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Archives of Osteoporosis

, 13:99 | Cite as

An epidemiological analysis of osteoporotic characteristics in patients affected with rheumatoid arthritis in Kazakhstan

  • Gulzhan Gabdulina
  • Melody Kasher
  • Aliya Beissebayeva
  • Dana Mussabaeva
  • Alexander Tokarev
  • Gulmira Mominova
  • Gulnar Essirkepova
  • Ainash Amanzholova
  • Korlan Zaurbekova
  • Maira Saparbaeva
  • Maira Bizhanova
  • Moldir Kulshymanova
  • Gregory LivshitsEmail author
Original Article
  • 55 Downloads

Abstract

Purpose

We aimed to assess which of the major risk factors associated with rheumatoid arthritis (RA) severity are also associated with osteoporosis-related phenotypes (OP-RP) in the native population of Kazakhstan.

Methods

Four hundred six RA patients (90.6% females) with 397 controls—unaffected first-degree relatives were recruited. Biochemical factors were recorded, and OP-RP were assessed using QCT scans and ultrasound densitometry (US) of the forearm to estimate cortical indices (CI), spongial bone mineral density (BMDSPN), and US_T-scores.

Results

In the RA affected female population, ~ 80% suffered from osteopenia or osteoporosis. All OP-RP were negatively correlated with age and female’s sex, as expected, and thus accordingly adjusted, resulting in consistent, significantly [p = 0.016 (CI), p < 0.0001 (both BMDSPN and US_T-scores)] lower OP-RP estimates in affected females. Using multiple regression analysis for OP-RP manifestations, only age and disease duration appeared consistently associated with all three studied phenotypes, while menopause status or years following the onset of menopause were also significant for BMDSPN and US_T-scores. However, when disease duration was examined, we found that it was significantly dependent on morning stiffness, ESR, total cholesterol levels, weight, and menopause status, which explains 38.6% of the disease duration.

Conclusions

Approximately 80% of female RA patients suffer from osteoporosis or osteopenia in the study group, which appears from a young age. RA disease duration is the major risk factor for OP-RP deterioration, especially as assessed by BMDSPNG, and US_T-scores. As a result, all OP-RP demonstrate significantly lower levels in comparison to sex- and age-matched unaffected individuals.

Keywords

Rheumatoid arthritis Bone mineral density (BMD) Cortical index US_T-score Osteoporosis Risk factors 

Abbreviations

ACPA

Anti-citrullinated protein antibody

ALT

Alanine transaminase

AST

Aspartame transaminase

BMDSPNG

Bone mineral density of the medullar compartment of ulna

BMI

Body mass index

CI

Bone cortical index

CIUR

Averaged cortical index of ulna and radius

CRP

C-reactive protein

ESR

Erythrocyte sedimentation rate

GLU

Blood glucose levels

Hb

Hemoglobin

HDL

High density lipoprotein

HR

Heart rate

HT

Height

LDL

Low-density lipoprotein

OP-RP

Osteoporosis-related phenotypes

RA

Rheumatoid arthritis

RF

Rheumatoid factor

SB/DB

Systolic blood pressure/diastolic blood pressure

TCH

Total cholesterol

US_T-scores

Ultrasound T-criterion (US TC)

US_Z-scores

Ultrasound Z-criterion (US ZC)

WHR

Waist hip ratio

WT

Weight

Notes

Funding information

The study was supported by Kazakhstan Ministry of Education and Science (grant № 2460/ГФ4, registration number 0115РК00901)

Supplementary material

11657_2018_514_MOESM1_ESM.docx (127 kb)
ESM 1 (DOCX 127 kb)

References

  1. 1.
    Silman AJ, Pearson JE (2002) Epidemiology and genetics of rheumatoid arthritis. Arthritis Res 4(Suppl 3):S265–S272CrossRefGoogle Scholar
  2. 2.
    Choy EHS, Panayi GS (2001) Cytokine pathways and joint inflammation in rheumatoid arthritis. N Engl J Med 344(12):907–916CrossRefGoogle Scholar
  3. 3.
    Gabriel SE (2001) The epidemiology of rheumatoid arthritis. Rheum Dis Clin N Am 27(2):269–281CrossRefGoogle Scholar
  4. 4.
    WHO (2016) WHO | Chronic rheumatic conditionsGoogle Scholar
  5. 5.
    Chopra A, Abdel-Nasser A (2008) Epidemiology of rheumatic musculoskeletal disorders in the developing world. Best Pract Res Clin Rheumatol 22(4):583–604CrossRefGoogle Scholar
  6. 6.
    Weyand CM, Schmidt D, Wagner U, Goronzy JJ (1998) The influence of sex on the phenotype of rheumatoid arthritis. Arthritis Rheum 41(5):817–822CrossRefGoogle Scholar
  7. 7.
    Sokka T et al (2009) Women, men, and rheumatoid arthritis: analyses of disease activity, disease characteristics, and treatments in the QUEST-RA study. Arthritis Res Ther 11(1):R7PubMedPubMedCentralGoogle Scholar
  8. 8.
    Hauser B, Riches PL, Wilson JF, Horne AE, Ralston SH (2014) Prevalence and clinical prediction of osteoporosis in a contemporary cohort of patients with rheumatoid arthritis. Rheumatology 53(10):1759–1766CrossRefGoogle Scholar
  9. 9.
    Lee J-H et al (2016) The frequency of and risk factors for osteoporosis in Korean patients with rheumatoid arthritis. BMC Musculoskelet Disord 17(1):98CrossRefGoogle Scholar
  10. 10.
    Mobini M, Kashi Z, Ghobadifar A (2012) Prevalence and associated factors of osteoporosis in female patients with rheumatoid arthritis. Casp J Intern Med 3(3):447–450Google Scholar
  11. 11.
    Haugeberg G, Uhlig T, Falch JA, Halse JI, Kvien TK (2000) Bone mineral density and frequency of osteoporosis in female patients with rheumatoid arthritis: results from 394 patients in the Oslo County rheumatoid arthritis register. Arthritis Rheum 43(3):522CrossRefGoogle Scholar
  12. 12.
    Jin S et al (2018) Incidence of fractures among patients with rheumatoid arthritis: a systematic review and meta-analysis. Osteoporos Int 29:1263.  https://doi.org/10.1007/s00198-018-4473-1
  13. 13.
    Sapir-Koren R, Livshits G (2017) Postmenopausal osteoporosis in rheumatoid arthritis: the estrogen deficiency-immune mechanisms link. Bone 103:102–115CrossRefGoogle Scholar
  14. 14.
    Wasserman AM (2011) Diagnosis and management of rheumatoid arthritis. Am Fam Physician 84(11):1245–52Google Scholar
  15. 15.
    Abdulameer SA, Sahib MN, Sulaiman SAS (2018) The Prevalence of osteopenia and osteoporosis among Malaysian type 2 diabetic patients using quantitative ultrasound densitometer. Open Rheumatol J 12:50–64CrossRefGoogle Scholar
  16. 16.
    Blake GM, Fogelman I (2007) The role of DXA bone density scans in the diagnosis and treatment of osteoporosis. Postgrad Med J 83(982):509–517CrossRefGoogle Scholar
  17. 17.
    Adams JE (2009) Quantitative computed tomography. Eur J Radiol 71(3):415–424CrossRefGoogle Scholar
  18. 18.
    Li N, Li X-M, Xu L, Sun W-J, Cheng X-G, Tian W (2013) Comparison of QCT and DXA: osteoporosis detection rates in postmenopausal women. Int J Endocrinol 2013:895474PubMedPubMedCentralGoogle Scholar
  19. 19.
    Sokka T, Pincus T (2009) Erythrocyte sedimentation rate, C-reactive protein, or rheumatoid factor are normal at presentation in 35%–45% of patients with rheumatoid arthritis seen between 1980 and 2004: analyses from Finland and the United States. J Rheumatol 36(7):1387–1390.  https://doi.org/10.3899/jrheum.080770 CrossRefPubMedGoogle Scholar
  20. 20.
    Pi H, Zhou H, Jin H, Ning Y, Wang Y (2017) Abnormal glucose metabolism in rheumatoid arthritis. Biomed Res Int 2017:9670434CrossRefGoogle Scholar
  21. 21.
    Rajput R, Dangi A, Singh H (2017) Prevalence of glucose intolerance in rheumatoid arthritis patients at a tertiary care centre in Haryana. Diabetes Metab Syndr Clin Res Rev 11:S1013–S1016CrossRefGoogle Scholar
  22. 22.
    Pincus T, Sokka T Laboratory tests to assess patients with rheumatoid arthritis: advantages and limitations. Rheum Dis Clin N Am 35(4):731–734Google Scholar
  23. 23.
    Ursum J, Bos WH, van de Stadt RJ, Dijkmans BAC, van Schaardenburg D (2009) Different properties of ACPA and IgM-RF derived from a large dataset: further evidence of two distinct autoantibody systems. Arthritis Res Ther 11(3):R75CrossRefGoogle Scholar
  24. 24.
    Hernlund E et al (2013) Osteoporosis in the European Union: medical management, epidemiology and economic burden. A report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch Osteoporos 8(1–2):136CrossRefGoogle Scholar
  25. 25.
    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
  26. 26.
    Moula K, Esfehani A (2002) A study of the bone density of rheumatoid arthritis patients in khoozestan province. J Shaheed Sadoughi Univ Med Sci 3:8–12Google Scholar
  27. 27.
    Piotr Leszczyński SM, Hrycaj P (2007) Osteoporoza u chorych na reumatoidalne zapalenie stawów – realny problem czy fikcja? Ocena występowania złamań trzonów kręgowych u kobiet z reumatoidalnym zapaleniem stawów w wieku do 50 lat. Reumatologia/Rheumatology 45(6):362–368Google Scholar
  28. 28.
    Xu S, Wang Y, Lu J, Xu J (2012) Osteoprotegerin and RANKL in the pathogenesis of rheumatoid arthritis-induced osteoporosis. Rheumatol Int 32(11):3397–3403CrossRefGoogle Scholar
  29. 29.
    Gonzalez-Lopez L et al (2012) Performance of risk indices for identifying low bone mineral density and osteoporosis in Mexican Mestizo women with rheumatoid arthritis. J Rheumatol 39(2):247–253CrossRefGoogle Scholar
  30. 30.
    Aeberli D et al (2010) Reduced trabecular bone mineral density and cortical thickness accompanied by increased outer bone circumference in metacarpal bone of rheumatoid arthritis patients: a cross-sectional study. Arthritis Res Ther 12(3):R119CrossRefGoogle Scholar
  31. 31.
    Jensen T et al (2004) Bone loss in unclassified polyarthritis and early rheumatoid arthritis is better detected by digital x ray radiogrammetry than dual x ray absorptiometry: relationship with disease activity and radiographic outcome. Ann Rheum Dis 63(1):15–22CrossRefGoogle Scholar
  32. 32.
    Eser P, Aeberli D, Widmer J, Ller BM, Villiger PM Abnormal bone geometry at the metacarpal bone shaft of rheumatoid arthritis patients with maintained muscle–bone relationship. Arthritis Care Res 63:383–389.  https://doi.org/10.1002/acr.20394
  33. 33.
    Keller C, Hafström I, Svensson B (2001) Scandinavian Journal of Rheumatology Bone mineral density in women and men with early rheumatoid arthritis. Ingia Èld Hafstro Èm 2 , and Bjo Èrn Svensson 1 for the BARFOT study group #. Scand J Rheumatol 30:213–20Google Scholar
  34. 34.
    Lane NE, Pressman AR, Star VL, Cummings SR, Nevitt MC (Dec. 2009) Rheumatoid arthritis and bone mineral density in elderly women. J Bone Miner Res 10(2):257–263CrossRefGoogle Scholar
  35. 35.
    Hafez EA, Mansour HE, Hamza SH, Moftah SG, Younes TB, Ismail MA (2011) Bone mineral density changes in patients with recent-onset rheumatoid arthritis. Clin Med Insights Arthritis Musculoskelet Disord 4:87–94CrossRefGoogle Scholar
  36. 36.
    Wafa H, Raja A, Dhia K, Nada B, Imene Z, Montacer KM (2018) Risk factors associated with bone loss and occurrence of fragility fractures in rheumatoid arthritis patients. Egypt Rheumatol.  https://doi.org/10.1016/j.ejr.2018.01.004
  37. 37.
    Karlsson MK, Gardsell P, Johnell O, Nilsson E, Akesson K, Obrant KJ (1993) Bone mineral normative data in Malmo, Sweden comparison with reference data and hip fracture incidence in other ethnic groups. Acta Orthop Scand 64(2):168–161CrossRefGoogle Scholar
  38. 38.
    Laan RF et al (1993) Bone mineral density in patients with recent onset rheumatoid arthritis: influence of disease activity and functional capacity. Ann Rheum Dis 52(52):21–26CrossRefGoogle Scholar
  39. 39.
    Gough AK, Lilley J, Eyre S, Holder RL, Emery P (1994) Generalised bone loss in patients with early rheumatoid arthritis. Lancet 344(8914):23–27CrossRefGoogle Scholar
  40. 40.
    Kroger H, Honkanen R, Saarikoski S, Alhava E (1994) Decreased axial bone mineral density in perimenopausal women with rheumatoid arthritis-a population based study. Ann Rheum Dis 53:18–23CrossRefGoogle Scholar
  41. 41.
    Myasoedova E, Crowson CS, Kremers HM, Fitz-Gibbon PD, Therneau TM, Gabriel SE (2010) Total cholesterol and LDL levels decrease before rheumatoid arthritis. Ann Rheum Dis 69(7):1310–1314CrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Authors and Affiliations

  • Gulzhan Gabdulina
    • 1
  • Melody Kasher
    • 2
    • 3
  • Aliya Beissebayeva
    • 4
  • Dana Mussabaeva
    • 4
  • Alexander Tokarev
    • 4
  • Gulmira Mominova
    • 4
  • Gulnar Essirkepova
    • 4
  • Ainash Amanzholova
    • 1
  • Korlan Zaurbekova
    • 4
  • Maira Saparbaeva
    • 1
  • Maira Bizhanova
    • 1
  • Moldir Kulshymanova
    • 1
  • Gregory Livshits
    • 2
    • 3
    Email author
  1. 1.Department of General Medical PracticeKazakh National Medical UniversityAlmatyKazakhstan
  2. 2.Human Population Biology Research Unit, Department of Anatomy and Anthropology, Sackler Faculty of MedicineTel Aviv UniversityTel-AvivIsrael
  3. 3.Lilian and Marcel Pollak Chair of Biological Anthropology, Sackler Faculty of MedicineTel Aviv UniversityTel Aviv-YafoIsrael
  4. 4.City Rheumatology Center of AlmatyAlmatyKazakhstan

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