Osteoporosis International

, Volume 30, Issue 1, pp 201–209 | Cite as

Trabecular microstructure is influenced by race and sex in Black and White young adults

  • K.L. PoppEmail author
  • C. Xu
  • A. Yuan
  • J.M. Hughes
  • G. Unnikrishnan
  • J. Reifman
  • M.L. Bouxsein
Original Article



Lower fracture rates in Black men and women compared to their White counterparts are incompletely understood. High-resolution imaging specific to trabecular bone may provide insight. Black participants have enhanced trabecular morphology. These differences may contribute to the lower fracture risk in Black versus White individuals.


Lower fracture rates in Black men and women compared to their White counterparts may be explained by favorable bone microstructure in Black individuals. Individual trabecular segmentation (ITS) analysis, which characterizes the alignment and plate- and rod-like nature of trabecular bone using high-resolution peripheral quantitative computed tomography (HR-pQCT), may provide insight into trabecular differences by race/ethnic origin.


We determined differences in trabecular bone microarchitecture, connectivity, and alignment according to race/ethnic origin and sex in young adults.


We analyzed HR-pQCT scans of 184 adult (24.2 ± 3.4 years) women (n = 51 Black, n = 50 White) and men (n = 34 Black, n = 49 White). We used ANCOVA to compare bone outcomes, and adjusted for age, height, and weight.


Overall, the effect of race on bone outcomes did not differ by sex, and the effect of sex on bone outcomes did not differ by race. After adjusting for covariates, Black participants and men of both races had greater trabecular plate volume fraction, plate thickness, plate number density, plate surface area, and greater axial alignment of trabeculae, leading to higher trabecular bone stiffness compared to White participants and women, respectively (p < 0.05 for all).


These findings demonstrate that more favorable bone microarchitecture in Black individuals compared to White individuals and in men compared to women is not unique to the cortical bone compartment. Enhanced plate-like morphology and greater trabecular axial alignment, established in young adulthood, may contribute to the improved bone strength and lower fracture risk in Black versus White individuals and in men compared to women.


Bone mineral density (BMD) Fracture risk Gender High-resolution peripheral quantitative computed tomography (HR-pQCT) Individual trabecular segmentation Stress fracture risk 



This study is supported by the U.S. Department of Defense, Defense Health Program, and Joint Program Committee (W811XWH-15-C-0024) managed by the U.S. Army Military Operational Medicine Program at the U.S. Army Medical Research and Materiel Command, Fort Detrick, MD, and the National Institutes of Health shared instrumentation grant (S10 RR023405).

Compliance with ethical standards

Conflicts of interest



The opinions or assertions contained herein are the private views of the authors and are not to be construed as official or reflecting the views of the U.S. Army or the U.S. Department of Defense. Any citations of commercial organizations and trade names in this report do not constitute an official Department of the Army endorsement of approval of the products or services of these organizations.


  1. 1.
    Lee, D. and C. Armed Forces Health surveillance, Stress fractures, active component, U.S. Armed Forces, 2004-2010. MSMR, 2011. 18(5): p. 8–11Google Scholar
  2. 2.
    Kanis JA, Johnell O, de Laet C, Jonsson B, Oden A, Ogelsby AK (2002) International variations in hip fracture probabilities: implications for risk assessment. J Bone Miner Res 17(7):1237–1244CrossRefGoogle Scholar
  3. 3.
    Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A (2007) Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025. J Bone Miner Res 22(3):465–475CrossRefGoogle Scholar
  4. 4.
    Wren TA et al (2012) Racial disparity in fracture risk between white and nonwhite children in the United States. J Pediatr 161(6):1035–1040CrossRefGoogle Scholar
  5. 5.
    Bulathsinhala L et al (2017) Risk of stress fracture varies by race/ethnic origin in a cohort study of 1.3 million U.S. Army soldiers. In: J Bone Miner ResGoogle Scholar
  6. 6.
    Bell NH et al (1991) Demonstration that bone mass is greater in black than in white children. J Bone Miner Res 6(7):719–723CrossRefGoogle Scholar
  7. 7.
    Ettinger B et al (1997) Racial differences in bone density between young adult black and white subjects persist after adjustment for anthropometric, lifestyle, and biochemical differences. J Clin Endocrinol Metab 82(2):429–434Google Scholar
  8. 8.
    Cauley JA, Lui LY, Stone KL, Hillier TA, Zmuda JM, Hochberg M, Beck TJ, Ensrud KE (2005) Longitudinal study of changes in hip bone mineral density in Caucasian and African-American women. J Am Geriatr Soc 53(2):183–189CrossRefGoogle Scholar
  9. 9.
    Putman MS, Yu EW, Lee H, Neer RM, Schindler E, Taylor AP, Cheston E, Bouxsein ML, Finkelstein JS (2013) Differences in skeletal microarchitecture and strength in African-American and white women. J Bone Miner Res 28(10):2177–2185CrossRefGoogle Scholar
  10. 10.
    Boutroy S et al (2008) Finite element analysis based on in vivo HR-pQCT images of the distal radius is associated with wrist fracture in postmenopausal women. J Bone Miner Res 23(3):392–399CrossRefGoogle Scholar
  11. 11.
    Stein EM, Liu XS, Nickolas TL, Cohen A, Thomas V, McMahon DJ, Zhang C, Yin PT, Cosman F, Nieves J, Guo XE, Shane E (2010) Abnormal microarchitecture and reduced stiffness at the radius and tibia in postmenopausal women with fractures. J Bone Miner Res 25(12):2572–2581CrossRefGoogle Scholar
  12. 12.
    Cohen A, Liu XS, Stein EM, McMahon DJ, Rogers HF, LeMaster J, Recker RR, Lappe JM, Guo XE, Shane E (2009) Bone microarchitecture and stiffness in premenopausal women with idiopathic osteoporosis. J Clin Endocrinol Metab 94(11):4351–4360CrossRefGoogle Scholar
  13. 13.
    Popp KL, Hughes JM, Martinez-Betancourt A, Scott M, Turkington V, Caksa S, Guerriere KI, Ackerman KE, Xu C, Unnikrishnan G, Reifman J, Bouxsein ML (2017) Bone mass, microarchitecture and strength are influenced by race/ethnicity in young adult men and women. Bone 103:200–208CrossRefGoogle Scholar
  14. 14.
    Wang J, Zhou B, Liu XS, Fields AJ, Sanyal A, Shi X, Adams M, Keaveny TM, Guo XE (2015) Trabecular plates and rods determine elastic modulus and yield strength of human trabecular bone. Bone 72:71–80CrossRefGoogle Scholar
  15. 15.
    Liu XS, Cohen A, Shane E, Stein E, Rogers H, Kokolus SL, Yin PT, McMahon DJ, Lappe JM, Recker RR, Guo XE (2010) Individual trabeculae segmentation (ITS)-based morphological analysis of high-resolution peripheral quantitative computed tomography images detects abnormal trabecular plate and rod microarchitecture in premenopausal women with idiopathic osteoporosis. J Bone Miner Res 25(7):1496–1505CrossRefGoogle Scholar
  16. 16.
    Mitchell DM, Tuck P, Ackerman KE, Cano Sokoloff N, Woolley R, Slattery M, Lee H, Bouxsein ML, Misra M (2015) Altered trabecular bone morphology in adolescent and young adult athletes with menstrual dysfunction. Bone 81:24–30CrossRefGoogle Scholar
  17. 17.
    Putman MS, Greenblatt LB, Sicilian L, Uluer A, Lapey A, Sawicki G, Gordon CM, Bouxsein ML, Finkelstein JS (2016) Young adults with cystic fibrosis have altered trabecular microstructure by ITS-based morphological analysis. Osteoporos Int 27(8):2497–2505CrossRefGoogle Scholar
  18. 18.
    Kepley AL, Nishiyama KK, Zhou B, Wang J, Zhang C, McMahon DJ, Foley KF, Walker MD, Edward Guo X, Shane E, Nickolas TL (2017) Differences in bone quality and strength between Asian and Caucasian young men. Osteoporos Int 28(2):549–558CrossRefGoogle Scholar
  19. 19.
    Liu XS, Walker MD, McMahon DJ, Udesky J, Liu G, Bilezikian JP, Guo XE (2011) Better skeletal microstructure confers greater mechanical advantages in Chinese-American women versus white women. J Bone Miner Res 26(8):1783–1792CrossRefGoogle Scholar
  20. 20.
    Putman MS et al (2016) Differences in trabecular microstructure between black and white women assessed by individual trabecular segmentation analysis of HR-pQCT images. In: J Bone Miner ResGoogle Scholar
  21. 21.
    Pialat JB, Burghardt AJ, Sode M, Link TM, Majumdar S (2012) Visual grading of motion induced image degradation in high resolution peripheral computed tomography: impact of image quality on measures of bone density and micro-architecture. Bone 50(1):111–118CrossRefGoogle Scholar
  22. 22.
    Unnikrishnan G, Xu C, Popp KL, Hughes JM, Yuan A, Guerriere KI, Caksa S, Ackerman KE, Bouxsein ML, Reifman J (2018) Regional variation of bone density, microarchitectural parameters, and elastic moduli in the ultradistal tibia of young black and white men and women. Bone 112:194–201CrossRefGoogle Scholar
  23. 23.
    Liu XS et al (2008) Complete volumetric decomposition of individual trabecular plates and rods and its morphological correlations with anisotropic elastic moduli in human trabecular bone. J Bone Miner Res 23(2):223–235CrossRefGoogle Scholar
  24. 24.
    Liu XS, Shane E, McMahon DJ, Guo XE (2011) Individual trabecula segmentation (ITS)-based morphological analysis of microscale images of human tibial trabecular bone at limited spatial resolution. J Bone Miner Res 26(9):2184–2193CrossRefGoogle Scholar
  25. 25.
    Schnitzler CM, Pettifor JM, Mesquita JM, Bird MDT, Schnaid E, Smyth AE (1990) Histomorphometry of iliac crest bone in 346 normal black and white South African adults. Bone Miner 10(3):183–199CrossRefGoogle Scholar
  26. 26.
    Wang Q, Wang XF, Iuliano-Burns S, Ghasem-Zadeh A, Zebaze R, Seeman E (2010) Rapid growth produces transient cortical weakness: a risk factor for metaphyseal fractures during puberty. J Bone Miner Res 25(7):1521–1526CrossRefGoogle Scholar
  27. 27.
    Nishiyama KK, Macdonald HM, Moore SA, Fung T, Boyd SK, McKay HA (2012) Cortical porosity is higher in boys compared with girls at the distal radius and distal tibia during pubertal growth: an HR-pQCT study. J Bone Miner Res 27(2):273–282CrossRefGoogle Scholar
  28. 28.
    Burrows M et al (2010) Bone microstructure at the distal tibia provides a strength advantage to males in late puberty: an HR-pQCT study. J Bone Miner Res 25(6):1423–1432Google Scholar
  29. 29.
    Gabel L, Macdonald HM, McKay HA (2016) Sex differences and growth-related adaptations in bone microarchitecture, geometry, density, and strength from childhood to early adulthood: a mixed longitudinal HR-pQCT study. J Bone Miner ResGoogle Scholar
  30. 30.
    Moayyeri A, Hammond CJ, Hart DJ, Spector TD (2012) Effects of age on genetic influence on bone loss over 17 years in women: the healthy ageing twin study (HATS). J Bone Miner Res 27(10):2170–2178CrossRefGoogle Scholar
  31. 31.
    Araujo AB, Yang M, Suarez EA, Dagincourt N, Abraham JR, Chiu G, Holick MF, Bouxsein ML, Zmuda JM (2014) Racial/ethnic and socioeconomic differences in bone loss among men. J Bone Miner Res 29(12):2552–2560CrossRefGoogle Scholar
  32. 32.
    Ackerman KE, Nazem T, Chapko D, Russell M, Mendes N, Taylor AP, Bouxsein ML, Misra M (2011) Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J Clin Endocrinol Metab 96(10):3123–3133CrossRefGoogle Scholar
  33. 33.
    Sigurdsson G, Halldorsson BV, Styrkarsdottir U, Kristjansson K, Stefansson K (2008) Impact of genetics on low bone mass in adults. J Bone Miner Res 23(10):1584–1590CrossRefGoogle Scholar
  34. 34.
    Ruffing JA, Nieves JW, Zion M, Tendy S, Garrett P, Lindsay R, Cosman F (2007) The influence of lifestyle, menstrual function and oral contraceptive use on bone mass and size in female military cadets. Nutr Metab (Lond) 4:17CrossRefGoogle Scholar
  35. 35.
    Cadogan J, Eastell R, Jones N, Barker ME (1997) Milk intake and bone mineral acquisition in adolescent girls: randomised, controlled intervention trial. BMJ 315(7118):1255–1260CrossRefGoogle Scholar
  36. 36.
    Modlesky CM, Majumdar S, Dudley GA (2008) Trabecular bone microarchitecture in female collegiate gymnasts. Osteoporos Int 19(7):1011–1018CrossRefGoogle Scholar
  37. 37.
    Heinonen A, Kannus P, Sievänen H, Oja P, Pasanen M, Rinne M, Uusi-Rasi K, Vuori I (1996) Randomised controlled trial of effect of high-impact exercise on selected risk factors for osteoporotic fractures. Lancet 348(9038):1343–1347CrossRefGoogle Scholar
  38. 38.
    Carter DR, Orr TE, Fyhrie DP (1989) Relationships between loading history and femoral cancellous bone architecture. J Biomech 22(3):231–244CrossRefGoogle Scholar
  39. 39.
    Raux P, Townsend PR, Miegel R, Rose RM, Radin EL (1975) Trabecular architecture of the human patella. J Biomech 8(1):1–7CrossRefGoogle Scholar
  40. 40.
    Biewener AA, Fazzalari NL, Konieczynski DD, Baudinette RV (1996) Adaptive changes in trabecular architecture in relation to functional strain patterns and disuse. Bone 19(1):1–8CrossRefGoogle Scholar
  41. 41.
    Araujo AB, et al., Race/ethnic differences in bone mineral density in menGoogle Scholar
  42. 42.
    Zhou B, Sherry Liu X, Wang J, Lucas Lu X, Fields AJ, Edward Guo X (2014) Dependence of mechanical properties of trabecular bone on plate-rod microstructure determined by individual trabecula segmentation (ITS). J Biomech 47(3):702–708CrossRefGoogle Scholar
  43. 43.
    Stauber M, Muller R (2006) Volumetric spatial decomposition of trabecular bone into rods and plates--a new method for local bone morphometry. Bone 38(4):475–484CrossRefGoogle Scholar
  44. 44.
    Wang J, Stein EM, Zhou B, Nishiyama KK, Yu YE, Shane E, Guo XE (2016) Deterioration of trabecular plate-rod and cortical microarchitecture and reduced bone stiffness at distal radius and tibia in postmenopausal women with vertebral fractures. Bone 88:39–46CrossRefGoogle Scholar
  45. 45.
    Liu XS, Stein EM, Zhou B, Zhang CA, Nickolas TL, Cohen A, Thomas V, McMahon DJ, Cosman F, Nieves J, Shane E, Guo XE (2012) Individual trabecula segmentation (ITS)-based morphological analyses and microfinite element analysis of HR-pQCT images discriminate postmenopausal fragility fractures independent of DXA measurements. J Bone Miner Res 27(2):263–272CrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Authors and Affiliations

  1. 1.Endocrine UnitMassachusetts General HospitalBostonUSA
  2. 2.Department of MedicineHarvard Medical SchoolBostonUSA
  3. 3.Military Performance DivisionUnited States Army Research Institute of Environmental MedicineNatickUSA
  4. 4.Department of Defense Biotechnology High Performance Computing Software Applications Institute, Telemedicine and Advance Technology Research CenterUnited States Army Medical Research and Materiel CommandFort DetrickUSA
  5. 5.Center for Advanced Orthopedic Studies, Beth Israel Deaconess Medical Center, and Department of Orthopedic SurgeryHarvard Medical SchoolBostonUSA

Personalised recommendations