J Bone Metab.  2017 Aug;24(3):161-173. 10.11005/jbm.2017.24.3.161.

Association between Hemoglobin Level and Bone Mineral Density in Korean Adults

• Oh YH
• Moon JH
• Cho B

• KMID: 2415954
• DOI: http://doi.org/10.11005/jbm.2017.24.3.161

Abstract

BACKGROUND
Low bone mineral density (BMD) increases fracture risk. Anemia is highly prevalent. Some studies suggested that anemia is an independent risk factor for osteoporosis. The aim of this study was to evaluate the association between hemoglobin (Hb) level and BMD in Korean adults.
METHODS
This study was based on data from the Korea National Health and Nutrition Examination Survey 2008 to 2011. Propensity score-matching was performed to establish a dataset for analysis. Regression analyses were used to evaluate the association between Hb and BMD. Mean BMD scores were compared between normal and anemia groups, and among normal, anemia with low ferritin, and anemia without low ferritin groups.
RESULTS
There were partial positive associations between Hb and BMD in men, but negative associations in women. The normal group had lower mean BMD scores than the anemia group in men. However, the anemia group had higher whole-body and lumbar-spine BMD scores than the normal group in women. In a comparison of the three groups, the anemia without low ferritin group had the lowest all-site BMD scores in men and women. However, the anemia with low ferritin group had the highest all-site BMD scores in women. In postmenopausal women, the anemia without low ferritin group had the lowest all-site BMD scores. In premenopausal women, the anemia with low ferritin group had the highest whole-body BMD scores.
CONCLUSIONS
This study found that Hb and anemia status were associated with BMD scores. However, the associations were different according to sex. This may be due to the etiology of anemia or low Hb levels.

Keyword

Anemia; Bone density; Hemoglobins

MeSH Terms

Adult*
Anemia
Bone Density*
Dataset
Female
Ferritins
Humans
Korea
Male
Nutrition Surveys
Osteoporosis
Risk Factors
Ferritins

Figure

• 

  Fig. 1 Flow diagram on selection of dataset. *2008-2011 The Fourth & The Fifth Korean National Health and Nutrition Examination. KNHANES, Korea National Health and Nutrition Examination Survey; DXA, dual energy X-ray absorptionmetry; BMD, bone mineral density.

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  Fig. 2 Bone mineral densities (BMDs) of whole body, femoral neck and lumbar spine by sex.

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  Fig. 3 Bone mineral densities (BMDs) of whole body, femoral neck, and lumbar spine across anemia-serum ferritin categories by sex. w/o, without.

Reference

1. Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int. 2006; 17:1726–1733.

2. Jang EJ, Lee YK, Choi HJ, et al. Osteoporotic fracture risk assessment using bone mineral density in Korean: a community-based cohort study. J Bone Metab. 2016; 23:34–39.

3. New SA. Exercise, bone and nutrition. Proc Nutr Soc. 2001; 60:265–274.

4. Espallargues M, Sampietro-Colom L, Estrada MD, et al. Identifying bone-mass-related risk factors for fracture to guide bone densitometry measurements: a systematic review of the literature. Osteoporos Int. 2001; 12:811–822.

5. Tang YJ, Sheu WH, Liu PH, et al. Positive associations of bone mineral density with body mass index, physical activity, and blood triglyceride level in men over 70 years old: a TCVGHAGE study. J Bone Miner Metab. 2007; 25:54–59.

6. Varenna M, Binelli L, Zucchi F, et al. Prevalence of osteoporosis by educational level in a cohort of postmenopausal women. Osteoporos Int. 1999; 9:236–241.

7. Campion JM, Maricic MJ. Osteoporosis in men. Am Fam Physician. 2003; 67:1521–1526.

8. Fujimoto H, Fujimoto K, Ueda A, et al. Hypoxemia is a risk factor for bone mass loss. J Bone Miner Metab. 1999; 17:211–216.

9. Karadag F, Cildag O, Yurekli Y, et al. Should COPD patients be routinely evaluated for bone mineral density? J Bone Miner Metab. 2003; 21:242–246.

10. Laudisio A, Marzetti E, Antonica L, et al. Association of left ventricular function with bone mineral density in older women: a population-based study. Calcif Tissue Int. 2008; 82:27–33.

11. Sarrai M, Duroseau H, D'Augustine J, et al. Bone mass density in adults with sickle cell disease. Br J Haematol. 2007; 136:666–672.

12. Gasche C. Complications of inflammatory bowel disease. Hepatogastroenterology. 2000; 47:49–56.

13. Taal MW, Masud T, Green D, et al. Risk factors for reduced bone density in haemodialysis patients. Nephrol Dial Transplant. 1999; 14:1922–1928.

14. Rutten EP, Franssen FM, Spruit MA, et al. Anemia is associated with bone mineral density in chronic obstructive pulmonary disease. Copd. 2013; 10:286–292.

15. Korkmaz U, Korkmaz N, Yazici S, et al. Anemia as a risk factor for low bone mineral density in postmenopausal Turkish women. Eur J Intern Med. 2012; 23:154–158.

16. Gurevitch O, Slavin S. The hematological etiology of osteoporosis. Med Hypotheses. 2006; 67:729–735.

17. Cesari M, Pahor M, Lauretani F, et al. Bone density and hemoglobin levels in older persons: results from the InCHIANTI study. Osteoporos Int. 2005; 16:691–699.

18. Laudisio A, Marzetti E, Pagano F, et al. Haemoglobin levels are associated with bone mineral density in the elderly: a population-based study. Clin Rheumatol. 2009; 28:145–151.

19. Kim CW, Hong S, Oh SH, et al. Change of bone mineral density and biochemical markers of bone turnover in patients on suppressive levothyroxine therapy for differentiated thyroid carcinoma. J Bone Metab. 2015; 22:135–141.

20. Chun MY. Validity and reliability of Korean version of international physical activity questionnaire short form in the elderly. Korean J Fam Med. 2012; 33:144–151.

21. Orimo H, Hayashi Y, Fukunaga M, et al. Diagnostic criteria for primary osteoporosis: year 2000 revision. J Bone Miner Metab. 2001; 19:331–337.

22. WHO Scientific Group. Nutritional anaemias. Report of a WHO scientific group. World Health Organ Tech Rep Ser. 1968; 405:5–37.

23. World Health Organization. Serum ferritin concentrations for the assessment of iron status and iron deficiency in populations. 2011. cited by 2016 March 1. Available from: www.who.int/vmnis/indicators/serum_ferritin.pdf.

24. Choi CD, Oh HJ, Joo IW, et al. The relationship between bone mineral density and behavioral factors in Korean adult men using data from the Korea national health and nutrition examination survey IV. Osteoporosis. 2012; 10:67–75.

25. Mun SO, Kim J, Yang YJ. Factors associated with bone mineral density in Korean postmenopausal women aged 50 years and above: using 2008-2010 Korean national health and nutrition examination survey. Korean J Community Nutr. 2013; 18:177–186.

26. Hardy R, Cooper MS. Bone loss in inflammatory disorders. J Endocrinol. 2009; 201:309–320.

27. Leng S, Chaves P, Koenig K, et al. Serum interleukin-6 and hemoglobin as physiological correlates in the geriatric syndrome of frailty: a pilot study. J Am Geriatr Soc. 2002; 50:1268–1271.

28. Hamed EA, Mohamed NA, El-Metwally TH, et al. Iron chelation therapy in upper Egyptian transfusion-dependent pediatric homozygous beta-thalassemia major: impact on serum L-carnitine/free fatty acids, osteoprotegerin/the soluble receptor activator of nuclear factor-kappabeta ligand systems, and bone mineral density. J Pediatr Hematol Oncol. 2010; 32:267–273.

29. Giri N, Batista DL, Alter BP, et al. Endocrine abnormalities in patients with Fanconi anemia. J Clin Endocrinol Metab. 2007; 92:2624–2631.

30. McLean E, Cogswell M, Egli I, et al. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr. 2009; 12:444–454.

31. Guralnik JM, Eisenstaedt RS, Ferrucci L, et al. Prevalence of anemia in persons 65 years and older in the United States: evidence for a high rate of unexplained anemia. Blood. 2004; 104:2263–2268.

32. Risteli L, Risteli J. Biochemical markers of bone metabolism. Ann Med. 1993; 25:385–393.