Abstract
Lymphoma arises from cells of the immune system and trace metals augment the immune system and their imbalance may promote immunological disorders including tumorigenesis. The primary aim of the present investigation was to evaluate the levels of essential/toxic trace metals in the nails of non-Hodgkin and Hodgkin lymphomas patients in comparison with controls. The samples collected from patients and controls were digested in the mixture of HNO3-HClO4 and selected trace metals were analysed using flame atomic absorption spectrometry. The results showed that mean concentrations of some elements (Pb, Ni, Cd, Cu and Cr) in nails of non-Hodgkin lymphoma patients were significantly elevated (p < 0.05) than that of the controls whereas mean contents of Pb, Cu, Cd and Cr were observed to be significantly higher in the nails of Hodgkin lymphoma patients compared with healthy donors. Additionally, correlation study pointed out significantly diverse mutual associations of the trace metals among the patients and controls. The present results revealed noticeable disparities in the metal concentrations based on gender, food habits, tobacco use and types/stages of the donor’s groups. Overall, the pathogenesis of disease significantly affected the trace metal balance in both patients’ groups.
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Golasik M, Przybyłowicz A, Wozniak A, Herman M, Gawecki W, Golusinski W, Walas S, Krejpcio Z, Szyfter K, Florek E, Piekoszewski W (2015) Essential metals profile of the hair and nails of patients with laryngeal cancer. J Trace Elem Med Biol 31:67–73
Hatton C, Collins G, Sweetenham J (2008) Fast facts: lymphoma. Health Press Limited, Abingdon, Oxford, p 2008
Mader SS, Windelspecht M (2012) Human biology, 12th edn. McGraw-Hill Companies, New York
Ansell SM (2016) Hodgkin lymphoma: 2016 update on diagnosis, risk-stratification, and management. Am J Hematol 91:435–442
Gobbi PG, Ferreri AJM, Ponzoni M, Levis A (2013) Hodgkin lymphoma. Crit Rev Oncol Hematol 85:216–237
Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J (2008) World Health Organization classification of tumours of haematopoietic and lymphoid tissues. IARC Press, Lyon
Sarwar MR, Saqib A (2017) Cancer prevalence, incidence and mortality rates in Pakistan in 2012. Cogent Med 4:1288773
Parodi S, Santi I, Marani E, Casella C, Puppo A, Vercelli M, Stagnaro E (2014) Risk of non-Hodgkin’s lymphoma and residential exposure to air pollution in an industrial area in Northern Italy: a case-control study. Arch Environ Occup Health 69:139–147
Hartge P, Smith MT (2007) Environmental and behavioral factors and the risk of non-Hodgkin lymphoma. Cancer Epidemiol Biomark Prev 16:367–368
Jamakovic M, Baljic R (2013) Significance of copper level in serum and routine laboratory parameters in estimation of outspreading of Hodgkin’s lymphoma. Med Arh 67:185–187
Dai L, Xu W, Li H, Frank JA, He C, Zhang Z, Chen G (2017) Effects of hexavalent chromium on mouse splenic T lymphocytes. Toxicol in Vitro 45:166–171
He K (2011) Trace elements in nails as biomarkers in clinical research. Eur J Clin Investig 41:98–102
Qayyum MA, Shah MH (2017) Study of trace metal imbalances in the blood, scalp hair and nails of oral cancer patients from Pakistan. Sci Total Environ 593:191–201
Johnson N, Shelton BJ, Hopenhayn C, Tucker TT, Unrine JM, Huang B, Jay WC, Zhang Z, Shi X, Li L (2011) Concentrations of arsenic, chromium, and nickel in toenail samples from Appalachian Kentucky residents. J Environ Pathol Toxicol Oncol 30:213–223
Cunzhi H, Jiexian J, Xianwen Z, Jingang G, Suling H (2001) Classification and prognostic value of serum copper/zinc ratio in Hodgkin’s disease. Biol Trace Elem Res 83:133–138
Kelly RS, Lundh T, Porta M, Bergdahl IA, Palli D, Johansson A, Botsivali M, Vineis P, Vermeulen R, Kyrtopoulos SA, Chadeau-Hyam M (2013) Blood erythrocyte concentrations of cadmium and lead and the risk of B-cell non-Hodgkin’s lymphoma and multiple myeloma: a nested case-control study. PLoS One 8:e81892
Cavdar AO, Gozdasoglu S, Babacan E, Mengubas K, Unal E, Yavus G, Tacyildiz N (2009) Zinc and selenium status in pediatric malignant lymphomas. Nutr Cancer 61:888–890
Ahmad B, Ghani H, Azam S, Bashir S, Begum N (2011) The status of trace elements in lymphoma and esophageal cancer patients: a case study. Afr J Biotechnol 10:19645–19649
Ilyas A, Ahmad H, Shah MH (2015) Comparative study of elemental concentrations in the scalp hair and nails of myocardial infarction patients versus controls from Pakistan. Biol Trace Elem Res 166:123–135
StatSoft (1999) STATISTICA for windows. Computer program manual, StatSoft, Tulsa, OK
Valko M, Jomova K, Rhodes CJ, Kuca K, Musílek K (2016) Redox and non-redox metal induced formation of free radicals and their role in human disease. Arch Toxicol 90:1–37
Klaunig JE, Wang Z, Pu X, Zhou S (2011) Oxidative stress and oxidative damage in chemical carcinogenesis. Toxicol Appl Pharm 254:86–99
El-Mezayen HA, Darwish H, Hasheim M, El-Baz HA, Mohamed MA (2015) Oxidant/antioxidant status and their relations to chemotherapy in non-Hodgkin’s lymphoma. Int J Pharm Clin Res 7:269–274
Bur H, Haapasaari K, Turpeenniemi-Hujanen T, Kuittinen O, Auvinen P, Marin K, Koivunen P, Sormunen R, Soini Y, Karihtala P (2014) Oxidative stress markers and mitochondrial antioxidant enzyme expression are increased in aggressive Hodgkin lymphomas. Histopathol 65:319–327
IARC (2012) Cadmium and cadmium compounds. IARC monographs on the evaluation of carcinogenic risks to humans. Volume 100C, International Agency for Research on Cancer, Lyon, France
Hartwig A (2013) Cadmium and cancer. Metal Ions Life Sci 11:491–507
Luevano J, Damodaran C (2014) A review of molecular events of cadmium-induced carcinogenesis. J Environ Pathol Toxicol Oncol 33:183–194
Joseph P (2009) Mechanisms of cadmium carcinogenesis. Toxicol Appl Pharmacol 238:272–279
Giaginis C, Gatzidou E, Theocharis S (2006) DNA repair systems as targets of cadmium toxicity. Toxicol Appl Pharm 213:282–290
Lafuente A, Carracedo AG, Esquifino AI (2004) Differential effects of cadmium on blood lymphocyte subsets. Biometals 17:451–456
Cui ZG, Ogawa R, Piao JL, Hamazaki K, Feril LB, Shimomura A, Kondo T, Inadera H (2011) Molecular mechanisms involved in the adaptive response to cadmium-induced apoptosis in human myelomonocytic lymphoma U937 cells. Toxicol in Vitro 25:1687–1693
Adams SV, Passarelli MN, Newcomb PA (2012) Cadmium exposure and cancer mortality in the third national health and nutrition examination survey cohort. Occup Environ Med 69:153–156
Czerny B, Krupka K, Ozarowski M, Mrozikiewicz AS (2014) Screening of trace elements in hair of the female population with different types of cancers in Wielkopolska region of Poland. Sci World J 2014:953181
Waalkes MP (2003) Cadmium carcinogenesis. Mutat Res 533:107–120
Khan FH, Ambreen K, Fatima G, Kumar S (2012) Assessment of health risks with reference to oxidative stress and DNA damage in chromium exposed population. Sci Total Environ 430:68–74
Bielcka A, Bojanowska L, Wisniewski A (2005) Two faces of chromium- pollutant and bioelement. Pol J Environ Stud 14:5–10
Ray RR (2016) Adverse hematological effects of hexavalent chromium: an overview. Interdiscip Toxicol 9:55–65
Briggs NC, Hall HI, Brann EA, Moriarty CJ, Levine RS (2002) Cigarette smoking and risk of Hodgkin’s disease: a population-based case-control study. Am J Epidemiol 156:1011–1020
Memoli VA, Urban RM, Alroy J, Galante JO (1986) Malignant neoplasms associated with orthopedic implant materials in rats. J Orthop Res 4:346–355
Kazmierski KJ, Ogilvie GK, Fettman MJ, Lana SE, Walton JA, Hansen RA, Richardson KL, Hamar DW, Bedwell CL, Andrews G, Chavey S (2001) Serum zinc, chromium, and iron concentrations in dogs with lymphoma and osteosarcoma. J Vet Intern Med 15:585–588
Zhitkovich A (2011) Chromium in drinking water: sources, metabolism, and cancer risks. Chem Res Toxicol 24:1617–1629
Canaz E, Kilinc M, Sayar H, Kiran G, Ozyurek E (2017) Lead, selenium and nickel concentrations in epithelial ovarian cancer, borderline ovarian tumor and healthy ovarian tissues. J Trace Elem Med Biol 43:217–223
Beyersmann D, Hartwig A (2008) Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch Toxicol 82:493–512
IARC (2006) Inorganic and organic lead compounds. IARC Monograph on the Evaluation of Carcinogenic Risks to Humans, vol 87. International Agency for Research on Cancer, Lyon
Mishra KP (2009) Lead exposure and its impact on immune system: a review. Toxicol in Vitro 23:969–972
Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicol 283:65–87
Lam TV, Agovino P, Niu X, Roche L (2007) Linkage study of cancer risk among lead-exposed workers in New Jersey. Sci Total Environ 372:455–462
Franklin RB, Costello LC (2007) Zinc as an anti-tumor agent in prostate cancer and in other cancers. Arch Biochem Biophys 463:211–217
Ibs KH, Rink L (2003) Zinc-altered immune function. J Nutr 133:1452S–1456S
Prasad AS (2009) Impact of the discovery of human zinc deficiency on health. J Am Coll Nutr 28:257–265
Amaral AF, Cymbron T, Gärtner F, Lima M, Rodrigues AS (2009) Trace metals and over-expression of metallothioneins in bladder tumoral lesions: a case-control study. BMC Vet Res 5:24
Ooi TC, Mohammad NH, Sharif R (2014) Zinc carnosine protects against hydrogen peroxide-induced DNA damage in WIL2-NS lymphoblastoid cell line independent of poly (ADP-ribose) polymerase expression. Biol Trace Elem Res 162:8–17
Ho E (2004) Zinc deficiency, DNA damage and cancer risk. J Nutr Biochem 15:572–578
King LE, Fraker PJ (2002) Zinc deficiency in mice alters myelopoiesis and hematopoiesis. J Nutr 132:3301–3307
Saleh SAK, Adly HM, Nassir AM (2017) Altered trace elements levels in hair of prostate cancer patients. J Cancer Sci Ther 9:336–339
Tapiero H, Townsend DM, Tew KD (2003) Trace elements in human physiology and pathology. Copper. Biomed Pharmacother 57:386–398
Bo S, Durazzo M, Gambino R, Berutti C, Milanesio N, Caropreso A, Gentile L, Cassader M, Cavallo-Perin P, Pagano G (2008) Associations of dietary and serum copper with inflammation, oxidative stress, and metabolic variables in adults. J Nutr 138:305–310
Turnlund JR, Jacob RA, Keen CL, Strain JJ, Kelley DS, Domek JM, Keyes WR, Ensunsa JL, Lykkesfeldt J, Coulter J (2004) Long-term high copper intake: effects on indexes of copper status, antioxidant status, and immune function in young men. Am J Clin Nutr 79:1037–1044
Linder MC, Hazegh-Azam M (1996) Copper biochemistry and molecular biology. Am J Clin Nutr 63:797S–811S
Lightfoot N, Berriault C (2012) Mortality and cancer incidence in a copper-zinc cohort. Workplace Health Safe 60:223–233
Cohen Y, Epelbaum R, Haim N, McShan D, Zinder O (1984) The value of serum copper levels in non-Hodgkin’s lymphoma. Cancer 53:296–300
Haiying W, Luyi W (1989) Clinical study on serum copper, zinc levels and copper/zinc ratio in malignant lymphoma. Chinese J Cancer Res 1:50–53
Rezazadeh H, Nayebi AR, Athar M (2001) Role of iron–dextran on 7,12-dimethylbenz(a) anthracene-initiated and croton oil-promoted cutaneous tumorigenesis in normal and pregnant mice. Hum Exp Toxicol 20:471–476
Naoum FA (2016) Iron deficiency in cancer patients. Rev Bras Hematol Hemoter 38:325–330
Das I, Saha K, Mukhopadhyay D, Roy S, Raychaudhuri G, Chatterjee M (2014) Impact of iron deficiency anemia on cell-mediated and humoral immunity in children: a case control study. J Nat Sci Biol Med 5:158–163
Ekiz C, Agaoglu L, Karakas Z, Gurel N, Yalcin I (2005) The effect of iron deficiency anemia on the function of the immune system. Hematol J 5:579–583
Crossgrove J, Zheng W (2004) Manganese toxicity upon over exposure. NMR Biomed 17:544–553
Reddi AR, Jensen LT, Naranuntarat A, Rosenfeld L, Leung E, Shah R, Culotta VC (2009) The overlapping roles of manganese and Cu/Zn SOD in oxidative stress protection. Free Rad Biol Med 46:154–162
Milde D, Novac O, Stuzka V, Vyslouzil K, Machacek J (2001) Serum levels of selenium, manganese, copper, and iron in colorectal cancer patients. Biol Trace Elem Res 79:107–114
Chtourou Y, Trabelsi K, Fetoui H, Mkannez G, Kallel H, Zeghal N (2011) Manganese induces oxidative stress, redox state unbalance and disrupts membrane bound ATPases on murine neuroblastoma cells in vitro: protective role of silymarin. Neurochem Res 36:1546–1557
Spangler JG, Reid JC (2010) Environmental manganese and cancer mortality rates by county in North Carolina: an ecological study. Biol Trace Elem Res 133:128–135
Yin Z, Jiang H, Lee ESY, Ni M, Erikson KM, Milatovic D, Bowman AB, Aschner M (2010) Ferroportin is a manganese-responsive protein that decreases manganese cytotoxicity and accumulation. Neurochem 112:1190–1198
Magaye R, Zhao J (2012) Recent progress in studies of metallic nickel and nickel-based nanoparticles’ genotoxicity and carcinogenicity. Environ Toxicol Pharm 34:644–650
Zambelli B, Uversky VN, Ciurli S (2016) Nickel impact on human health: an intrinsic disorder perspective. Biochim Biophys Acta 1864:1714–1731
Cameron KS, Buchner V, Tchounwou PB (2011) Exploring the molecular mechanisms of nickel-induced genotoxicity and carcinogenicity: a literature review. Rev Environ Health 26:81–92
Kamil ZH, Ewadh MJ, Alta’ee AH (2016) Determination of serum trace elements and haematological parameters in lymphoma patients receiving chemotherapy. J Babylon Univ 24:2489–2500
Acknowledgements
The authors would like to acknowledge the patients as well as the administrations/staff of Nuclear Oncology and Radiotherapy Institute (NORI), Islamabad, for their invaluable help during the sample collection.
Funding
This study was financially supported by the Higher Education Commission, Government of Pakistan. Financial and technical help was also provided by Quaid-i-Azam University, Islamabad, Pakistan.
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (Ethical Review Committee, NORI, Islamabad REF. NO. QAUC-2009-A98) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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Qayyum, M.A., Shah, M.H. Disparities in Trace Metal Levels in Hodgkin/Non-Hodgkin Lymphoma Patients in Comparison with Controls. Biol Trace Elem Res 194, 34–47 (2020). https://doi.org/10.1007/s12011-019-01746-y
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DOI: https://doi.org/10.1007/s12011-019-01746-y