Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Article
  • Published:
Archives of Osteoporosis Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

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

References

  1. Silman AJ, Pearson JE (2002) Epidemiology and genetics of rheumatoid arthritis. Arthritis Res 4(Suppl 3):S265–S272

    Article  Google Scholar 

  2. Choy EHS, Panayi GS (2001) Cytokine pathways and joint inflammation in rheumatoid arthritis. N Engl J Med 344(12):907–916

    Article  CAS  Google Scholar 

  3. Gabriel SE (2001) The epidemiology of rheumatoid arthritis. Rheum Dis Clin N Am 27(2):269–281

    Article  CAS  Google Scholar 

  4. WHO (2016) WHO | Chronic rheumatic conditions

  5. Chopra A, Abdel-Nasser A (2008) Epidemiology of rheumatic musculoskeletal disorders in the developing world. Best Pract Res Clin Rheumatol 22(4):583–604

    Article  Google Scholar 

  6. Weyand CM, Schmidt D, Wagner U, Goronzy JJ (1998) The influence of sex on the phenotype of rheumatoid arthritis. Arthritis Rheum 41(5):817–822

    Article  CAS  Google Scholar 

  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):R7

    PubMed  PubMed Central  Google Scholar 

  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):1759–1766

    Article  CAS  Google Scholar 

  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):98

    Article  Google Scholar 

  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):447–450

    CAS  Google Scholar 

  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):522

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  13. Sapir-Koren R, Livshits G (2017) Postmenopausal osteoporosis in rheumatoid arthritis: the estrogen deficiency-immune mechanisms link. Bone 103:102–115

    Article  Google Scholar 

  14. Wasserman AM (2011) Diagnosis and management of rheumatoid arthritis. Am Fam Physician 84(11):1245–52

  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 12:50–64

    Article  Google Scholar 

  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):509–517

    Article  Google Scholar 

  17. Adams JE (2009) Quantitative computed tomography. Eur J Radiol 71(3):415–424

    Article  Google Scholar 

  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 2013:895474

    PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  20. Pi H, Zhou H, Jin H, Ning Y, Wang Y (2017) Abnormal glucose metabolism in rheumatoid arthritis. Biomed Res Int 2017:9670434

    Article  Google Scholar 

  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–S1016

    Article  Google Scholar 

  22. Pincus T, Sokka T Laboratory tests to assess patients with rheumatoid arthritis: advantages and limitations. Rheum Dis Clin N Am 35(4):731–734

    Article  Google Scholar 

  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):R75

    Article  Google Scholar 

  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):136

    Article  CAS  Google Scholar 

  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):1005–1014

    Article  Google Scholar 

  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 3:8–12

    Google Scholar 

  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):362–368

    Google Scholar 

  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):3397–3403

    Article  CAS  Google Scholar 

  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):247–253

    Article  Google Scholar 

  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):R119

    Article  Google Scholar 

  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):15–22

    Article  CAS  Google Scholar 

  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. 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 30:213–20

  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):257–263

    Article  Google Scholar 

  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 4:87–94

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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):168–161

    Article  CAS  Google Scholar 

  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):21–26

    Article  CAS  Google Scholar 

  39. Gough AK, Lilley J, Eyre S, Holder RL, Emery P (1994) Generalised bone loss in patients with early rheumatoid arthritis. Lancet 344(8914):23–27

    Article  CAS  Google Scholar 

  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 53:18–23

    Article  CAS  Google Scholar 

  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):1310–1314

    Article  CAS  Google Scholar 

Download references

Funding

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

Author information

Authors and Affiliations

  1. Department of General Medical Practice, Kazakh National Medical University, Almaty, Kazakhstan

    Gulzhan Gabdulina, Ainash Amanzholova, Maira Saparbaeva, Maira Bizhanova & Moldir Kulshymanova

  2. Human Population Biology Research Unit, Department of Anatomy and Anthropology, Sackler Faculty of Medicine, Tel Aviv University, Ramat-Aviv, Tel-Aviv, Israel

    Melody Kasher & Gregory Livshits

  3. Lilian and Marcel Pollak Chair of Biological Anthropology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv-Yafo, Israel

    Melody Kasher & Gregory Livshits

  4. City Rheumatology Center of Almaty, Almaty, Kazakhstan

    Aliya Beissebayeva, Dana Mussabaeva, Alexander Tokarev, Gulmira Mominova, Gulnar Essirkepova & Korlan Zaurbekova

Authors
  1. Gulzhan Gabdulina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Melody Kasher
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aliya Beissebayeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dana Mussabaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexander Tokarev
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gulmira Mominova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gulnar Essirkepova
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ainash Amanzholova
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Korlan Zaurbekova
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Maira Saparbaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Maira Bizhanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Moldir Kulshymanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Gregory Livshits
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gregory Livshits.

Electronic supplementary material

ESM 1

(DOCX 127 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gabdulina, G., Kasher, M., Beissebayeva, A. et al. An epidemiological analysis of osteoporotic characteristics in patients affected with rheumatoid arthritis in Kazakhstan. Arch Osteoporos 13, 99 (2018). https://doi.org/10.1007/s11657-018-0514-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11657-018-0514-9

Keywords

Search

Navigation