Advertisement

Bone microstructure and volumetric bone mineral density in patients with hyperuricemia with and without psoriasis

  • D. Simon
  • J. Haschka
  • C. Muschitz
  • A. Kocijan
  • A. Baierl
  • A. Kleyer
  • G. Schett
  • S. Kapiotis
  • H. Resch
  • M. Sticherling
  • J. Rech
  • R. KocijanEmail author
Original Article
  • 46 Downloads

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.

Keywords

HR-pQCT Psoriasis Hyperuricemia Bone Mineral Density 

Notes

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 information

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.

Compliance with ethical standards

The study was approved by the appropriate ethics committees and was conducted in accordance with the Declaration of Helsinki.

Conflicts of interest

None.

References

  1. 1.
    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):3136–3141CrossRefGoogle Scholar
  2. 2.
    Feig DI, Kang DH, Johnson RJ (2008) Uric acid and cardiovascular risk. N Engl J Med 359(17):1811–1821CrossRefGoogle Scholar
  3. 3.
    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):27–35CrossRefGoogle Scholar
  4. 4.
    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):135CrossRefGoogle Scholar
  5. 5.
    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):2961–2970CrossRefGoogle Scholar
  6. 6.
    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):955–964CrossRefGoogle Scholar
  7. 7.
    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):1837–1844CrossRefGoogle Scholar
  8. 8.
    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):1701–1707CrossRefGoogle Scholar
  9. 9.
    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):1005–1014CrossRefGoogle Scholar
  10. 10.
    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):1775–1783CrossRefGoogle Scholar
  11. 11.
    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):660–666CrossRefGoogle Scholar
  12. 12.
    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):854–860CrossRefGoogle Scholar
  13. 13.
    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):2068–2074CrossRefGoogle Scholar
  14. 14.
    Gisondi P, Targher G, Cagalli A, Girolomoni G (2014) Hyperuricemia in patients with chronic plaque psoriasis. J Am Acad Dermatol 70(1):127–130CrossRefGoogle Scholar
  15. 15.
    AlJohani R, Polachek A, Ye JY, Chandran V, Gladman DD (2017) Characteristic and outcome of psoriatic arthritis patients with hyperuricemia. J RheumatolGoogle Scholar
  16. 16.
    Goldman M (1981) Uric acid in the etiology of psoriasis. Am J Dermatopathol 3(4):397–404CrossRefGoogle Scholar
  17. 17.
    Tsuruta N, Imafuku S, Narisawa Y (2017) Hyperuricemia is an independent risk factor for psoriatic arthritis in psoriatic patients. J Dermatol 44(12):1349–1352CrossRefGoogle Scholar
  18. 18.
    Lai YC, Yew YW (2016) Psoriasis and uric acid: a population-based cross-sectional study. Clin Exp Dermatol 41(3):260–266CrossRefGoogle Scholar
  19. 19.
    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):210–217CrossRefGoogle Scholar
  20. 20.
    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):722–730CrossRefGoogle Scholar
  21. 21.
    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):2557–2568CrossRefGoogle Scholar
  22. 22.
    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):2665–2673CrossRefGoogle Scholar
  23. 23.
    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):6508–6515CrossRefGoogle Scholar
  24. 24.
    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):524–536CrossRefGoogle Scholar
  25. 25.
    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):519–528CrossRefGoogle Scholar
  26. 26.
    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):e0154692CrossRefGoogle Scholar
  27. 27.
    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):973–981CrossRefGoogle Scholar
  28. 28.
    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):920–930CrossRefGoogle Scholar
  29. 29.
    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):985–991CrossRefGoogle Scholar
  30. 30.
    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):438–446CrossRefGoogle Scholar
  31. 31.
    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):e4669CrossRefGoogle Scholar
  32. 32.
    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):230–236CrossRefGoogle Scholar
  33. 33.
    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):2299–2307CrossRefGoogle Scholar
  34. 34.
    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):30–35CrossRefGoogle Scholar
  35. 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):446–448CrossRefGoogle Scholar
  36. 36.
    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):457–461PubMedGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2020

Authors and Affiliations

  • D. Simon
    • 1
  • J. Haschka
    • 2
    • 3
  • C. Muschitz
    • 2
  • A. Kocijan
    • 4
  • A. Baierl
    • 5
  • A. Kleyer
    • 1
  • G. Schett
    • 1
  • S. Kapiotis
    • 6
  • H. Resch
    • 2
    • 3
    • 7
  • M. Sticherling
    • 8
  • J. Rech
    • 1
  • R. Kocijan
    • 2
    • 3
    Email author
  1. 1.Department of Internal Medicine 3 - Rheumatology and ImmunologyFriedrich-Alexander University (FAU) Erlangen-Nürnberg and Universitätsklinikum ErlangenErlangenGermany
  2. 2.St. Vincent Hospital Vienna, Medical Department IIAcademic Teaching Hospital of the Medical University ViennaViennaAustria
  3. 3.Karl Landsteiner Institute for Rheumatology and GastroenterologyViennaAustria
  4. 4.Optimal Essen e.UViennaAustria
  5. 5.Department of Statistics and Operations ResearchUniversity of ViennaViennaAustria
  6. 6.Central LaboratorySt. Vincent GroupViennaAustria
  7. 7.Medical Faculty of Bone DiseasesSigmund Freud University ViennaViennaAustria
  8. 8.Department of DermatologyFriedrich-Alexander University (FAU) Erlangen-Nürnberg and Universitätsklinikum ErlangenErlangenGermany

Personalised recommendations