Log in

Detrimental Association Between Blood Cadmium Concentration and Trabecular Bone Score

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Osteoporosis has been recognized as a significant cause of disability in the elderly leading to heavy socioeconomic burden. Current measurements such as dual-energy X-ray absorptiometry (DEXA) and bone mineral density (BMD) have limitations. In contrast, trabecular bone score (TBS) is an emerging tool for bone quality assessment. The objective of our study was to investigate the relationship between TBS and trace elements (cadmium and lead). We analyzed all subjects from the 2005–2006 and 2007–2008 National Health and Nutrition Examination Survey (NHANES) dataset and included a total of 8,244 participants in our study; 49.4% of the enrolled subjects were male. We used blood cadmium (Cd) and lead (Pb) concentrations to define environmental exposure. The main variables were TBS and BMD. Other significant demographic features were included as covariates and later adjusted using linear regression models to determine the association between TBS and four quartiles based on the blood trace element concentrations with or without sex differences. The fully adjusted regression model revealed a negative relationship between TBS and blood cadmium (B-Cd) significant for both males and females (both p < 0.05). The β-coefficient for males was −0.009 (95% confidence intervals (CI): (−0.015 to −0.004)) and −0.019 for female (95% CI: (−0.024 to −0.013)). We also found a dose-dependent relationship between TBS and B-Cd for both sexes (both trend’s p < 0.05). Our study concluded that TBS could measure Cd-related bone quality deterioration for both males and females.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Data Availability

The datasets generated during and/or analyzed during the current study are not publicly available due to containing information that could compromise the privacy of research participants but are available from the corresponding author on reasonable request.

Abbreviations

B-Cd :

Blood cadmium

B-Pb :

Blood lead

BMD :

Bone mineral density

BMI :

Body mass index

Cd :

Cadmium

CHD :

Coronary heart disease

CHF :

Congestive heart failure

CRP :

C-reactive protein

DEXA :

Dual-energy X-ray absorptiometry

FRAX :

Fracture Risk Assessment Tool

LOD :

Lower limit of detection

lsBMD :

Lumbar spine BMD

NHANES :

National Health and Nutrition Examination Survey program

Pb :

Lead

TBS :

Trabecular bone score

WHO :

World Health Organization

References

  1. Harvey N, Dennison E, Cooper C (2010) Osteoporosis: impact on health and economics. Nat Rev Rheumatol. 6(2):99–105

    Article  Google Scholar 

  2. Johnell O, Kanis JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int. 17(12):1726–33

    Article  CAS  Google Scholar 

  3. Johnell O (1997) The socioeconomic burden of fractures: today and in the 21st century. Am J Med 03(2a):20S–25S; discussion 5S-6S

  4. Morgan SL, Prater GL (2017) Quality in dual-energy X-ray absorptiometry scans. Bone. 104:13–28

    Article  CAS  Google Scholar 

  5. Syed Z, Khan A (2002) Bone densitometry: applications and limitations. J Obstet Gynaecol Can. 24(6):476–84

    Article  Google Scholar 

  6. Iconaru L, Moreau M, Kinnard V et al (2019) Does the prediction accuracy of osteoporotic fractures by BMD and clinical risk factors vary with fracture site? JBMR Plus. 3(12):e10238

    Article  CAS  Google Scholar 

  7. Middleton RG, Shabani F, Uzoigwe CE, et al. (2012) FRAX and the assessment of the risk of develo** a fragility fracture. J Bone Joint Surg Br Vol 94-B(10):1313–1320

  8. Silverman SL, Calderon AD (2010) The utility and limitations of FRAX: a US perspective. Curr Osteoporos Rep. 8(4):192–7

    Article  Google Scholar 

  9. Campbell JR, Auinger P (2007) The association between blood lead levels and osteoporosis among adults–results from the third national health and nutrition examination survey (NHANES III). Environ Health Perspect. 115(7):1018–22

    Article  CAS  Google Scholar 

  10. Gallagher CM, Kovach JS, Meliker JR (2008) Urinary cadmium and osteoporosis in U.S. women &#x2265;50 years of age: NHANES 1988&#x2013;1994 and 1999&#x2013;2004. Environ Health Perspect 116(10):1338–1343

  11. Silva BC, Leslie WD, Resch H et al (2014) Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res. 29(3):518–30

    Article  Google Scholar 

  12. Pothuaud L, Carceller P, Hans D (2008) Correlations between grey-level variations in 2D projection images (TBS) and 3D microarchitecture: applications in the study of human trabecular bone microarchitecture. Bone. 42(4):775–87

    Article  Google Scholar 

  13. Bousson V, Bergot C, Sutter B et al (2012) Trabecular bone score (TBS): available knowledge, clinical relevance, and future prospects. Osteoporos Int. 23(5):1489–501

    Article  CAS  Google Scholar 

  14. Hans D, Šteňová E, Lamy O (2017) The trabecular bone score (TBS) complements DXA and the FRAX as a fracture risk assessment tool in routine clinical practice. Curr Osteoporos Rep. 15(6):521–31

    Article  Google Scholar 

  15. Sheu A, Diamond T (2016) Bone mineral density: testing for osteoporosis. Aust Prescr. 39(2):35–9

    Article  Google Scholar 

  16. Amnuaywattakorn S, Sritara C, Utamakul C et al (2016) Simulated increased soft tissue thickness artefactually decreases trabecular bone score: a phantom study. BMC Musculoskelet Disord. 17:17

    Article  Google Scholar 

  17. Shevroja E, Lamy O, Kohlmeier L et al (2017) Use of trabecular bone score (TBS) as a complementary approach to dual-energy X-ray absorptiometry (DXA) for fracture risk assessment in clinical practice. J Clin Densitom. 20(3):334–45

    Article  Google Scholar 

  18. Pabis K, Chiari Y, Sala C et al (2021) Elevated metallothionein expression in long-lived species mediates the influence of cadmium accumulation on aging. Geroscience 43(4):1975–1993

    Article  CAS  Google Scholar 

  19. Tinkov AA, Filippini T, Ajsuvakova OP et al (2017) The role of cadmium in obesity and diabetes. Sci Total Environ 601–602:741–55

    Article  Google Scholar 

  20. Johri N, Jacquillet G, Unwin R (2010) Heavy metal poisoning: the effects of cadmium on the kidney. BioMetals 23(5):783–92

    Article  CAS  Google Scholar 

  21. Buser MC, Ingber SZ, Raines N et al (2016) Urinary and blood cadmium and lead and kidney function: NHANES 2007–2012. Int J Hyg Environ Health 219(3):261–7

    Article  CAS  Google Scholar 

  22. Järup L, Berglund M, Elinder CG et al (1998) Health effects of cadmium exposure – a review of the literature and a risk estimate. Scand J Work Environ Health. 24:1–51

    Google Scholar 

  23. Waalkes MP (2003) Cadmium carcinogenesis. Mutat Res. 533(1–2):107–20

    Article  CAS  Google Scholar 

  24. Zofkova I, Davis M, Blahos J (2017) Trace elements have beneficial, as well as detrimental effects on bone homeostasis. Physiol Res. 66(3):391–402

    Article  CAS  Google Scholar 

  25. Alfvén T, Elinder C-G, Carlsson MD et al (2000) Low-level cadmium exposure and osteoporosis. J Bone Miner Res. 15(8):1579–86

    Article  Google Scholar 

  26. Sun Y, Sun D, Zhou Z et al (2008) Osteoporosis in a Chinese population due to occupational exposure to lead. Am J Ind Med 51(6):436–42

    Article  CAS  Google Scholar 

  27. Alfvén T, Elinder CG, Carlsson MD et al (2000) Low-level cadmium exposure and osteoporosis. J Bone Miner Res 15(8):1579–86

    Article  Google Scholar 

  28. Järup L, Alfvén T, Persson B et al (1998) Cadmium may be a risk factor for osteoporosis. Occup Environ Med 55(7):435–9

    Article  Google Scholar 

  29. Hans D, Barthe N, Boutroy S et al (2011) Correlations between trabecular bone score, measured using anteroposterior dual-energy X-ray absorptiometry acquisition, and 3-dimensional parameters of bone microarchitecture: an experimental study on human cadaver vertebrae. J Clin Densitom 14(3):302–12

    Article  Google Scholar 

  30. Pouillès J-M, Gosset A, Breteau A, Trémollieres FA (2021) TBS in early postmenopausal women with severe vertebral osteoporosis. Bone. 142:115698

    Article  Google Scholar 

  31. Greendale GA, Huang M, Cauley JA et al (2020) Trabecular bone score declines during the menopause transition: the study of Women’s Health Across the Nation (SWAN). J Clin Endocrinol Metab. 105(4):e1872-82

    Article  Google Scholar 

  32. Povoroznyuk V, Musiienko A (2018) Bone mineral density and trabecular bone score in men with vertebral fractures. J Clin Densitom. 21(4):597

    Article  Google Scholar 

  33. Akesson A, Lundh T, Vahter M et al (2005) Tubular and glomerular kidney effects in Swedish women with low environmental cadmium exposure. Environ Health Perspect. 113(11):1627–31

    Article  Google Scholar 

  34. He S, Zhuo L, Cao Y et al (2020) Effect of cadmium on osteoclast differentiation during bone injury in female mice. Environ Toxicol. 35(4):487–94

    Article  CAS  Google Scholar 

  35. He S, Zhuo L, Cao Y et al (2020) Effect of cadmium on osteoclast differentiation during bone injury in female mice. Environ Toxicol. 35(4):487–94

    Article  CAS  Google Scholar 

  36. Chen X, Zhu G, Gu S et al (2009) Effects of cadmium on osteoblasts and osteoclasts in vitro. Environ Toxicol Pharmacol. 28(2):232–6

    Article  CAS  Google Scholar 

  37. Chen X, Wang G, Li X et al (2013) Environmental level of cadmium exposure stimulates osteoclasts formation in male rats. Food Chem Toxicol. 60:530–5

    Article  CAS  Google Scholar 

  38. Iwami K, Moriyama T (1993) Comparative effect of cadmium on osteoblastic cells and osteoclastic cells. Arch Toxicol 67(5):352–7

    Article  CAS  Google Scholar 

  39. Kazantzis G (2004) Cadmium, osteoporosis and calcium metabolism. Biometals 17(5):493–8

    Article  CAS  Google Scholar 

  40. ** T, Nordberg G, Ye T et al (2004) Osteoporosis and renal dysfunction in a general population exposed to cadmium in China. Environ Res 96(3):353–9

    Article  CAS  Google Scholar 

  41. Sugawara N (1977) Inhibitory effect of cadmium on calcium absorption from the rat duodenum. Arch Environ Contam Toxicol 5(1):167–75

    Article  CAS  Google Scholar 

  42. Tsuritani I, Honda R, Ishizaki M et al (1992) Impairment of vitamin D metabolism due to environmental cadmium exposure, and possible relevance to sex-related differences in vulnerability to the bone damage. J Toxicol Environ Health. 37(4):519–33

    Article  CAS  Google Scholar 

  43. Kjellström T (1992) Mechanism and epidemiology of bone effects of cadmium. IARC Sci Publ. 118:301–10

    Google Scholar 

  44. Sweet MG, Sweet JM, Jeremiah MP, Galazka SS (2009) Diagnosis and treatment of osteoporosis. Am Fam Physician. 79(3):193–200

    Google Scholar 

  45. Bonaccorsi G, Fila E, Messina C et al (2017) Comparison of trabecular bone score and hip structural analysis with FRAX® in postmenopausal women with type 2 diabetes mellitus. Aging Clin Exp Res. 29(5):951–7

    Article  Google Scholar 

  46. Lobos S, Cooke A, Simonett G et al (2019) Trabecular bone score at the distal femur and proximal tibia in individuals with spinal cord injury. J Clin Densitom. 22(2):249–56

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Jun-Wei Huang and Wei-Liang Chen designed the initial study. Jun-Wei Huang also managed and retrieved the data, contributed to primary data analysis and explanation, and drafted the initial script. Jun-Wei Huang and Wei-Liang Chen decided on the methods of data collection. Jun-Wei Huang and Wei-Liang Chen were both responsible for the decisions of data analysis. Wei-Liang Chen conceptualized the study, inspected all sides of the study, critically reviewed and revised the initial script, and approved the final manuscript as submitted. All authors meet the ICMJE criteria for authorship.

Corresponding author

Correspondence to Wei-Liang Chen.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Ethics Approval

All statistics of this study were obtained from National Health and Nutrition Examination Survey (NHANES) database, which had been authorized by the National Center for Health Statistics (NCHS) Institutional Review Board (IRB).

Consent to Participate

All participants were asked to complete the informed consents before survey.

Consent for Publication

Our study does not contain any individual person’s data in any form.

Additional information

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 16 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, JW., Fang, WH. & Chen, WL. Detrimental Association Between Blood Cadmium Concentration and Trabecular Bone Score. Biol Trace Elem Res 201, 82–89 (2023). https://doi.org/10.1007/s12011-022-03143-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-022-03143-4

Keywords

Navigation