Abstract
Summary
We analyzed volumetric bone mineral density (vBMD) and bone microstructure using HR-pQCT in subjects with normouricemia (NU) and subjects with hyperuricemia (HU) with and without psoriasis (PSO). HU was associated with higher cortical vBMD and thickness. Differences in average and trabecular vBMD were found between patients with PSO + HU and NU.
Introduction
Hyperuricemia (HU) and gout are co-conditions of psoriasis and psoriatic arthritis. Current data suggest a positive association between HU and areal bone mineral density (BMD) and a negative influence of psoriasis on local bone, even in the absence of arthritis. However, the influence of the combination of HU and psoriasis on bone is still unclear. The aim of this study was to assess the impact of HU with and without psoriasis on bone microstructure and volumetric BMD (vBMD).
Methods
Healthy individuals with uric acid levels within the normal range (NU), with hyperuricemia (HU), patients with hyperuricemia and psoriasis (PSO + HU), and patients with uric acid within the normal range and psoriasis (PSO + NU) were included in our study. Psoriasis patients had no current or past symptoms of arthritis. Average, trabecular, and cortical vBMD (mgHA/cm3); trabecular number (Tb.N, 1/mm) and thickness (Tb.Th, mm); inhomogeneity of the network (1/N.SD, mm); and cortical thickness (Ct.Th., mm) were carried out at the ultradistal radius using high-resolution peripheral quantitative computed tomography. In addition, bone turnover markers such as DKK-1, sclerostin, and P1NP were analyzed.
Results
In total, 130 individuals were included (44 NU participants (34% female), 50 HU (24%), 16 PSO + HU (6%), 20 PSO + NU (60%)). Subjects were aged: NU 54.5 (42.8, 62.1), HU 57.5 (18.6, 65.1), PSO + HU 52.0 (42.3, 57.8), and PSO + NU 42.5 (34.8, 56.8), respectively. After adjusting for age, sex, BMI, and diabetes, patients in the HU group revealed significantly higher values of cortical vBMD (p < 0.001) as well as cortical thickness (p = 0.04) compared to the NU group. PSO + NU showed no differences to NU, but PSO + HU demonstrated both lower average (p = 0.03) and trabecular vBMD (p = 0.02). P1NP was associated with average, cortical, and trabecular vBMD as well as cortical thickness while sclerostin levels were related to trabecular vBMD.
Conclusion
Hyperuricemia in otherwise healthy subjects was associated with a better cortical vBMD and higher cortical thickness. However, patients with both psoriasis and hyperuricemia revealed a lower vBMD.
Similar content being viewed by others
References
Zhu Y, Pandya BJ, Choi HK (2011) Prevalence of gout and hyperuricemia in the US general population: the National Health and Nutrition Examination Survey 2007-2008. Arthritis Rheum 63(10):3136–3141
Feig DI, Kang DH, Johnson RJ (2008) Uric acid and cardiovascular risk. N Engl J Med 359(17):1811–1821
Zurlo A, Veronese N, Giantin V, Maselli M, Zambon S, Maggi S, Musacchio E, Toffanello ED, Sartori L, Perissinotto E, Crepaldi G, Manzato E, Sergi G (2016) High serum uric acid levels increase the risk of metabolic syndrome in elderly women: the PRO.V.A study. Nutr Metab Cardiovasc Dis 26(1):27–35
Harre U, Derer A, Schorn C, Schett G, Herrmann M (2011) T cells as key players for bone destruction in gouty arthritis? Arthritis Res Ther 13(6):135
Ahn SH, Lee SH, Kim BJ, Lim KH, Bae SJ, Kim EH, Kim HK, Choe JW, Koh JM, Kim GS (2013) Higher serum uric acid is associated with higher bone mass, lower bone turnover, and lower prevalence of vertebral fracture in healthy postmenopausal women. Osteoporos Int 24(12):2961–2970
Nabipour I, Sambrook PN, Blyth FM, Janu MR, Waite LM, Naganathan V, Handelsman DJ, le Couteur DG, Cumming RG, Seibel MJ (2011) Serum uric acid is associated with bone health in older men: a cross-sectional population-based study. J Bone Miner Res 26(5):955–964
Kim BJ, Baek S, Ahn SH, Kim SH, Jo MW, Bae SJ, Kim HK, Choe J, Park GM, Kim YH, Lee SH, Kim GS, Koh JM (2014) Higher serum uric acid as a protective factor against incident osteoporotic fractures in Korean men: a longitudinal study using the National Claim Registry. Osteoporos Int 25(7):1837–1844
Lane NE, Parimi N, Lui LY, Wise BL, Yao W, Lay YA et al (2014) Association of serum uric acid and incident nonspine fractures in elderly men: the Osteoporotic Fractures in Men (MrOS) study. J Bone Miner Res 29(7):1701–1707
Kocijan R, Finzel S, Englbrecht M, Engelke K, Rech J, Schett G (2014) Decreased quantity and quality of the periarticular and nonperiarticular bone in patients with rheumatoid arthritis: a cross-sectional HR-pQCT study. J Bone Miner Res 29(4):1005–1014
Kocijan R, Englbrecht M, Haschka J, Simon D, Kleyer A, Finzel S, Kraus S, Resch H, Muschitz C, Engelke K, Sticherling M, Rech J, Schett G (2015) Quantitative and qualitative changes of bone in psoriasis and psoriatic arthritis patients. J Bone Miner Res 30(10):1775–1783
Simon D, Faustini F, Kleyer A, Haschka J, Englbrecht M, Kraus S, Hueber AJ, Kocijan R, Sticherling M, Schett G, Rech J (2016) Analysis of periarticular bone changes in patients with cutaneous psoriasis without associated psoriatic arthritis. Ann Rheum Dis 75(4):660–666
Kleyer A, Finzel S, Rech J, Manger B, Krieter M, Faustini F, Araujo E, Hueber AJ, Harre U, Engelke K, Schett G (2014) Bone loss before the clinical onset of rheumatoid arthritis in subjects with anticitrullinated protein antibodies. Ann Rheum Dis 73(5):854–860
Faustini F, Simon D, Oliveira I, Kleyer A, Haschka J, Englbrecht M, Cavalcante AR, Kraus S, Tabosa TP, Figueiredo C, Hueber AJ, Kocijan R, Cavallaro A, Schett G, Sticherling M, Rech J (2016) Subclinical joint inflammation in patients with psoriasis without concomitant psoriatic arthritis: a cross-sectional and longitudinal analysis. Ann Rheum Dis 75(12):2068–2074
Gisondi P, Targher G, Cagalli A, Girolomoni G (2014) Hyperuricemia in patients with chronic plaque psoriasis. J Am Acad Dermatol 70(1):127–130
AlJohani R, Polachek A, Ye JY, Chandran V, Gladman DD (2017) Characteristic and outcome of psoriatic arthritis patients with hyperuricemia. J Rheumatol
Goldman M (1981) Uric acid in the etiology of psoriasis. Am J Dermatopathol 3(4):397–404
Tsuruta N, Imafuku S, Narisawa Y (2017) Hyperuricemia is an independent risk factor for psoriatic arthritis in psoriatic patients. J Dermatol 44(12):1349–1352
Lai YC, Yew YW (2016) Psoriasis and uric acid: a population-based cross-sectional study. Clin Exp Dermatol 41(3):260–266
Kuo CF, Grainge MJ, Mallen C, Zhang W, Doherty M (2016) Comorbidities in patients with gout prior to and following diagnosis: case-control study. Ann Rheum Dis 75(1):210–217
Simon D, Kleyer A, Stemmler F, Simon C, Berlin A, Hueber AJ, Haschka J, Renner N, Figueiredo C, Neuhuber W, Buder T, Englbrecht M, Rech J, Engelke K, Schett G (2017) Age- and sex-dependent changes of intra-articular cortical and trabecular bone structure and the effects of rheumatoid arthritis. J Bone Miner Res 32(4):722–730
Neogi T, Jansen TL, Dalbeth N, Fransen J, Schumacher HR, Berendsen D et al (2015) 2015 Gout Classification Criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 67(10):2557–2568
Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, Mielants H (2006) Classification criteria for psoriatic arthritis: development of new criteria from a large international study. Arthritis Rheum 54(8):2665–2673
Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 90(12):6508–6515
Burghardt AJ, Pialat JB, Kazakia GJ, Boutroy S, Engelke K, Patsch JM, Valentinitsch A, Liu D, Szabo E, Bogado CE, Zanchetta MB, McKay HA, Shane E, Boyd SK, Bouxsein ML, Chapurlat R, Khosla S, Majumdar S (2013) Multicenter precision of cortical and trabecular bone quality measures assessed by high-resolution peripheral quantitative computed tomography. J Bone Miner Res 28(3):524–536
Burghardt AJ, Buie HR, Laib A, Majumdar S, Boyd SK (2010) Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone. 47(3):519–528
Dong XW, Tian HY, He J, Wang C, Qiu R, Chen YM (2016) Elevated serum uric acid is associated with greater bone mineral density and skeletal muscle mass in middle-aged and older adults. PLoS One 11(5):e0154692
Pirro M, Mannarino MR, Bianconi V, De Vuono S, Sahebkar A, Bagaglia F et al (2017) Uric acid and bone mineral density in postmenopausal osteoporotic women: the link lies within the fat. Osteoporos Int 28(3):973–981
Veronese N, Carraro S, Bano G, Trevisan C, Solmi M, Luchini C, Manzato E, Caccialanza R, Sergi G, Nicetto D, Cereda E (2016) Hyperuricemia protects against low bone mineral density, osteoporosis and fractures: a systematic review and meta-analysis. Eur J Clin Investig 46(11):920–930
Dalbeth N, Topless R, Flynn T, Cadzow M, Bolland MJ, Merriman TR (2015) Mendelian randomization analysis to examine for a causal effect of urate on bone mineral density. J Bone Miner Res 30(6):985–991
Mehta T, Buzkova P, Sarnak MJ, Chonchol M, Cauley JA, Wallace E et al (2015) Serum urate levels and the risk of hip fractures: data from the Cardiovascular Health Study. Metabolism. 64(3):438–446
Tzeng HE, Lin CC, Wang IK, Huang PH, Tsai CH (2016) Gout increases risk of fracture: a nationwide population-based cohort study. Medicine (Baltimore) 95(34):e4669
Kim SC, Paik JM, Liu J, Curhan GC, Solomon DH (2017) Gout and the risk of non-vertebral fracture. J Bone Miner Res 32(2):230–236
Yin P, Lv H, Li Y, Meng Y, Zhang L, Tang P (2017) The association between serum uric acid level and the risk of fractures: a systematic review and meta-analysis. Osteoporos Int 28(8):2299–2307
Attia EA, Khafagy A, Abdel-Raheem S, Fathi S, Saad AA (2011) Assessment of osteoporosis in psoriasis with and without arthritis: correlation with disease severity. Int J Dermatol 50(1):30–35
Millard TP, Antoniades L, Evans AV, Smith HR, Spector TD, Barker JN (2001) Bone mineral density of patients with chronic plaque psoriasis. Clin Exp Dermatol 26(5):446–448
Nolla JM, Fiter J, Rozadilla A, Gomez-Vaquero C, Mateo L, Rodriguez-Moreno J, Roig-Escofet D (1999) Bone mineral density in patients with peripheral psoriatic arthritis. Rev Rhum Engl Ed 66(10):457–461
Acknowledgements
The authors thank T.A. Vacca at Linz/Austria for proofreading. The authors further acknowledge the work of Dragana Simic and Patricia Gumbo from the VINFORCE study group and Silke Winkler from the University of Erlangen.
Funding
This study was supported by the Austrian Society for Bone and Mineral Research (Project Award 2013), the German Research Community (Deutsche Forschungsgemeinschaft, DFG-SFB1181-A01; GS, DFG - FOR2886 PANDORA Z-project), the Federal Ministry for Education and Research (Bundesministerium für Bildung und Forschung, BMBF; project METARTHROS TP 2), and the EU IMI2 funded project RTCure, the TEAM project of the European Union, the EU IMI2 funded project PREFER, the ERC Synergy Grant 4D Nanoscope (ERC-Syg 810316 4DnanoSCOPE), the Emerging Fields Initiative MIRACLE of the Friedrich-Alexander- Universität Erlangen-Nürnberg and the Else Kröner-Memorial Scholarship (DS) of the Else Kröner-Fresenius-Stiftung.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The study was approved by the appropriate ethics committees and was conducted in accordance with the Declaration of Helsinki.
Conflicts of interest
None.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Simon, D., Haschka, J., Muschitz, C. et al. Bone microstructure and volumetric bone mineral density in patients with hyperuricemia with and without psoriasis. Osteoporos Int 31, 931–939 (2020). https://doi.org/10.1007/s00198-019-05160-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-019-05160-x