Toenail and serum levels as biomarkers of iron status in pre- and postmenopausal women: correlations and stability over eight-year follow-up.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
19 Jan 2024
19 Jan 2024
Historique:
received:
24
02
2023
accepted:
20
12
2023
medline:
20
1
2024
pubmed:
20
1
2024
entrez:
19
1
2024
Statut:
epublish
Résumé
Iron status is often assessed in epidemiologic studies, and toenails offer a convenient alternative to serum because of ease of collection, transport, and storage, and the potential to reflect a longer exposure window. Very few studies have examined the correlation between serum and toenail levels for trace metals. Our aim was to compare iron measures using serum and toenails on both a cross-sectional and longitudinal basis. Using a subset of the US-wide prospective Sister Study cohort, we compared toenail iron measures to serum concentrations for iron, ferritin and percent transferrin saturation. Among 146 women who donated both blood and toenails at baseline, a subsample (59%, n = 86) provided specimens about 8 years later. Cross-sectional analyses included nonparametric Spearman's rank correlations between toenail and serum biomarker levels. We assessed within-woman maintenance of rank across time for the toenail and serum measures and fit mixed effects models to measure change across time in relation to change in menopause status. Spearman correlations at baseline (follow-up) were 0.08 (0.09) for serum iron, 0.08 (0.07) for transferrin saturation, and - 0.09 (- 0.17) for ferritin. The within-woman Spearman correlation for toenail iron between the two time points was higher (0.47, 95% CI 0.30, 0.64) than for serum iron (0.30, 95% CI 0.09, 0.51) and transferrin saturation (0.34, 95% CI 0.15, 0.54), but lower than that for ferritin (0.58, 95% CI 0.43, 0.73). Serum ferritin increased over time while nail iron decreased over time for women who experienced menopause during the 8-years interval. Based on cross-sectional and repeated assessments, our evidence does not support an association between serum biomarkers and toenail iron levels. Toenail iron concentrations did appear to be moderately stable over time but cannot be taken as a proxy for serum iron biomarkers and they may reflect physiologically distinct fates for iron.
Identifiants
pubmed: 38242893
doi: 10.1038/s41598-023-50506-5
pii: 10.1038/s41598-023-50506-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1682Subventions
Organisme : NIEHS NIH HHS
ID : Z01-ES044005
Pays : United States
Informations de copyright
© 2024. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.
Références
Garcia-Casal, M. N., Pasricha, S.-R., Martinez, R. X., Lopez-Perez, L. & Peña-Rosas, J. P. Serum or plasma ferritin concentration as an index of iron deficiency and overload. Cochr. Database Syst. Rev. 5, CD011817 (2021).
Brissot, P. Iron overload: Diagnosis, complications, and management. In Nonmalignant Hematology: Expert Clinical Review: Questions and Answers (eds Abutalib, S. A. et al.) 103–112 (Springer, 2016). https://doi.org/10.1007/978-3-319-30352-9_11 .
doi: 10.1007/978-3-319-30352-9_11
Pfeifhofer-Obermair, C., Tymoszuk, P., Petzer, V., Weiss, G. & Nairz, M. Iron in the tumor microenvironment—Connecting the dots. Front. Oncol. 8, 549 (2018).
pubmed: 30534534
pmcid: 6275298
doi: 10.3389/fonc.2018.00549
Quintana Pacheco, D. A. et al. Iron status in relation to cancer risk and mortality: Findings from a population-based prospective study. Int. J. Cancer 143, 561–569 (2018).
pubmed: 29574909
doi: 10.1002/ijc.31384
Khan, A., Singh, P. & Srivastava, A. Iron: Key player in cancer and cell cycle?. J. Trace Elem. Med. Biol. 62, 126582 (2020).
pubmed: 32673942
doi: 10.1016/j.jtemb.2020.126582
Torti, S. V. & Torti, F. M. Iron: The cancer connection. Mol. Aspects Med. 75, 100860 (2020).
pubmed: 32340745
pmcid: 9107937
doi: 10.1016/j.mam.2020.100860
Deugnier, Y. & Turlin, B. Pathology of hepatic iron overload. Semin. Liver Dis. 31, 260–271 (2011).
pubmed: 21901656
doi: 10.1055/s-0031-1286057
McClain, D. A. et al. High prevalence of abnormal glucose homeostasis secondary to decreased insulin secretion in individuals with hereditary haemochromatosis. Diabetologia 49, 1661–1669 (2006).
pubmed: 16538487
doi: 10.1007/s00125-006-0200-0
Huang, J. et al. Increased glucose disposal and AMP-dependent kinase signaling in a mouse model of hemochromatosis. J. Biol. Chem. 282, 37501–37507 (2007).
pubmed: 17971451
doi: 10.1074/jbc.M703625200
Gulati, V. et al. Cardiac involvement in hemochromatosis. Cardiol. Rev. 22, 56–68 (2014).
pubmed: 24503941
doi: 10.1097/CRD.0b013e3182a67805
Pfeiffer, C. M. & Looker, A. C. Laboratory methodologies for indicators of iron status: Strengths, limitations, and analytical challenges. Am. J. Clin. Nutr. 106, 1606S-1614S (2017).
pubmed: 29070545
pmcid: 5701713
doi: 10.3945/ajcn.117.155887
Arosio, P., Ingrassia, R. & Cavadini, P. Ferritins: A family of molecules for iron storage, antioxidation and more. Biochim. Biophys. Acta BBA Gen. Subj. 1790, 589–599 (2009).
doi: 10.1016/j.bbagen.2008.09.004
Lipschitz, D. A., Cook, J. D. & Finch, C. A. A clinical evaluation of serum ferritin as an index of iron stores. N. Engl. J. Med. 290, 1213–1216 (1974).
pubmed: 4825851
doi: 10.1056/NEJM197405302902201
Katsarou, A. & Pantopoulos, K. Basics and principles of cellular and systemic iron homeostasis. Mol. Aspects Med. 75, 100866 (2020).
pubmed: 32564977
doi: 10.1016/j.mam.2020.100866
Anderson, G. J. & Frazer, D. M. Current understanding of iron homeostasis. Am. J. Clin. Nutr. 106, 1559S-1566S (2017).
pubmed: 29070551
pmcid: 5701707
doi: 10.3945/ajcn.117.155804
Wallace, D. F. The regulation of iron absorption and homeostasis. Clin. Biochem. Rev. 37, 51–62 (2016).
pubmed: 28303071
pmcid: 5198508
Ahluwalia, N., Lammi-Keefe, C. J., Haley, N. R. & Beard, J. L. Day-to-day variation in iron-status indexes in elderly women. Am. J. Clin. Nutr. 57, 414–419 (1993).
pubmed: 8438777
doi: 10.1093/ajcn/57.3.414
Lacher, D. A., Hughes, J. P. & Carroll, M. D. Biological variation of laboratory analytes based on the 1999–2002 National Health and Nutrition Examination Survey. Natl. Health Stat. Rep. 1–7 (2010).
Ricós, C., Alvarez, V. & Cava, F. Current databases on biological variation: pros, cons and progress. Scand. J. Clin. Lab. Invest. 59, 491–500 (1999).
pubmed: 10667686
doi: 10.1080/00365519950185229
Cooper, M. J. & Zlotkin, S. H. Day-to-day variation of transferrin receptor and ferritin in healthy men and women. Am. J. Clin. Nutr. 64, 738–742 (1996).
pubmed: 8901794
doi: 10.1093/ajcn/64.5.738
Bowen, R. A. R. & Remaley, A. T. Interferences from blood collection tube components on clinical chemistry assays. Biochem. Med. 24, 31–44 (2014).
doi: 10.11613/BM.2014.006
Moyer, T. P., Mussmann, G. V. & Nixon, D. E. Blood-collection device for trace and ultra-trace metal specimens evaluated. Clin. Chem. 37, 709–714 (1991).
pubmed: 2032325
doi: 10.1093/clinchem/37.5.709
McCaughey, E. J. et al. Key factors influencing the incidence of hemolysis: A critical appraisal of current evidence. Crit. Rev. Clin. Lab. Sci. 54, 59–72 (2017).
pubmed: 28013559
doi: 10.1080/10408363.2016.1250247
Carraro, P., Servidio, G. & Plebani, M. Hemolyzed specimens: A reason for rejection or a clinical challenge?. Clin. Chem. 46, 306–307 (2000).
pubmed: 10657399
doi: 10.1093/clinchem/46.2.306
He, K. Trace elements in nails as biomarkers in clinical research. Eur. J. Clin. Invest. 41, 98–102 (2011).
pubmed: 20813017
doi: 10.1111/j.1365-2362.2010.02373.x
Gutiérrez-González, E. et al. Toenails as biomarker of exposure to essential trace metals: A review. Environ. Res. 179, 108787 (2019).
pubmed: 31610392
pmcid: 8164381
doi: 10.1016/j.envres.2019.108787
Karagas, M. R. et al. Measurement of low levels of arsenic exposure: A comparison of water and toenail concentrations. Am. J. Epidemiol. 152, 84–90 (2000).
pubmed: 10901333
doi: 10.1093/aje/152.1.84
Jaramillo Ortiz, S. et al. Biomarkers of disease in human nails: A comprehensive review. Crit Rev. Clin. Lab. Sci. 59, 125–141 (2022).
pubmed: 34726550
doi: 10.1080/10408363.2021.1991882
Solimini, R. et al. Nails in forensic toxicology: An update. Curr. Pharm. Des. 23, 5468–5479 (2017).
pubmed: 28677498
Longnecker, M. P. et al. Selenium in diet, blood, and toenails in relation to human health in a seleniferous area. Am. J. Clin. Nutr. 53, 1288–1294 (1991).
pubmed: 2021136
doi: 10.1093/ajcn/53.5.1288
Kilinc, E., Buturak, B. & Alkan, F. A. Level of trace elements in serum and toenail samples of patients with onychocryptosis (ingrown toenail) and onychomycosis. J. Trace Elem. Med. Biol. 61, 126509 (2020).
pubmed: 32302924
doi: 10.1016/j.jtemb.2020.126509
Woźniak, A. et al. Physiological metals in the serum, hair and nails of patients with head and neck cancer. Przegląd Lek 69, 785 (2012).
Garland, M. et al. Toenail trace element levels and breast cancer: A prospective study. Am. J. Epidemiol. 144, 653–660 (1996).
pubmed: 8823061
doi: 10.1093/oxfordjournals.aje.a008977
Sandler, D. P. et al. The sister study cohort: Baseline methods and participant characteristics. Environ. Health Perspect. 125, 127003 (2017).
pubmed: 29373861
pmcid: 5963586
doi: 10.1289/EHP1923
Von Holle, A., O’Brien, K. M., Sandler, D. P., Janicek, R. & Weinberg, C. R. Association between serum iron biomarkers and breast cancer. Cancer Epidemiol. Prev. Biomark. 30, 422–425 (2021).
doi: 10.1158/1055-9965.EPI-20-0715
O’Brien, K. M. et al. Do post-breast cancer diagnosis toenail trace element concentrations reflect prediagnostic concentrations?. Epidemiology 30, 112–119 (2019).
pubmed: 30256233
pmcid: 6275107
doi: 10.1097/EDE.0000000000000927
O’Brien, K. M. et al. Toenail-based metal concentrations and young-onset breast cancer. Am. J. Epidemiol. 188, 646–655 (2019).
pubmed: 30608527
pmcid: 6454842
doi: 10.1093/aje/kwy283
Milman, N. Serum ferritin in Danes: Studies of iron status from infancy to old age, during blood donation and pregnancy. Int. J. Hematol. 63, 103–135 (1996).
pubmed: 8867722
doi: 10.1016/0925-5710(95)00426-2
Niehoff, N. M. et al. Metals and breast cancer risk: A prospective study using toenail biomarkers. Am. J. Epidemiol. 190, 2360–2373 (2021).
pubmed: 34268559
pmcid: 8799900
doi: 10.1093/aje/kwab204
Cole, T. J. Sympercents: Symmetric percentage differences on the 100 loge scale simplify the presentation of log transformed data. Stat. Med. 19, 3109–3125 (2000).
pubmed: 11113946
doi: 10.1002/1097-0258(20001130)19:22<3109::AID-SIM558>3.0.CO;2-F
Cole, T. J. & Altman, D. G. Statistics notes: Percentage differences, symmetry, and natural logarithms. BMJ https://doi.org/10.1136/bmj.j3683 (2017).
doi: 10.1136/bmj.j3683
pubmed: 28814563
Milman, N., Kirchhoff, M. & Jorgensen, T. Iron status markers, serum ferritin and hemoglobin in 1359 danish women in relation to menstruation, hormonal contraception, parity, and postmenopausal hormone-treatment. Ann. Hematol. 65, 96–102 (1992).
pubmed: 1511065
doi: 10.1007/BF01698138
Warne, C. D. et al. HFE pC282Y homozygosity predisposes to rapid serum ferritin rise after menopause: A genotype-stratified cohort study of hemochromatosis in Australian women: HFE genotype, SF levels and menopause. J. Gastroenterol. Hepatol. 32, 797–802 (2017).
pubmed: 27784128
pmcid: 5365371
doi: 10.1111/jgh.13621
Milman, N., Byg, K.-E., Ovesen, L., Kirchhoff, M. & Jürgensen, K.S.-L. Iron status in Danish women, 1984–1994: a cohort comparison of changes in iron stores and the prevalence of iron deficiency and iron overload. Eur. J. Haematol. 71, 51–61 (2003).
pubmed: 12801299
doi: 10.1034/j.1600-0609.2003.00090.x
Barnett, A. G. & Dobson, A. J. Cosinor. in Analysing Seasonal Health Data (eds. Barnett, A. G. & Dobson, A. J.) 75–92 (Springer, 2010). https://doi.org/10.1007/978-3-642-10748-1_3 .
R Core Team. R: A language and environment for statistical computing. https://www.R-project.org/ (2020).
Pfeiffer, C. M. et al. National Report on Biochemical Indicators of Diet and Nutrition in the U.S. Population 1999‐2002. FASEB J. 23, (2009).
U.S. Centers for Disease Control and Prevention. Second National Report on Biochemical Indicators of Diet and Nutrition in the U.S. Population 2012. 495 https://www.cdc.gov/nutritionreport/report_2012.html (2012).
Al-Saleh, I. & Billedo, G. Determination of selenium concentration in serum and toenail as an indicator of selenium status. Bull. Environ. Contam. Toxicol. 77, 155–163 (2006).
pubmed: 16977515
doi: 10.1007/s00128-006-1045-4
McKenzie, J. M. Content of zinc in serum, urine, hair, and toenails of New Zealand adults. Am. J. Clin. Nutr. 32, 570–579 (1979).
pubmed: 420149
doi: 10.1093/ajcn/32.3.570
Djaldetti, M., Fishman, P. & Hart, J. The iron content of finger-nails in iron deficient patients. Clin. Sci. 72, 669–672 (1987).
doi: 10.1042/cs0720669
Yaemsiri, S., Hou, N., Slining, M. M. & He, K. Growth rate of human fingernails and toenails in healthy American young adults. J. Eur. Acad. Dermatol. Venereol. 24, 420–423 (2010).
pubmed: 19744178
doi: 10.1111/j.1468-3083.2009.03426.x
Baumgartner, M. R. Nails: An adequate alternative matrix in forensic toxicology for drug analysis?. Bioanalysis 6, 2189–2191 (2014).
pubmed: 25383731
doi: 10.4155/bio.14.165
Garside, D. Drugs-of-abuse in nails. In Drug Testing in Alternate Biological Specimens (eds Jenkins, A. J. & Caplan, Y. H.) 43–65 (Humana Press, 2008). https://doi.org/10.1007/978-1-59745-318-9_3 .
doi: 10.1007/978-1-59745-318-9_3
Hirobe, T. Iron and skin health: Iron stimulates skin function. In Handbook of Diet, Nutrition and the Skin (ed. Preedy, V. R.) 196–214 (Academic Publishers, 2012).
doi: 10.3920/9789086867295_013
Kell, D. B. & Pretorius, E. Serum ferritin is an important inflammatory disease marker, as it is mainly a leakage product from damaged cells. Metallomics 6, 748–773 (2014).
pubmed: 24549403
doi: 10.1039/C3MT00347G
Orentreich, N., Markofsky, J. & Vogelman, J. H. The effect of aging on the rate of linear nail growth. J. Invest. Dermatol. 73, 126–130 (1979).
pubmed: 448171
doi: 10.1111/1523-1747.ep12532799
Chessa, M. A. et al. Pathogenesis, clinical signs and treatment recommendations in brittle nails: A review. Dermatol. Ther. 10, 15–27 (2020).
doi: 10.1007/s13555-019-00338-x
Le, C. H. H. The prevalence of anemia and moderate-severe anemia in the US population (NHANES 2003–2012). PLOS ONE 11, e0166635 (2016).
pubmed: 27846276
pmcid: 5112924
doi: 10.1371/journal.pone.0166635
Wright, R. O. Environment, susceptibility windows, development, and child health. Curr. Opin. Pediatr. 29, 211–217 (2017).
pubmed: 28107208
pmcid: 5473288
doi: 10.1097/MOP.0000000000000465