Skip to main content

Advertisement

SpringerLink
Log in

Association between blood manganese and bone mineral density in US adolescents

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Manganese (Mn) exposure may reduce bone mineral density (BMD); however, studies investigating its effects on BMD are limited, especially among adolescents. Therefore, the present study is aimed at investigating the association between blood Mn levels and BMD in adolescents. This cross-sectional study included participants aged 12–19 years with National Health and Nutrition Examination Survey data collected between 2011 and 2018. Total, trunk bone, lumbar spine, and pelvic BMDs were used as outcome variables. Multivariate linear regression models were used to investigate the association between blood Mn levels and BMD. The relationship between blood Mn level and BMD was assessed using smooth curve fitting. In total, 1,703 participants (mean age 15.62 ± 2.31 years) were considered. Multivariable linear regression models demonstrated that BMD decreased as blood Mn level increased, especially among girls aged 12–15 years. This relationship was also observable in non-Hispanic whites and other races according to subgroup analyses stratified by race. Smooth curve fitting indicated the existence of a non-linear relationship between blood Mn and BMD after confounding variable adjustment. The present study indicated that blood Mn levels were negatively associated with BMD in adolescents, especially in girls aged 12–15 years. Therefore, clinicians should be aware of the potential risk of low bone mass among adolescents with high blood Mn levels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

All data were extracted from National Health and Nutrition Examination Survey (NHANES) 2017–2018 database. The detailed information was provided on the NHANES website.

Code availability

All analyses were performed with R software, V.4.1.3 (R: a language and statistical computing environment (program), Vienna, Austria: R Foundation for Statistical Computing, 2016), and EmpowerStats (http://www.empowerstats. com).

References

  • Baxter-Jones AD, Faulkner RA, Forwood MR, Mirwald RL, Bailey DA (2011) Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res 26:1729–1739

    Article  Google Scholar 

  • Bocca B, Madeddu R, Asara Y, Tolu P, Marchal JA, Forte G (2011) Assessment of reference ranges for blood Cu, Mn, Se and Zn in a selected Italian population. J Trace Elem Med Biol 25:19–26

    Article  CAS  Google Scholar 

  • Bouchard MF, Surette C, Cormier P, Foucher D (2018) Low level exposure to manganese from drinking water and cognition in school-age children. Neurotoxicology 64:110–117

    Article  CAS  Google Scholar 

  • Callaway DA, Jiang JX (2015) Reactive oxygen species and oxidative stress in osteoclastogenesis, skeletal aging and bone diseases. J Bone Miner Metab 33:359–370

    Article  CAS  Google Scholar 

  • CDC (2011) National Health and Nutrition Examination Survey, NHANES 2011–2012. https://wwwn.cdc.gov/nchs/nhanes/continuousnhanes/default.aspx?BeginYear=2011. Accessed 10 June 2022

  • CDC (2013) National Health and Nutrition Examination Survey, NHANES 2013–2014. https://wwwn.cdc.gov/nchs/nhanes/continuousnhanes/default.aspx?BeginYear=2013. Accessed 10 June 2022

  • CDC (2015) National Health and Nutrition Examination Survey, NHANES 2015–2016. https://wwwn.cdc.gov/nchs/nhanes/continuousnhanes/default.aspx?BeginYear=2015. Accessed 10 June 2022

  • CDC (2017) National Health and Nutrition Examination Survey, NHANES 2017–2018. https://wwwn.cdc.gov/nchs/nhanes/continuousnhanes/default.aspx?BeginYear=2017. Accessed 10 June 2022

  • CDC (2022a) NHANES 2017–2018 brochures and consent documents.https://wwwn.cdc.gov/nchs/nhanes/continuousnhanes/documents.aspx?BeginYear=2017. Accessed 10 June 2022a

  • CDC (2022b) NHANES body composition procedures manual. https://wwwn.cdc.gov/nchs/data/nhanes/2011-2012/manuals/Body_Composition_Procedures_Manual.pdf. Accessed 10 June 2022b

  • CDC (2022c) NHANES laboratory procedure manual.https://wwwn.cdc.gov/nchs/data/nhanes/2011-2012/labmethods/uhm_g_met_heavy_metals.pdf. Accessed 10 June 2022c

  • Conley TE, Richardson C, Pacheco J, Dave N, Jursa T, Guazzetti S, Lucchini RG, Fendorf S, Ritchie RO, Smith DR (2022) Bone manganese is a sensitive biomarker of ongoing elevated manganese exposure, but does not accumulate across the lifespan. Environ Res 204:112355

    Article  CAS  Google Scholar 

  • Cui A, Xiao P, Hu B, Ma Y, Fan Z, Wang H, Zhou F, Zhuang Y (2022) Blood lead level is negatively associated with bone mineral density in U.S. children and adolescents aged 8–19 years. Front Endocrinol (Lausanne) 13:928752

    Article  Google Scholar 

  • Davis CD, Greger JL (1992) Longitudinal changes of manganese-dependent superoxide dismutase and other indexes of manganese and iron status in women. Am J Clin Nutr 55:747–752

    Article  CAS  Google Scholar 

  • Erikson KM, Thompson K, Aschner J, Aschner M (2007) Manganese neurotoxicity: a focus on the neonate. Pharmacol Ther 113:369–377

    Article  CAS  Google Scholar 

  • Glass NA, Torner JC, Letuchy EM, Burns TL, Janz KF, Eichenberger Gilmore JM, Schlechte JA, Levy SM (2016) The relationship between greater prepubertal adiposity, subsequent age of maturation, and bone strength during adolescence. J Bone Miner Res 31:1455–1465

    Article  Google Scholar 

  • Guo T, Zhang L, Konermann A, Zhou H, Jin F, Liu W (2015) Manganese superoxide dismutase is required to maintain osteoclast differentiation and function under static force. Sci Rep 5:8016

    Article  CAS  Google Scholar 

  • Hatano S, Nishi Y, Usui T (1983) Erythrocyte manganese concentration in healthy Japanese children, adults, and the elderly, and in cord blood. Am J Clin Nutr 37:457–460

    Article  CAS  Google Scholar 

  • Himes JH, Dietz WH (1994) Guidelines for overweight in adolescent preventive services: recommendations from an expert committee The Expert Committee on Clinical Guidelines for Overweight in Adolescent Preventive Services. Am J Clin Nutr 59:307–316

    Article  CAS  Google Scholar 

  • Kirmani S, Christen D, van Lenthe GH, Fischer PR, Bouxsein ML, McCready LK, Melton LJ 3rd, Riggs BL, Amin S, Müller R, Khosla S (2009) Bone structure at the distal radius during adolescent growth. J Bone Miner Res 24:1033–1042

    Article  Google Scholar 

  • Lane NE (2006) Epidemiology, etiology, and diagnosis of osteoporosis. Am J Obstet Gynecol 194:S3-11

    Article  CAS  Google Scholar 

  • Lee JW, Lee CK, Moon CS, Choi IJ, Lee KJ, Yi SM, Jang BK, Yoon BJ, Kim DS, Peak D, Sul D, Oh E, Im H, Kang HS, Kim J, Lee JT, Kim K, Park KL, Ahn R, Park SH, Kim SC, Park CH, Lee JH (2012) Korea National Survey For Environmental Pollutants in the Human Body 2008: heavy metals in the blood or urine of the Korean population. Int J Hyg Environ Health 215:449–457

    Article  CAS  Google Scholar 

  • Li D, Ge X, Liu Z, Huang L, Zhou Y, Liu P, Qin L, Lin S, Liu C, Hou Q, Li L, Cheng H, Ou S, Wei F, Shen Y, Zou Y, Yang X (2020) Association between long-term occupational manganese exposure and bone quality among retired workers. Environ Sci Pollut Res Int 27:482–489

    Article  CAS  Google Scholar 

  • Li L, Yang X (2018) The essential element manganese, oxidative stress, and metabolic diseases: links and interactions. Oxid Med Cell Longev 2018:7580707

    Article  Google Scholar 

  • Li T, Xie Y, Wang L, Huang G, Cheng Y, Hou D, Liu W, Zhang T, Liu J (2022) The association between lead exposure and bone mineral density in childhood and adolescence: results from NHANES 1999–2006 and 2011–2018. Nutrients 14(7)

  • Ljung K, Vahter M (2007) Time to re-evaluate the guideline value for manganese in drinking water? Environ Health Perspect 115:1533–1538

    Article  CAS  Google Scholar 

  • Lu L, Zhang LL, Li GJ, Guo W, Liang W, Zheng W (2005) Alteration of serum concentrations of manganese, iron, ferritin, and transferrin receptor following exposure to welding fumes among career welders. Neurotoxicology 26:257–265

    Article  CAS  Google Scholar 

  • Lucchini RG, Guazzetti S, Zoni S, Donna F, Peter S, Zacco A, Salmistraro M, Bontempi E, Zimmerman NJ, Smith DR (2012) Tremor, olfactory and motor changes in Italian adolescents exposed to historical ferro-manganese emission. Neurotoxicology 33:687–696

    Article  CAS  Google Scholar 

  • Menezes-Filho JA, Bouchard M, Sarcinelli Pde N, Moreira JC (2009) Manganese exposure and the neuropsychological effect on children and adolescents: a review. Rev Panam Salud Publica 26:541–548

    Article  Google Scholar 

  • O’Neal SL, Hong L, Fu S, Jiang W, Jones A, Nie LH, Zheng W (2014) Manganese accumulation in bone following chronic exposure in rats: steady-state concentration and half-life in bone. Toxicol Lett 229:93–100

    Article  CAS  Google Scholar 

  • Oulhote Y, Mergler D, Bouchard MF (2014) Sex- and age-differences in blood manganese levels in the U.S. general population: national health and nutrition examination survey 2011–2012. Environ Health 13:87

    Article  Google Scholar 

  • Pinsino A, Roccheri MC, Costa C, Matranga V (2011) Manganese interferes with calcium, perturbs ERK signaling, and produces embryos with no skeleton. Toxicol Sci 123:217–230

    Article  CAS  Google Scholar 

  • Rükgauer M, Klein J, Kruse-Jarres JD (1997) Reference values for the trace elements copper, manganese, selenium, and zinc in the serum/plasma of children, adolescents, and adults. J Trace Elem Med Biol 11:92–98

    Article  Google Scholar 

  • van Coeverden SC, Netelenbos JC, de Ridder CM, Roos JC, Popp-Snijders C, Delemarre-van de Waal HA (2002) Bone metabolism markers and bone mass in healthy pubertal boys and girls. Clin Endocrinol (oxf) 57:107–116

    Article  Google Scholar 

  • Wei MH, Cui Y, Zhou HL, Song WJ, Di DS, Zhang RY, Huang Q, Liu JA, Wang Q (2021) Associations of multiple metals with bone mineral density: a population-based study in US adults. Chemosphere 282:131150

    Article  CAS  Google Scholar 

  • Yamasaki K, Hagiwara H (2009) Excess iron inhibits osteoblast metabolism. Toxicol Lett 191:211–215

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to express our gratitude to American Journal Experts (https://www.aje.com/) for the language editing services provided.

Funding

This study was supported by the National Natural Science Foundation of China (81874017, 81960403, and 82060405) and Cuiying Scientific and Technological Innovation Program of Lanzhou University Second Hospital (CY2017-ZD02, CY2021-MS-A07).

Author information

Author notes

  1. Jinmin Liu and Yuchen Tang contributed equally to this work.

Authors and Affiliations

  1. Department of Orthopaedics, Lanzhou University Second Hospital, Gansu, Lanzhou, China

    Jinmin Liu, Yuchen Tang, Yi Chen, Xiaohui Zhang, Yayi Xia & Bin Geng

  2. Orthopaedics Key Laboratory of Gansu Province, Gansu, Lanzhou, China

    Jinmin Liu, Yuchen Tang, Yi Chen, Xiaohui Zhang, Yayi Xia & Bin Geng

  3. Orthopaedic Clinical Research Center of Gansu Province, Gansu, Lanzhou, China

    Jinmin Liu, Yuchen Tang, Yi Chen, Xiaohui Zhang, Yayi Xia & Bin Geng

  4. Lanzhou University Second Hospital, #82 Cuiyingmen, Lanzhou, Gansu, 730000, People’s Republic of China

    Bin Geng

Authors
  1. Jinmin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuchen Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yi Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaohui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yayi Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bin Geng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JL and YT contributed equally to this work, contributed the central idea, and analyzed most of the data. JL wrote the initial draft of the paper. The remaining authors contributed to refining the ideas, carrying out additional analyses, and finalizing this paper.

Corresponding author

Correspondence to Bin Geng.

Ethics declarations

Ethics approval

The ethics review board of the National Center for Health Statistics approved the study. The detailed information was provided on the NHANES website.

Consent to participate

Informed consent was obtained from all study participants. The detailed information was provided on the NHANES website.

Consent for publication

Not applicable.

Conflicts of interest

The authors declare no conflict of interest.

Additional information

Responsible Editor: Lotfi Aleya

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 20 KB)

Supplementary file2 (DOCX 18 KB)

Supplementary file3 (DOCX 18 KB)

ESM 4

(PNG 92 kb)

11356_2022_24314_MOESM4_ESM.tif

The relationship between blood manganese concentration and BMD stratified by age. Sex, race, poverty income ratio, BMI status, ALT, AST, total serum calcium, phosphorus, creatinine, blood lead, blood cadmium, use of glucocorticoid, milk intake, and physical activity level were adjusted. (A) Lumbar spine BMD; (B) Pelvis BMD; (C) Total BMD; (D) Trunk bone BMD. BMD, bone mineral density; BMI, body mass index; ALT, alanine aminotransferase; AST, aspartate aminotransferase. High resolution image (TIF 9724 kb) 

ESM 5

(PNG 147 kb)

11356_2022_24314_MOESM5_ESM.tif

The relationship between blood manganese concentration and BMD stratified by race. Age, sex, poverty income ratio, BMI status, ALT, AST, total serum calcium, phosphorus, creatinine, blood lead, blood cadmium, use of glucocorticoid, milk intake, and physical activity level were adjusted. (A) Lumbar spine BMD; (B) Pelvis BMD; (C) Total BMD; (D) Trunk bone BMD. BMD, bone mineral density; BMI, body mass index; ALT, alanine aminotransferase; AST, aspartate aminotransferase. High resolution image (TIF 9872 kb) 

ESM 6

(PNG 89 kb)

11356_2022_24314_MOESM6_ESM.tif

The relationship between blood manganese concentration and BMD stratified in male participants stratified by age. Race, poverty income ratio, BMI status, ALT, AST, total serum calcium, phosphorus, creatinine, blood lead, blood cadmium, use of glucocorticoid, milk intake, and physical activity level were adjusted. (A) Lumbar spine BMD; (B) Pelvis BMD; (C) Total BMD; (D) Trunk bone BMD. BMD, bone mineral density; BMI, body mass index; ALT, alanine aminotransferase; AST, aspartate aminotransferase. High resolution image (TIF 9706 kb) 

ESM 7

(PNG 93 kb)

11356_2022_24314_MOESM7_ESM.tif

The relationship between blood manganese concentration and BMD stratified in female participants stratified by age. Race, poverty income ratio, BMI status, ALT, AST, total serum calcium, phosphorus, creatinine, blood lead, blood cadmium, use of glucocorticoid, milk intake, and physical activity level were adjusted. (A) Lumbar spine BMD; (B) Pelvis BMD; (C) Total BMD; (D) Trunk bone BMD. BMD, bone mineral density; BMI, body mass index; ALT, alanine aminotransferase; AST, aspartate aminotransferase. High resolution image (TIF 9670 kb) 

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, J., Tang, Y., Chen, Y. et al. Association between blood manganese and bone mineral density in US adolescents. Environ Sci Pollut Res 30, 29743–29754 (2023). https://doi.org/10.1007/s11356-022-24314-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-24314-9

Keywords

Search

Navigation