MN, Nowrin FT, Rahman MM, Rauf A, Thiruvengadam M (2023) Exploring the potential function of trace elements in human health: a therapeutic perspective. Mol Cell Biochem. https://doi.org/10.1007/s11010-022-04638-3
doi: 10.1007/s11010-022-04638-3 pubmed: 36637616
Kumar A, Misra BB (2019) Challenges and opportunities in cancer metabolomics. Proteomics 19:e1900042. https://doi.org/10.1002/pmic.201900042
doi: 10.1002/pmic.201900042 pubmed: 30950571
Bradl H (2005) Sources and origins of heavy metals. Interface science and technology, 6th edn. Elsevier, pp 1–27
Azevedo JA, Carter BS, Meng F, Turner DL, Dai M, Schatzberg AF, Barchas JD, Jones EG, Bunney WE, Myers RM (2016) The microrna network is altered in anterior cingulate cortex of patients with unipolar and bipolar depression. J Psychiatri Res. https://doi.org/10.1016/j.jpsychires.2016.07.012
doi: 10.1016/j.jpsychires.2016.07.012
Ahmad M, Islam S, Rahman S, Haque M,  Islam M. (2010) Heavy metals in water, sediment and some fishes of buriganga river, bangladesh.
Wang Y, Liu Y, Zhan W, Zheng K, Wang J, Zhang C, Chen R (2020) Stabilization of heavy metal-contaminated soils by biochar: challenges and recommendations. Sci Total Environ 729:139060
pubmed: 32498182 doi: 10.1016/j.scitotenv.2020.139060
Sardar K, Ali S, Hameed S, Afzal S, Fatima S, Shakoor MB, Bharwana SA (2013) Heavy metals contamination and what are the impacts on living organisms. Greener J Environ Manag Public Safety 2:172–179
doi: 10.15580/GJEMPS.2013.4.060413652
Jaishankar M, Tseten T, Anbalagan N (2014) Mathew and K. N. J. I. t. Beeregowda. Toxic Mechanism Health Eff some Heavy Met 7:60
Fu Z, Xi S (2020) The effects of heavy metals on human metabolism. Toxicol Mech Methods 30:167–176
pubmed: 31818169 doi: 10.1080/15376516.2019.1701594
O’Carroll RE, Masterton G, Dougall N, Ebmeier KP, Goodwin GM (1995) The neuropsychiatric sequelae of mercury poisoning. The mad hatter’s disease revisited. Br J Psychiatry 167:95–98
pubmed: 7551618 doi: 10.1192/bjp.167.1.95
Harada M (1995) Minamata disease: methylmercury poisoning in Japan caused by environmental pollution. Crit Rev Toxicol 25:1–24
pubmed: 7734058 doi: 10.3109/10408449509089885
Canfield, R., T. Jusko and K. J. R. Kordas (2005) Environmental lead exposure and children’s cognitive function. 31: 293
Balali-Mood M, Naseri K, Tahergorabi Z, Khazdair MR, Sadeghi M (2021) Toxic mechanisms of five heavy metals: mercury, lead, chromium, cadmium, and arsenic. Front Pharmacol 12:643972. https://doi.org/10.3389/fphar.2021.643972
doi: 10.3389/fphar.2021.643972 pubmed: 33927623 pmcid: 8078867
Hossini H, Shafie B, Niri AD, Nazari M, Esfahlan AJ, Ahmadpour M, Nazmara Z, Ahmadimanesh M (2022) Makhdoumi and N. Mirzaei. A comprehensive review on human health effects of chromium: insights on induced toxicity. Environ Sci Pollut Res 29:70686–70705
doi: 10.1007/s11356-022-22705-6
Ferlay J, Colombet M, Soerjomataram I, Parkin DM, Piñeros M, Znaor A, Bray F (2021) Cancer statistics for the year 2020: an overview. Int J Cancer 149:778–789
doi: 10.1002/ijc.33588
Siegel RL, Miller KD, Jemal A (2019) Cancer statistics, 2019. CA Cancer J Clin 69:7–34. https://doi.org/10.3322/caac.21551
doi: 10.3322/caac.21551 pubmed: 30620402
Lappano R, Malaguarnera R, Belfiore A, Maggiolini M (2017) Recent advances on the stimulatory effects of metals in breast cancer. Mol Cell Endocrinol 457:49–56.
pubmed: 27765682 doi: 10.1016/j.mce.2016.10.017
Lee NW, Wang HY, Du CL, Yuan TH, Chen CY, Yu CJ, Chan CC (2022) Air-polluted environmental heavy metal exposure increase lung cancer incidence and mortality: a population-based longitudinal cohort study. Sci Total Environ 810:152186.
pubmed: 34883183 doi: 10.1016/j.scitotenv.2021.152186
Yuan W, Yang N, Li X (2016) Advances in understanding how heavy metal pollution triggers gastric cancer. BioMed Res Int. https://doi.org/10.1155/2016/7825432
doi: 10.1155/2016/7825432 pubmed: 28078284 pmcid: 5203887
Boffetta P (1993) Carcinogenicity of trace elements with reference to evaluations made by the international agency for research on cancer. Scandinavian J Work, Environ Health 19:67–70
Kim HS, Kim YJ, Seo YR (2015) An overview of carcinogenic heavy metal molecular toxicity mechanism and prevention. J Cancer Prev 20:232–240
pubmed: 26734585 pmcid: 4699750 doi: 10.15430/JCP.2015.20.4.232
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. Exp Suppl 101:133–64. https://doi.org/10.1007/978-3-7643-8340-4_6
doi: 10.1007/978-3-7643-8340-4_6 pubmed: 22945569
Jomova K, Raptova R, Alomar SY, Alwasel SH, Nepovimova E, Kuca K, Valko M (2023) Reactive oxygen species, toxicity, oxidative stress, and antioxidants: chronic diseases and aging. Arch Toxicol 97:2499–2574
pubmed: 37597078 pmcid: 10475008 doi: 10.1007/s00204-023-03562-9
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. Mol, Clinical Environ Toxicol: Environ Toxicol 3:133–64
doi: 10.1007/978-3-7643-8340-4_6
Ohsawa M (1997) Biomarkers for responses to heavy metals. Cancer Causes Control 8:514–517
pubmed: 9498908 doi: 10.1023/A:1018473708846
Farombi E, Adelowo O, Ajimoko Y (2007) Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria Ogun river. Int J Environ Res Public Health 4:158–165
pubmed: 17617680 pmcid: 3728582 doi: 10.3390/ijerph2007040011
Maresca V, Fusaro L, Sorbo S, Siciliano A, Loppi S, Paoli L, Monaci F, Piscopo M, Guida M, Galdiero E (2018) Functional and structural biomarkers to monitor heavy metal pollution of one of the most contaminated freshwater sites in southern europe. Ecotoxicol Environ Safety 163:665–673
pubmed: 30098556 doi: 10.1016/j.ecoenv.2018.07.122
Malhotra J, Malvezzi M, Negri E, Vecchia CL, Boffetta P (2016) Risk factors for lung cancer worldwide. Eur Respir J 48:889–902.
pubmed: 27174888 doi: 10.1183/13993003.00359-2016
Huang HH, Huang JY, Lung CC, Wu CL, Ho CC, Sun YH, Ko PC, Su SY, Chen SC, Liaw YP (2013) Cell-type specificity of lung cancer associated with low-dose soil heavy metal contamination in Taiwan: an ecological study. BMC Public Health 13:330. https://doi.org/10.1186/1471-2458-13-330
doi: 10.1186/1471-2458-13-330 pubmed: 23575356 pmcid: 3643867
Hong Y-S, Song K-H, Chung JY (2014) Health effects of chronic arsenic exposure. J Prev Med Public Health 47:245
pubmed: 25284195 pmcid: 4186552 doi: 10.3961/jpmph.14.035
Tran JQ, Dranikov A, Iannucci A, Wagner WP, LoBello J, Allen J, Weiss GJ (2014) Heavy metal content in thoracic tissue samples from patients withand without NSCLC. Lung Cancer Int. https://doi.org/10.1155/2014/853158
doi: 10.1155/2014/853158 pubmed: 26316947 pmcid: 4437387
Pietrzak S, Wójcik J, Baszuk P, Marciniak W, Wojtyś M, Dębniak T, Cybulski C, Gronwald J, Alchimowicz J, Masojć BJB (2021) Influence of the levels of arsenic, cadmium, mercury and lead on overall survival in lung cancer. Biomolecules 11:1160
pubmed: 34439826 pmcid: 8392714 doi: 10.3390/biom11081160
Bai Y, Wang G, Fu W, Lu Y, Wei W, Chen W, Wu X, Meng H, Feng Y, Liu Y et al (2019) Circulating essential metals and lung cancer: risk assessment and potential molecular effects. Environ Int 127:685–693.
pubmed: 30991224 doi: 10.1016/j.envint.2019.04.021
Solomon EI, Heppner DE, Johnston EM, Ginsbach JW, Cirera J, Qayyum M, Kieber-Emmons MT, Kjaergaard CH, Hadt RG, Tian L (2014) Copper active sites in biology. Chem Rev 114:3659–3853.
pubmed: 24588098 pmcid: 4040215 doi: 10.1021/cr400327t
Ge EJ, Bush AI, Casini A, Cobine PA, Cross JR, DeNicola GM, Dou QP, Franz KJ, Gohil VM, Gupta S et al (2022) Connecting copper and cancer: from transition metal signalling to metalloplasia. Nat Rev Cancer 22:102–113.
pubmed: 34764459 doi: 10.1038/s41568-021-00417-2
Krishnamoorthy L, Cotruvo JA Jr., Chan J, Kaluarachchi H, Muchenditsi A, Pendyala VS, Jia S, Aron AT, Ackerman CM, Wal MN et al (2016) Copper regulates cyclic-amp-dependent lipolysis. Nat Chem Biol 12:586–592.
pubmed: 27272565 pmcid: 4955676 doi: 10.1038/nchembio.2098
Turski ML, Brady DC, Kim HJ, Kim BE, Nose Y, Counter CM, Winge DR, Thiele DJ (2012) A novel role for copper in ras/mitogen-activated protein kinase signaling. Mol Cell Biol 32:1284–1295. https://doi.org/10.1128/MCB.05722-11
doi: 10.1128/MCB.05722-11 pubmed: 22290441 pmcid: 3302449
Tsang T, Posimo JM, Gudiel AA, Cicchini M, Feldser DM, Brady DC (2020) Copper is an essential regulator of the autophagic kinases ulk1/2 to drive lung adenocarcinoma. Nature Cell Biol 22:412–24. https://doi.org/10.1038/s41556-020-0481-4
doi: 10.1038/s41556-020-0481-4 pubmed: 32203415
Yun YH, Wang Y, Yang ED, Jing X (2022) Cuproptosis-related gene-slc31a1 fdx1 and atp7b-polymorphisms are associated with risk of lung cancer. Pharmacogenomics Personalized Med 15:733
doi: 10.2147/PGPM.S372824
Cobanoglu U, Demir H, Sayir F, Duran M, Mergan D (2010) Some mineral, trace element and heavy metal concentrations in lung cancer. Asian Pacific J Cancer Prev 11:1383–88
Torti SV, Manz DH, Paul BT, Blanchette-Farra N, Torti FM (2018) Iron and cancer. Annu Rev Nutr 38:97–125
pubmed: 30130469 pmcid: 8118195 doi: 10.1146/annurev-nutr-082117-051732
Alemán MR, Santolaria F, Batista N, Marıa J, González-Reimers E, Milena A, Llanos M, Gómez-Sirvent JC (2002) Leptin role in advanced lung cancer. A mediator of the acute phase response or a marker of the status of nutrition? Cytokine 19:21–26
pubmed: 12200109 doi: 10.1006/cyto.2002.1051
Fracchia A, Ubbiali A, El Bitar O, Pacetti M, Sommariva E, Arreghini M, Longhini E, Bonalumi GP (1999) A comparative study on ferritin concentration in serum and bilateral bronchoalveolar lavage fluid of patients with peripheral lung cancer versus control subjects. Oncology 56:181–188.
pubmed: 10202271 doi: 10.1159/000011962
Shi HB, Li XD, Jiang JT, Zhao WQ, Ji M, Wu CP (2014) Serum ferritin is elevated in advanced non-small cell lung cancer patients and is associated with efficacy of platinum-based chemotherapy. J Cancer Res Ther 10:2014. https://doi.org/10.4103/0973-1482.139156
doi: 10.4103/0973-1482.139156
Xiong R, He R, Liu B, Jiang W, Wang B, Li N, Geng Q (2021) Ferroptosis: a new promising target for lung cancer therapy. Oxid Med Cell Longev 2021:8457521.
pubmed: 34616505 pmcid: 8487823 doi: 10.1155/2021/8457521
Kukulj S, Jaganjac M, Boranic M, Krizanac S, Santic Z, Poljak-Blazi M (2010) Altered iron metabolism, inflammation, transferrin receptors, and ferritin expression in non-small-cell lung cancer. Med Oncol 27:268–277.
pubmed: 19308738 doi: 10.1007/s12032-009-9203-2
Wu HK, Wang M, Raman JD, McDonald AC (2021) Association between urinary arsenic, blood cadmium, blood lead, and blood mercury levels and serum prostate-specific antigen in a population-based cohort of men in the United States. PLoS ONE 16:e0250744
pubmed: 33891655 pmcid: 8064543 doi: 10.1371/journal.pone.0250744
Coradduzza D, Congiargiu A, Chen Z, Zinellu A, Carru C, Medici S (2023) Ferroptosis and senescence: a systematic review. Int J Mol Sci 24:3658.
pubmed: 36835065 pmcid: 9963234 doi: 10.3390/ijms24043658
Benderli Cihan Y, Sozen S, Ozturk Yildirim S (2011) Trace elements and heavy metals in hair of stage iii breast cancer patients. Biol Trace Elem Res 144:360–79.
pubmed: 21660533 doi: 10.1007/s12011-011-9104-z
Khalaf EA, Abduljaleel SA, Al-Jassani HMJTI (2021) Appraisal of trace elements and heavy metals levels in breast cancer patients of Basrah Province. Toxicol Int 28:8–14
Siddiqui MKJ, Jyoti S, Singh PK, Mehrotra K, Singh Sarangi R (2006) Comparison of some trace elements concentration in blood, tumor free breast and tumor tissues of women with benign and malignant breast lesions: an Indian study. Environ Int 32:630–37. https://doi.org/10.1016/j.envint.2006.02.002
doi: 10.1016/j.envint.2006.02.002 pubmed: 16580070
Marouf BH (2018) Association between serum heavy metals level and cancer incidence in Darbandikhan and Kalar area, Kurdistan region, Iraq. Nigerian J Clin Pract 21:766–71. https://doi.org/10.4103/njcp.njcp_384_16
doi: 10.4103/njcp.njcp_384_16
Aquino NB, Sevigny MB, Sabangan J, Louie MC (2012) The role of cadmium and nickel in estrogen receptor signaling and breast cancer: metalloestrogens or not? J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 30:189–224. https://doi.org/10.1080/10590501.2012.705159
doi: 10.1080/10590501.2012.705159 pubmed: 22970719 pmcid: 3476837
Grattan BJ (2012) Freake. Zinc and cancer: implications for liv-1 in breast cancer. Nutrients 4:648–675.
pubmed: 22852056 pmcid: 3407987 doi: 10.3390/nu4070648
Ionescu JG (2006) Heavy metal accumulation in malignant tumours as basis for a new integrative therapy model. Anti-Aging Ther 9:189–201
Li L, Zhang MH, Men YH, Wang W, Zhang WD (2020) Heavy metals interfere with plasma metabolites, including lipids and amino acids, in patients with breast cancer. Oncol Lett 19:2925–33. https://doi.org/10.3892/ol.2020.11402
doi: 10.3892/ol.2020.11402 pubmed: 32218848 pmcid: 7068226
Men Y, Li L, Zhang F, Kong X, Zhang W, Hao C, Wang G (2020) Evaluation of heavy metals and metabolites in the urine of patients with breast cancer. Oncol Lett 19:1331–1337.
pubmed: 31966065
O’Brien KM, White AJ, Jackson BP, Karagas MR, Sandler DP, Weinberg CRJ (2019) Toenail-based Metal Concentrations and young-onset Breast cancer 188:646–655
Pala V, Agnoli C, Cavalleri A, Rinaldi S, Orlandi R, Segrado F, Venturelli E, Vinceti M, Krogh V, Sieri S (2022) Prediagnostic levels of copper and zinc and breast cancer risk in the ordet cohort. Cancer Epidemiol Biomarkers Prev 31:1209–1215.
pubmed: 35255128 doi: 10.1158/1055-9965.EPI-21-1252
White AJ, Weinberg CR, O’Meara ES, Sandler DP, Sprague BL (2019) Airborne metals and polycyclic aromatic hydrocarbons in relation to mammographic breast density. Breast Cancer Res 21:24.
pubmed: 30760301 pmcid: 6373138 doi: 10.1186/s13058-019-1110-7
Liu L, Chen J, Liu C, Luo Y, Chen J, Fu Y, Xu Y, Wu H, Li X, Wang H (2022) Relationships between biological heavy metals and breast cancer: a systematic review and meta-analysis. Front Nutr 9:838762
pubmed: 35782923 pmcid: 9245072 doi: 10.3389/fnut.2022.838762
Jouybari L, Saei Ghare Naz M, Sanagoo A, Kiani F, Sayehmiri F, Sayehmiri K, Hasanpour Dehkordi A (2018) Toxic elements as biomarkers for breast cancer: a meta-analysis study. Cancer Manage Res. https://doi.org/10.2147/CMAR.S151324
doi: 10.2147/CMAR.S151324
Jouybari L, Kiani F, Islami F, Sanagoo A, Sayehmiri F, Hosnedlova B, Dosa MD, Kizek R, Chirumbolo S, Bjorklund G (2020) Copper concentrations in breast cancer: a systematic review and meta-analysis. Curr Med Chem 27:6373–6383.
pubmed: 31533596 doi: 10.2174/0929867326666190918120209
Chang VC, Cotterchio M, Khoo E (2019) Iron intake, body iron status, and risk of breast cancer: a systematic review and meta-analysis. BMC Cancer 19:543.
pubmed: 31170936 pmcid: 6555759 doi: 10.1186/s12885-019-5642-0
Rawla P (2019) Epidemiology of prostate cancer. World J Oncol 10:63–89.
pubmed: 31068988 pmcid: 6497009 doi: 10.14740/wjon1191
Neslund-Dudas C, Kandegedara A, Kryvenko ON, Gupta N, Rogers C, Rybicki BA, Dou QP, Mitra B (2014) Prostate tissue metal levels and prostate cancer recurrence in smokers. Biol Trace Elem Res 157:107–112
pubmed: 24385087 pmcid: 4096659 doi: 10.1007/s12011-013-9874-6
Vella V, Malaguarnera R, Lappano R, Maggiolini M, Belfiore A (2017) Recent views of heavy metals as possible risk factors and potential preventive and therapeutic agents in prostate cancer. Mol Cell Endocrinol 457:57–72
pubmed: 27773847 doi: 10.1016/j.mce.2016.10.020
Jomova K, Jenisova Z, Feszterova M, Baros S, Liska J, Hudecova D, Rhodes CJ, Valko M (2011) Arsenic: toxicity, oxidative stress and human disease. J Appl Toxicol 31:95–107.
pubmed: 21321970 doi: 10.1002/jat.1649
Lim JT, Tan YQ, Valeri L, Lee J, Geok PP, Chia SE, Ong CN, Seow WJ (2019) Association between serum heavy metals and prostate cancer risk-a multiple metal analysis. Environ Int 132:105109
pubmed: 31491608 doi: 10.1016/j.envint.2019.105109
Sarafanov AG, Todorov TI, Centeno JA, Macias V, Gao W, Liang WM, Beam C, Gray MA, Kajdacsy-Balla AA (2011) Prostate cancer outcome and tissue levels of metal ions. Prostate 71:1231–1238
pubmed: 21271612 doi: 10.1002/pros.21339
Karimi G, Shahar S, Homayouni N, Rajikan R, Bakar NFA, Othman MS (2012) Association between trace element and heavy metal levels in hair and nail with prostate cancer. Asian Pac J Cancer Prev 13:4249–4253
pubmed: 23167323 doi: 10.7314/APJCP.2012.13.9.4249
Sohrabi M, Nikkhah M, Sohrabi M, Farimani AR, Shahi MM, Ziaie H, Shirmardi S, Kohi Z, Salehpour D, Tameshkel FS et al (2021) Evaluating tissue levels of the eight trace elements and heavy metals among esophagus and gastric cancer patients: a comparison between cancerous and non-cancerous tissues. J Trace Elem Med Biol 68:126761
pubmed: 34139544 doi: 10.1016/j.jtemb.2021.126761
Wang L, Miao C, He Y, Li H, Zhang S, Li K, Liu H, Li W, Zhao J, Xu Y et al (2022) The influence of heavy metals on gastric tumorigenesis. J Oncol 2022:6425133. https://doi.org/10.1155/2022/6425133
doi: 10.1155/2022/6425133 pubmed: 35669240 pmcid: 9167133
Feng L, Du J, Yao C, Jiang Z, Li T, Zhang Q, Guo X, Yu M, Xia H, Shi L (2020) Ribosomal DNA copy number is associated with p53 status and levels of heavy metals in gastrectomy specimens from gastric cancer patients. Environ Int 138:105593
pubmed: 32120062 doi: 10.1016/j.envint.2020.105593
Fonseca-Nunes A, Agudo A, Aranda N, Arija V, Cross AJ, Molina E, Sanchez MJ, Bueno-de-Mesquita HB, Siersema P, Weiderpass E et al (2015) Body iron status and gastric cancer risk in the eurgast study. Int J Cancer 137:2904–2914. https://doi.org/10.1002/ijc.29669
doi: 10.1002/ijc.29669 pubmed: 26135329 pmcid: 6284801
Morgan RL, Whaley P, Thayer KA, Schunemann HJ (2018) Identifying the peco: a framework for formulating good questions to explore the association of environmental and other exposures with health outcomes. Environ Int 121:1027–1031.
pubmed: 30166065 pmcid: 6908441 doi: 10.1016/j.envint.2018.07.015

Auteurs

Donatella Coradduzza (D)

Department of Biomedical Sciences, University of Sassari, Viale San Pietro 43/B, 07100, Sassari, Italy. donatella.coradduzza0@gmail.com.

Antonella Congiargiu (A)

Department of Biomedical Sciences, University of Sassari, Viale San Pietro 43/B, 07100, Sassari, Italy.

Emanuela Azara (E)

Institute of Biomolecular Chemistry, National Research Council, Sassari, Italy.

Ismaeil Mohammed Abulkahar Mammani (IMA)

College of Health Sciences, University of Duhok, Duhok, Iraq.

Maria Rosaria De Miglio (MR)

Department of Medical, Surgery and Experimental Sciences, University of Sassari, Sassari, Italy.

Angelo Zinellu (A)

Department of Biomedical Sciences, University of Sassari, Viale San Pietro 43/B, 07100, Sassari, Italy.

Ciriaco Carru (C)

Department of Biomedical Sciences, University of Sassari, Viale San Pietro 43/B, 07100, Sassari, Italy. carru@uniss.com.

Serenella Medici (S)

Department of Chemistry and Pharmacy, University of Sassari, Vienna 2, 07100, Sassari, Italy.

Classifications MeSH