Abstract
Tobacco use has a negative impact on health due to its relationship with the development of high-mortality diseases, such as pulmonary cancer. However, the effect of cadmium (Cd), present in tobacco smoke, on the development of joint diseases has been scarcely studied. The objective of this review is to discuss the evidence regarding the mechanisms by which Cd exposure, through tobacco smoke, may lead to the development of osteoarthritis (OA), osteoporosis (OP), and rheumatoid arthritis (RA). There’s evidence suggesting a string association between moderate to severe OA development and tobacco use, and that a higher blood concentration of Cd can trigger oxidative stress (OS) and inflammation, favoring cartilage loss. At the bone level, the Cd that is inhaled through tobacco smoke affects bone mineral density, resulting in OP mediated by a decrease in the antioxidant enzymes, which favors the bone resorption process. In RA, tobacco use promotes the citrullination process through Cd exposure and increases OS and inflammation. Understanding how tobacco use can increase the damage at the articular level mediated by a toxic metal, i.e., Cd, is important. Finally, we propose prevention, control, and treatment strategies for frequently disabling diseases, such as OA, OP, and RA to reduce its prevalence in the population.
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04 August 2021
A Correction to this paper has been published: https://doi.org/10.1007/s12011-021-02853-5
References
Al-Bashaireh AM, Haddad LG, Weaver M, Kelly DL, Chengguo X, Yoon S (2018) The effect of tobacco smoking on musculoskeletal health: a systematic review. J Environ Public Health. https://doi.org/10.1155/2018/4184190
Attia AM, Attalla SM, Shaat RM, El Dafrawy MM (2014) A study of the toxic effects of some environmental pollutants and cigarette smoking in the development of osteoarthritis. Adv Environ Biol 8(15):33–40
Afridi HI, Kazi TG, Brabazon D, Naher S (2011) Association between essential trace and toxic elements in scalp hair samples of smokers rheumatoid arthritis subjects. Sci Total Environ 412–413:93–100. https://doi.org/10.1016/j.scitotenv.2011.09.033
Ashraf MW (2012) Levels of heavy metals in popular cigarette brands and exposure to these metals via smoking. ScientificWorldJournal 2012:729430. https://doi.org/10.1100/2012/729430
Galazyn-Sidorczuk M, Brzóska MM, Moniuszko-Jakoniuk J (2008) Estimation of Polish cigarettes contamination with cadmium and lead, and exposure to these metals via smoking. Environ Monit Assess 137(1–3):481–493. https://doi.org/10.1007/s10661-007-9783-2
Sigel A, Sigel H, Sigel, RK (2013) Cadmium: from toxicity to essentiality. https://doi.org/10.1007/978-94-007-5179-8
Arroyo VS, Flores KM, Ortiz LB, Gómez-Quiroz LE, Gutiérrez-Ruiz MC (2012) Liver and cadmium toxicity. J Drug Metab Toxicol S5:001
Martínez-Flores K, Arroyo V, Ortiz L, Gomez-Quiroz L, Gutiérrez-Ruiz MC (2013) Cadmio: efectos sobre la salud. Respuesta celular y molecular. Acta Toxicol Argent 21:33–49
Bizoń A, Milnerowicz H (2014) Participation of metallothionein and superoxide dismutase in the blood of smoking smelters. Int J Occup Med Environ Health 27(2):326–334. https://doi.org/10.2478/s13382-014-0258-8
Pizent A, Lazarus M, Kovačić J, Tariba Lovaković B, Brčić Karačonji I, Živković Semren T, Sekovanić A, Orct T, Branović-Čakanić K, Brajenović N, Jurič A, Miškulin I, Škrgatić L, Stasenko S, Mioč T, Jurasović J, Piasek M (2020) Cigarette smoking during pregnancy: effects on antioxidant enzymes, metallothionein and trace elements in mother-newborn pairs. Biomolecules 10(6):892. https://doi.org/10.3390/biom10060892
Hashmi GM, Shah MH (2012) Comparative assessment of essential and toxic metals in the blood of rheumatoid arthritis patients and healthy subjects. Biol Trace Elem Res 146(1):13–22. https://doi.org/10.1007/s12011-011-9220-9
Faroon, O, Ashizawa A, Wright S, Tucker P, Jenkins K, Ingerman L, Rudisill C (2012) Toxicological profile for cadmium. Agency for Toxic Substances and Disease Registry (US)
Kazi TG, Jalbani N, Kazi N, Jamali MK, Arain MB, Afridi HI, Kandhro A, Pirzado Z (2008) Evaluation of toxic metals in blood and urine samples of chronic renal failure patients, before and after dialysis. Ren Fail 30(7):737–745. https://doi.org/10.1080/08860220802212999
Zhang S, Sun L, Zhang J, Liu S, Han J, Liu Y (2020) Adverse impact of heavy metals on bone cells and bone metabolism dependently and independently through anemia. Adv Sci (Weinh) 7(19):2000383. https://doi.org/10.1002/advs.202000383
Navarro-Compán V, Melguizo-Madrid E, Hernández-Cruz B, Santos-Rey K, Leyva-Prado C, González-Martín C, Navarro-Sarabia F, González-Rodríguez C (2013) Interaction between oxidative stress and smoking is associated with an increased risk of rheumatoid arthritis: a case-control study. Rheumatology (Oxford) 52(3):487–493. https://doi.org/10.1093/rheumatology/kes286
Novikov DA, Swensen SJ, Buza JA, Gidumal RH, Strauss EJ (2016) The effect of smoking on ACL reconstruction: a systematic review. Phys Sportsmed 44(4):335–341. https://doi.org/10.1080/00913847.2016.1216239
World Health Organization (2015) WHO global report on trends in prevalence of tobacco smoking 2015. World Health Organization
Dubé CE, Liu SH, Driban JB, McAlindon TE, Eaton CB, Lapane KL (2016) The relationship between smoking and knee osteoarthritis in the Osteoarthritis Initiative. Osteoarthritis Cartilage 24(3):465–472. https://doi.org/10.1016/j.joca.2015.09.015
Hui M, Doherty M, Zhang W (2011) Does smoking protect against osteoarthritis? Meta-analysis of observational studies. Ann Rheum Dis 70(7):1231–1237. https://doi.org/10.1136/ard.2010.142323
Kong L, Wang L, Meng F, Cao J, Shen Y (2017) Association between smoking and risk of knee osteoarthritis: a systematic review and meta-analysis. Osteoarthritis Cartilage 25(6):809–816. https://doi.org/10.1016/j.joca.2016.12.020
Abate M, Vanni D, Pantalone A, Salini V (2013) Cigarette smoking and musculoskeletal disorders. Muscles Ligaments Tendons J 3(2):63–69. https://doi.org/10.11138/mltj/2013.3.2.063
Lanocha-Arendarczyk N, Kosik-Bogacka DI, Prokopowicz A, Kalisinska E, Sokolowski S, Karaczun M, Zietek P, Podlasińska J, Pilarczyk B, Tomza-Marciniak A, Baranowska-Bosiacka I, Gutowska I, Safranow K, Chlubek D (2015) The effect of risk factors on the levels of chemical elements in the tibial plateau of patients with osteoarthritis following knee surgery. Biomed Res Int 2015:650282. https://doi.org/10.1155/2015/650282
Yessica Eduviges ZC, Martínez-Nava G, Reyes-Hinojosa D, Mendoza-Soto L, Fernández-Torres J, López-Reyes A, Olivos-Meza A, Armienta-Hernández MA, Ruíz-Huerta EA, de Jesús G-G, Sandoval BV, Landa-Solís C, Sánchez-Sánchez R, Suarez-Ahedo C, Lozada-Pérez CA, Gutiérrez-Ruiz MC, Clavijo-Cornejo D, Pineda C, Jacobo-Albavera L, Domínguez-Pérez M, Martínez-Flores K (2020) Impact of cadmium toxicity on cartilage loss in a 3D in vitro model. Environ Toxicol Pharmacol 74:103307. https://doi.org/10.1016/j.etap.2019.103307
Chen X, Wang G, Li X, Gan C, Zhu G, Jin T, Wang Z (2013) Environmental level of cadmium exposure stimulates osteoclasts formation in male rats. Food Chem Toxicol 60:530–535. https://doi.org/10.1016/j.fct.2013.08.017
Afridi HI, Kazi TG, Brabazon D, Naher S (2012) Interaction between zinc, cadmium, and lead in scalp hair samples of Pakistani and Irish smokers rheumatoid arthritis subjects in relation to controls. Biol Trace Elem Res 148(2):139–147. https://doi.org/10.1007/s12011-012-9352-6
Martínez-Nava GA, Mendoza-Soto L, Fernández-Torres J, Zamudio-Cuevas Y, Reyes-Hinojosa D, Plata-Rodríguez R, Olivos-Meza A, Ruíz-Huerta EA, Armienta-Hernández MA, Hernández-Álvarez E, Vargas-Sandoval B, Landa-Solís C, Suárez-Ahedo C, Barbier OC, Narváez-Morales J, Del Razo LM, Camacho-Rea MC, Martínez-Flores K (2020) Effect of cadmium on the concentration of essential metals in a human chondrocyte micromass culture. J Trace Elem Med Biol 62:126614. https://doi.org/10.1016/j.jtemb.2020.126614
Borba-Pinheiro CJ, Drigo AJ, de Alencar Carvalho MC, da Silva NS, Dantas EH (2011) Factors that contribute to low bone density in postmenopausal women in different Amazonian communities. Ther Adv Musculoskelet Dis 3(2):81–90. https://doi.org/10.1177/1759720X11401674
Wu ZJ, Zhao P, Liu B, Yuan ZC (2016) Effect of cigarette smoking on risk of hip fracture in men: a meta-analysis of 14 prospective cohort studies. PLoS ONE 11(12):e0168990. https://doi.org/10.1371/journal.pone.0168990
Ratajczak AE, Szymczak-Tomczak A, Rychter AM, Zawada A, Dobrowolska A, Krela-Kaźmierczak I (2021) Impact of cigarette smoking on the risk of osteoporosis in inflammatory bowel diseases. J Clin Med 10(7):1515. https://doi.org/10.3390/jcm10071515
Buha A, Jugdaohsingh R, Matovic V, Bulat Z, Antonijevic B, Kerns JG, Goodship A, Hart A, Powell JJ (2019) Bone mineral health is sensitively related to environmental cadmium exposure- experimental and human data. Environ Res 176:108539. https://doi.org/10.1016/j.envres.2019.108539
Li H, Wallin M, Barregard L, Sallsten G, Lundh T, Ohlsson C, Mellström D, Andersson EM (2020) Smoking-induced risk of osteoporosis is partly mediated by cadmium from tobacco smoke: the MrOS Sweden Study. J Bone Miner Res 35(8):1424–1429. https://doi.org/10.1002/jbmr.4014
Kim ES, Shin S, Lee YJ, Ha IH (2021) Association between blood cadmium levels and the risk of osteopenia and osteoporosis in Korean post-menopausal women. Arch Osteoporos 16(1):22. https://doi.org/10.1007/s11657-021-00887-9
Jalili C, Kazemi M, Taheri E, Mohammadi H, Boozari B, Hadi A, Moradi S (2020) Exposure to heavy metals and the risk of osteopenia or osteoporosis: a systematic review and meta-analysis. Osteoporos Int 31(9):1671–1682. https://doi.org/10.1007/s00198-020-05429-6
Roczniak W, Brodziak-Dopierała B, Cipora E, Jakóbik-Kolon A, Kluczka J, Babuśka-Roczniak M (2017) Factors that affect the content of cadmium, nickel, copper and zinc in tissues of the knee. Biol Trace Elem Res 178(2):201–209. https://doi.org/10.1007/s12011-016-0927-5
Dorn LD, Pabst S, Sontag LM, Kalkwarf HJ, Hillman JB, Susman EJ (2011) Bone mass, depressive, and anxiety symptoms in adolescent girls: variation by smoking and alcohol use. J Adolesc Health 49(5):498–504. https://doi.org/10.1016/j.jadohealth.2011.03.008
Lucas R, Fraga S, Ramos E, Barros H (2012) Early initiation of smoking and alcohol drinking as a predictor of lower forearm bone mineral density in late adolescence: a cohort study in girls. PLoS ONE 7(10):e46940. https://doi.org/10.1371/journal.pone.0046940
Taha MM, Mahdy-Abdallah H, Shahy EM, Ibrahim KS, Elserougy S (2018) Impact of occupational cadmium exposure on bone in sewage workers. Int J Occup Environ Health 24(3–4):101–108. https://doi.org/10.1080/10773525.2018.1518745
Youness ER, Mohammed NA, Morsy FA (2012) Cadmium impact and osteoporosis: mechanism of action. Toxicol Mech Methods 22(7):560–567. https://doi.org/10.3109/15376516.2012.702796
Brzóska MM, Rogalska J, Roszczenko A, Galazyn-Sidorczuk M, Tomczyk M (2016) The mechanism of the osteoprotective action of a polyphenol-rich Aronia melanocarpa extract during chronic exposure to cadmium is mediated by the oxidative defense System. Planta Med 82(7):621–631. https://doi.org/10.1055/s-0042-103593
Rani A, Kumar A, Lal A, Pant M (2014) Cellular mechanisms of cadmium-induced toxicity: a review. Int J Environ Health Res 24(4):378–399. https://doi.org/10.1080/09603123.2013.835032
Reyes-Hinojosa D, Lozada-Pérez CA, Zamudio Cuevas Y, López-Reyes A, Martínez-Nava G, Fernández-Torres J, Olivos-Meza A, Landa-Solis C, Gutiérrez-Ruiz MC, Rojas Del Castillo E, Martínez-Flores K (2019) Toxicity of cadmium in musculoskeletal diseases. Environ Toxicol Pharmacol 72:103219. https://doi.org/10.1016/j.etap.2019.103219
Engler A, Niederer F, Klein K, Gay RE, Kyburz D, Camici GG, Gay S, Ospelt C (2014) SIRT6 regulates the cigarette smoke-induced signalling in rheumatoid arthritis synovial fibroblasts. J Mol Med (Berl) 92(7):757–767. https://doi.org/10.1007/s00109-014-1139-0
Sugiyama D, Nishimura K, Tamaki K, Tsuji G, Nakazawa T, Morinobu A, Kumagai S (2010) Impact of smoking as a risk factor for developing rheumatoid arthritis: a meta-analysis of observational studies. Ann Rheum Dis 69(1):70–81. https://doi.org/10.1136/ard.2008.096487
Lahiri M, Morgan C, Symmons DP, Bruce IN (2012) Modifiable risk factors for RA: prevention, better than cure? Rheumatology (Oxford) 51(3):499–512. https://doi.org/10.1093/rheumatology/ker299
Di Giuseppe D, Discacciati A, Orsini N, Wolk A (2014) Cigarette smoking and risk of rheumatoid arthritis: a dose-response meta-analysis. Arthritis Res Ther 16(2):R61. https://doi.org/10.1186/ar4498
Di Giuseppe D, Orsini N, Alfredsson L, Askling J, Wolk A (2013) Cigarette smoking and smoking cessation in relation to risk of rheumatoid arthritis in women. Arthritis Res Ther 15(2):R56. https://doi.org/10.1186/ar4218
Okamoto S, Adachi M, Chujo S, Yamada K, Akita K, Itoh S, Takii T, Hayakawa K, Onozaki K (2011) Etiological role of cigarette smoking in rheumatoid arthritis: nasal exposure to cigarette smoke condensate extracts augments the development of collagen-induced arthritis in mice. Biochem Biophys Res Commun 404(4):1088–1092. https://doi.org/10.1016/j.bbrc.2010.12.118
Chujo S, Okamoto S, Sunahara R, Adachi M, Yamada K, Hayashi H, Takii T, Hayakawa K, Onozaki K (2010) Cigarette smoke condensate extracts augment collagen-induced arthritis in mice. Int Immunopharmacol 10(10):11941199. https://doi.org/10.1016/j.intimp.2010.06.26
Hutchinson D (2015) Cadmium, one of the villains behind the curtain: has exposure to cadmium helped to pull the strings of seropositive rheumatoid arthritis pathogenesis all along? Int J Rheum Dis 18(5):570–576. https://doi.org/10.1111/1756-185X.12673
Bonaventura P, Courbon G, Lamboux A, Lavocat F, Marotte H, Albarède F, Miossec P (2017) Protective effect of low dose intra-articular cadmium on inflammation and joint destruction in arthritis. Sci Rep 7(1):2415. https://doi.org/10.1038/s41598-017-02611-5
Afridi HI, Talpur FN, Kazi TG, Brabazon D (2015) Estimation of toxic elements in the samples of different cigarettes and their effect on the essential elemental status in the biological samples of Irish smoker rheumatoid arthritis consumers. Environ Monit Assess 187(4):157. https://doi.org/10.1007/s10661-015-4353-5
Joo SH, Lee J, Hutchinson D, Song YW (2019) Prevalence of rheumatoid arthritis in relation to serum cadmium concentrations: cross-sectional study using Korean National Health and Nutrition Examination Survey (KNHANES) data. BMJ Open 9(1):e023233. https://doi.org/10.1136/bmjopen-2018-023233
Cates M, Hutchinson D (2015) Cadmium the missing link between smoking and increased rheumatoid disease activity. Ann Rheum Dis 74(1):e1. https://doi.org/10.1136/annrheumdis-2014-206538
Murphy D, Bellis K, Hutchinson D (2018) Occupational dust and cigarette smoke exposure might link rheumatoid arthritis to COPD. Lancet Respir Med 6(8):e36. https://doi.org/10.1016/S2213-2600(18)30188-7
Pinto E, Cruz M, Ramos P, Santos A, Almeida A (2017) Metals transfer from tobacco to cigarette smoke: evidences in smokers’ lung tissue. J Hazard Mater 325:31–35. https://doi.org/10.1016/j.jhazmat.2016.11.069
Brusselle GG, Joos GF, Bracke KR (2011) New insights into the immunology of chronic obstructive pulmonary disease. Lancet 378(9795):1015–1026. https://doi.org/10.1016/S0140-6736(11)60988-4
Arnson Y, Shoenfeld Y, Amital H (2010) Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun 34(3):J258–J265. https://doi.org/10.1016/j.jaut.2009.12.003
Mohapatra P, Preet R, Das D, Satapathy SR, Siddharth S, Choudhuri T, Wyatt MD, Kundu CN (2014) The contribution of heavy metals in cigarette smoke condensate to malignant transformation of breast epithelial cells and in vivo initiation of neoplasia through induction of a PI3K-AKT-NFκB cascade. Toxicol Appl Pharmacol 274(1):168–179. https://doi.org/10.1016/j.taap.2013.09.028
Qiu F, Liang CL, Liu H, Zeng YQ, Hou S, Huang S, Lai X, Dai Z (2017) Impacts of cigarette smoking on immune responsiveness: up and down or upside down? Oncotarget 8(1):268–284. https://doi.org/10.18632/oncotarget.13613
Hecht EM, Landy DC, Ahn S, Hlaing WM, Hennekens CH (2013) Hypothesis: cadmium explains, in part, why smoking increases the risk of cardiovascular disease. J Cardiovasc Pharmacol Ther 18(6):550–554. https://doi.org/10.1177/1074248413494815
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The authors thank the National Rehabilitation Institute “Luis Guillermo Ibarra Ibarra” (INRLGII).
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JFT and YZC designed the study and performed literature search, data extraction, analysis, and drafting the manuscript. GAMN supported the writing of the manuscript. OGAA contributed to design and interpretation of data. MPSV supported the literature search and the writing of the manuscript. CALP supported data extraction, analysis, and writing of the manuscript. CSA data verification and contributed analysis. CLS supported the literature search and the writing of the manuscript. AOM wrote the manuscript and supported the literature search. LMDR contributed in the critical review of the manuscript. MCCR supported the literature search. KMF wrote the manuscript, conceived the study, and designed the review. All authors read and critically revised the manuscript and approved the final version.
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Fernández-Torres, J., Zamudio-Cuevas, Y., Martínez-Nava, G.A. et al. Impact of Cadmium Mediated by Tobacco Use in Musculoskeletal Diseases. Biol Trace Elem Res 200, 2008–2015 (2022). https://doi.org/10.1007/s12011-021-02814-y
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DOI: https://doi.org/10.1007/s12011-021-02814-y