Abstract
Our aim was to appraise publications from Bulgaria, to assess their global impact, and to describe features and challenges unique to the rheumatology practice in Bulgaria characterized by stringent cost constraints. The Scopus database was queried on 25th July 2018 and data on the number of published documents, their Hirsch-indices and citations number were extracted. Published Bulgarian guidelines for the management of rheumatic diseases and the presented data on Bulgarian Rheumatology Society were identified based on prior knowledge of the authors. From all the identified 1082 document the most extensively researched areas were rheumatoid arthritis (RA), systemic lupus erythematosus (SLE), osteoporosis, and osteoarthritis (OA). For the last five years (from Jan 2013 to 25th July 2018) the number of publications was 293. We found that Bulgaria’s international scientific collaboration in the field of rheumatology is focused on a handful of countries mainly from Europe. Although Bulgarian rheumatologists have access to costly biologic agents for treating their patients with rheumatic diseases, their funding may not be granted according to the current recommendations of European League against Rheumatism (EULAR) and national guidelines for the management of rheumatic diseases. Although the western world clearly dominates the production of scientific publications in rheumatology, Bulgarian rheumatology may present another perspective for diagnosis and management of patients with rheumatic diseases in a cost-stringent environment. Nevertheless, both rheumatology science and practice in Bulgaria still have a long way to go to take its deserved place among the other European countries.
Similar content being viewed by others
Abbreviations
- AAV:
-
ANCA-associated vasculitis
- ACR:
-
American College of Rheumatology
- ANCA:
-
Anti-neutrophil cytoplasmic antibody
- BRS:
-
Bulgarian Rheumatology Society
- BS:
-
Behçet’s syndrome
- CHCC:
-
Chapel Hill Consensus Conference
- COMP:
-
Cartilage oligomeric matrix protein
- csDMARDs:
-
Conventional synthetic disease modifying anti-rheumatic drugs
- DM:
-
Dermatomyositis
- DMARDs:
-
Disease modifying anti-rheumatic drugs
- EMA:
-
European Medicine Agency
- EULAR:
-
European league against rheumatism
- FDA:
-
Food and Drug Administration
- GCA:
-
Giant cell arteritis
- h:
-
Hirsch
- IIMs:
-
Inflammatory idiopathic myopathies
- LVV:
-
Large vessel vasculitis
- MMP-3:
-
Matrix metalloproteinase 3
- MPO:
-
Myeloperoxidase
- MSK:
-
Musculoskeletal
- NCPHA:
-
National Center of Public Health and Analyses
- NHIF:
-
National Health Insurance Fund
- nrAxSpA:
-
Non-radiographic axial spondyloarthritis
- OA:
-
Osteoarthritis
- PM:
-
Polymyositis
- PR3:
-
Proteinase 3
- RA:
-
Rheumatoid arthritis
- RNA:
-
Ribonucleic acid
- SLE:
-
Systemic lupus erythematosus
- SS:
-
Sjogren’s syndrome
- SSc:
-
Systemic sclerosis
- TA:
-
Takayasu arteritis
- tsDMARDS:
-
Targeted synthetic disease modifying anti-rheumatic drugs
- USA:
-
United States of America
References
Sinigaglia L (2014) Metabolic bone diseases: an overview. Reumatismo 66(2):109–111. https://doi.org/10.4081/reumatismo.2014.783
Mikuls TR et al (2013) Rheumatology: a color handbook. CRC Press, Boca Raton
Chopra A, Abdel-Nasser A (2008) Epidemiology of rheumatic musculoskeletal disorders in the developing world. Best Pract Res Clin Rheumatol 22(4):583–604. https://doi.org/10.1016/j.berh.2008.07.001
Orlewska E, Ancuta I, Anic B, Codrenau C, Damjanov N, Djukic P, Ionescu R, Marinchev L, Nasonov EL, Peets T, Praprotnik S (2011) Access to biologic treatment for rheumatoid arthritis in Central and Eastern European (CEE) countries. Med Sci Monit 17(4):SR1
National Center of Public Health and Analyses of Bulgaria (2018) Hospitalized patients (discharged and deceased) in hospitals by classes of ICD-10 in 2016 (Internet). http://ncpha.government.bg/files/nczi/zdr.statistika/health_BB_6.pdf. Accessed 25 July 2018
Kolarov Z, Monov S (2014) Development of Rheumatology in Bulgaria. In: History of rheumatology in Bulgaria [Развитие на ревматологията в България. В: История на ревматологията в България]. Central Medical Library of Medical University-Sofia, Sofia, pp 13–17
Atanasova E, Pavlova M, Velickovski R, Nikov B, Moutafova E, Groot W (2011) What have 10 years of health insurance reforms brought about in Bulgaria? Re-appraising the Health Insurance Act of 1998. Health Policy 102(2–3):263–269
Cheng T, Guoyou Z (2013) Worldwide research productivity in the field of rheumatology from 1996 to 2010: a bibliometric analysis. Rheumatology 52(9):1630–1634. https://doi.org/10.1093/rheumatology/ket008
Gasparyan AY, Ayvazyan L, Blackmore H, Kitas GD (2011) Writing a narrative biomedical review: considerations for authors, peer reviewers, and editors. Rheumatol Int 31(11):1409. https://doi.org/10.1007/s00296-011-1999-3
Woywodt A, Matteson EL (2007) Head to head: should eponyms be abandoned? Yes. BMJ 335(7617):424. https://doi.org/10.1136/bmj.39308.342639.AD
Matteson EL, Woywodt A (2006) Eponymophilia in rheumatology. Rheumatology 45(11):1328–1330. https://doi.org/10.1093/rheumatology/kel259
Abubakar II, Tillmann T, Banerjee A (2015) Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 385(9963):117–171
Emery P (2011) Pocket reference to early rheumatoid arthritis. Springer, Berlin
Kobelt G, Kasteng F (2009) Access to innovative treatments in rheumatoid arthritis in Europe. A report prepared for the European Federation of Pharmaceutical Industry Associations (EFPIA) (Internet). http://www.comparatorreports.se/Access%20to%20RA%20Treatments%20October%202009.pdf. Accessed 14 Oct 2018
Solakov P, Khristova M (1977) Rheumatoid arthritis among the rural population of southern Bulgaria (transitory morbidity established using the Rome and New York diagnostic criteria). Vutreshni Boles 16(3):52–56
Aletaha D et al (2010) 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 62(9):2569–2581
Verschueren P, De Cock D, Corluy L et al (2015) Methotrexate in combination with other DMARDs is not superior to methotrexate alone for remission induction with moderate-to-high-dose glucocorticoid bridging in early rheumatoid arthritis after 16 weeks of treatment: the CareRA trial. Ann Rheum Dis 74:27–34. https://doi.org/10.1136/annrheumdis-2014-205489
O’Dell JR, Mikuls TR, Taylor TH et al (2013) Therapies for active rheumatoid arthritis after methotrexate failure. N Engl J Med 369:307–318. https://doi.org/10.1056/NEJMoa1303006
Smolen JS, Landewé R, Bijlsma J, Burmester G, Chatzidionysiou K, Dougados M, Nam J, Ramiro S, Voshaar M, van Vollenhoven R, Aletaha D (2017) EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2016 update. Ann Rheum Dis 76(6):960–977
Bulgarian Rheumatology Society (2018) National consensus for the treatment of rheumatoid arthritis with biologic agents [Национален консенсус за лечение на ревматоиден артрит с биологични средства] (Internet). http://rheumatologybg.org/download/consensus_3.doc. Accessed 14 Oct 2018
NHIF requirements for the treatment of seropositive rheumatoid and psoriatic arthritis with disease-modifying antirheumatic drugs (DMARDs) in outpatient care [Изисквания на НЗОК при лечение на серопозитивен ревматоиден и псориатичен артрит с болест-модифициращи антиревматични лекарства (БМАРЛ) в извънболничната помощ] (Internet). https://www.nhif.bg/get_file?uuid=79d71f42-0189-4232-af78-97e0f2fd0dbb. Accessed 14 Oct 2018
NHIF requirements for treatment of moderate to severe active seropositive rheumatoid arthritis, active juvenile arthritis, active and progressive psoriatic arthritis and severe active ankylosing spondylitis with disease-modifying antirheumatic drugs over 18 years of age in outpatient care [Изисквания на НЗОК при лечение на умерен до тежък активен серопозитивен ревматоиден артрит, активен ювенилен артрит, активен и прогресиращ псориатичен артрит и тежък активен анкилозиращ спондилит с антиревматични лекарствени продукти над 18 годишна възраст в извънболничната помощ] (Internet). https://www.nhif.bg/get_file?uuid=74d9c325-9d5c-4494-bc53-68ddc9ccc955. Accessed 14 Oct 2018
Dougados M, Baeten D (2011) Spondyloarthritis. Lancet 377:2127–2137
Stolwijk C, van Tubergen A, Castillo-Ortiz JD et al (2015) Prevalence of extra-articular manifestations in patients with ankylosing spondylitis: a systematic review and meta-analysis. Ann Rheum Dis 74(1):65–73. https://doi.org/10.1136/annrheumdis-2013-203582
van der Heijde D, Ramiro S, Landewé R, Baraliakos X, Van den Bosch F, Sepriano A, Regel A, Ciurea A, Dagfinrud H, Dougados M, van Gaalen F (2017) 2016 update of the ASAS-EULAR management recommendations for axial spondyloarthritis. Annals of the rheumatic diseases. 2016 update of the ASAS-EULAR management recommendations for axial spondyloarthritis. Ann Rheum Dis 76:978–991. https://doi.org/10.1136/annrheumdis-2016-210770
van der Linden S, Valkenburg HA, Cats A (1984) Evaluation of diagnostic criteria for ankylosing spondylitis. Arthritis Rheum 27(4):361–368
Rudwaleit M, Landewé R, Van der Heijde D, Listing J, Brandt J, Braun JV, Burgos-Vargas R, Collantes-Estevez E, Davis J, Dijkmans B, Dougados M (2009) The development of Assessment of SpondyloArthritis International Society classification criteria for axial spondyloarthritis (part I): classification of paper patients by expert opinion including uncertainty appraisal. Ann Rheum Dis 68(6):770–776
Rudwaleit MV, Van Der Heijde D, Landewé R, Akkoc N, Brandt J, Chou CT, Dougados M, Huang F, Gu J, Kirazli Y, Van den Bosch F (2011) The Assessment of SpondyloArthritis International Society classification criteria for peripheral spondyloarthritis and for spondyloarthritis in general. Ann Rheum Dis 70(1):25–31
Ivanova M, Manolova I, Goycheva P, Stoilov R (2014) Serum cytokines (TNF-alpha and IL-18) in ankylosing spondylitis in relation to disease activity. C R l‘Académie Bulg Sci 67(4):593–606
Smolen JS, Schöls M, Braun J, Dougados M, FitzGerald O, Gladman DD, Kavanaugh A, Landewé R, Mease P, Sieper J, Stamm T (2018) Treating axial spondyloarthritis and peripheral spondyloarthritis, especially psoriatic arthritis, to target: 2017 update of recommendations by an international task force. Ann Rheum Dis 77(1):3–17
Bulgarian Rheumatology Society (2018) Consensus for the treatment of psoriatic arthritis [Консенсус за лечение на псориатичен артрит] (Internet). http://rheumatologybg.org/download/consensus_2.doc. Accessed 14 Oct 2018
Bulgarian Rheumatology Society (2018) Consensus for the treatment of axial spondyloarthritis [Консенсус за лечение на аксиален спондилоартрит] (Internet). http://rheumatologybg.org/download/consensus_1.doc. Accessed 14 Oct 2018
Baraliakos X, Braun J (2015) Non-radiographic axial spondyloarthritis and ankylosing spondylitis: what are the similarities and differences? RMD Open 1(Suppl 1):e000053. https://doi.org/10.1136/rmdopen-2015-000053
McAlindon TE, Cooper C, Kirwan JR, Dieppe PA (1992) Knee pain and disability in the community. Br J Rheumatol 31:189–192
Nuesch E, Dieppe P, Reichenbach S et al (2011) All cause and disease specific mortality in patients with knee or hip osteoarthritis: population based cohort study. BMJ 342:d1165
Felson DT, Lawrence RC, Dieppe PA et al (2000) Osteoarthritis: new insights. Part 1: the disease and its risk factors. Ann Intern Med 133(8):635–646
Kellgren JH, Lawrence JS (1957) Radiological assessment of osteo-arthrosis. Ann Rheum Dis 16:494–502
Georgiev T, Stoilov R, Penkov M, Ivanova M, Trifonov A (2016) Radiographic assessment of knee osteoarthritis. Revmatologiia (Bulgaria) 24(2):16–24
Sakellariou G, Conaghan PG, Zhang W et al (2017) EULAR recommendations for the use of imaging in the clinical management of peripheral joint osteoarthritis. Ann Rheum Dis 76:1484–1494. https://doi.org/10.1136/annrheumdis-2016-210815
Kraus VB, Burnett B, Coindreau J et al (2011) Application of biomarkers in the development of drugs intended for the treatment of osteoarthritis. Osteoarthritis Cartil 19(5):515–542
Georgiev T, Ivanova M, Kopchev A, Velikova T, Miloshov A, Kurteva E, Yuzeir K, Penkov M, Kabakchieva P, Rashkov R, Stoilov R (2018) Cartilage oligomeric protein, matrix metalloproteinase-3, and Coll2-1 as serum biomarkers in knee osteoarthritis: a cross-sectional study. Rheumatol Int 38(5):821–830
Simon TM, Jackson DW (2018) Articular cartilage: injury pathways and treatment options. Sports Med Arthrosc Rev 26(1):31–39
Bulgarian Rheumatology Society (2018) Consensus for the diagnosis and treatment of osteoarthritis [Консенсус за диагноза и лечение на артрозната болест] (Internet). http://rheumatologybg.org/download/consensus_4.pdf. Accessed 14 Oct 2018
Cong Y, Gershwin EM, Chang C (2014) Diagnostic criteria for systemic lupus erythematosus: a critical review. J Autoimmun 48:10–13. https://doi.org/10.1016/j.jaut.2014.01.004
Miteva LD, Manolova IM, Ivanova MG, Rashkov RK, Stoilov RM, Gulubova MV, Stanilova SA (2012) Functional genetic polymorphisms in interleukin-12B gene in association with systemic lupus erythematosus. Rheumatol Int 32(1):53–59
Petri M, Orbai AM, Alarcón GS, Gordon C, Merrill JT, Fortin PR, Bruce IN, Isenberg D, Wallace DJ, Nived O, Sturfelt G (2012) Derivation and validation of the systemic lupus international collaborating clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum 64(8):2677–2686. https://doi.org/10.1002/art.34473
Tedeschi SK, Johnson SR, Boumpas D, Daikh D, Dörner T, Jayne D, Kamen D, Lerstrøm K, Mosca M, Ramsey-Goldman R, Sinnette C (2018) Developing and refining new candidate criteria for systemic lupus erythematosus classification: an international collaboration. Arthritis Care Res 70(4):571–581. https://doi.org/10.1002/acr.23317
Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40(9):1725–1725
Fonseca AR, Gaspar-Elsas MI, Land MG, de Oliveira SK (2015) Comparison between three systems of classification criteria in juvenile systemic lupus erythematous. Rheumatology 54:241–247
Bertsias GK, Tektonidou M, Amoura Z et al (2012) Joint European League Against Rheumatism and European Renal Association–European Dialysis and Transplant Association (EULAR/ERA-EDTA) recommendations for the management of adult and paediatric lupus nephritis. Ann Rheum Dis 71:1771–1782. https://doi.org/10.1136/annrheumdis-2012-201940
Bertsias GK, Ioannidis JPA, Aringer M et al (2010) EULAR recommendations for the management of systemic lupus erythematosus with neuropsychiatric manifestations: report of a task force of the EULAR standing committee for clinical affairs. Ann Rheum Dis 69:2074–2082. https://doi.org/10.1136/ard.2010.130476
Bertsias G, Ioannidis JPA, Boletis J et al (2008) EULAR recommendations for the management of systemic lupus erythematosus. Report of a task force of the EULAR Standing Committee for International Clinical Studies including therapeutics. Ann Rheum Dis 67:195–205. https://doi.org/10.1136/ard.2007.070367
Muller S, Monneaux F, Schall N, Rashkov RK, Oparanov BA, Wiesel P, Geiger J, Zimmer R (2008) Spliceosomal peptide P140 for immunotherapy of systemic lupus erythematosus: results of an early phase II clinical trial. Arthritis Rheum 58:3873–3883. https://doi.org/10.1002/art.24027
Merrill JT, Neuwelt CM, Wallace DJ, Shanahan JC, Latinis KM, Oates JC, Utset TO, Gordon C, Isenberg DA, Hsieh HJ, Zhang D (2010) Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: The randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial. Arthritis Rheum 62:222–233. https://doi.org/10.1002/art.27233
Clowse ME, Wallace DJ, Furie RA, Petri MA, Pike MC, Leszczyński P, Neuwelt CM, Hobbs K, Keiserman M, Duca L, Kalunian KC et al (2017) Efficacy and safety of epratuzumab in moderately to severely active systemic lupus erythematosus: results from two phase III randomized, double-blind, placebo-controlled trials. Arthritis Rheumatol 69(2):362–375
Mavragani CP, Nezos A, Moutsopoulos HM (2013) New advances in the classification, pathogenesis and treatment of Sjogren’s syndrome. Curr Opin Rheumatol 25(5):623–629
Tincani A, Andreoli L, Cavazzana I, Doria A, Favero M, Fenini MG et al (2013) Novel aspects of Sjögren’s syndrome in 2012. BMC Med 11:93
Vivino FB, Carsons SE, Foulks G, Daniels TE, Parke A, Brennan MT, Forstot SL, Scofield RH, Hammitt KM (2016) New treatment guidelines for Sjögren’s disease. Rheum Dis Clin 42(3):531–551
Bolster MB, Silver RM (2015) Clinical features of systemic sclerosis. In: Hochberg MC, Silman AJ, Smolen JS et al (eds) Rheumatology, 6th edn. Mosby, St. Louis, pp 1165–1176
Wei J, Bhattacharyya S, Tourtellotte WG et al (2011) Fibrosis in systemic sclerosis: emerging concepts and implications for targeted therapy. Autoimmun Rev 10(5):267–275
Rocco VK, Hurd ER (1986) Scleroderma and scleroderma-like syndromes. Semin Arthritis Rheum 16:22
Chifflot H, Fautrel B, Sordet C, Chatelus E, Sibilia J. Incidence and prevalence of systemic sclerosis: a systematic literature review. In: Seminars in arthritis and rheumatism, 1 Feb 2008 (vol 37, No. 4, pp. 223–235). WB Saunders, Philadelphia
Van Den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A, Matucci-Cerinic M, Naden RP, Medsger TA Jr, Carreira PE, Riemekasten G (2013) 2013 classification criteria for systemic sclerosis: an American College of Rheumatology/European League against Rheumatism collaborative initiative. Arthritis Rheum 65(11):2737–2747
Krasimirova E, Velikova T, Tumangelova-Yuzeir K, Ivanova-Todorova E, Kyurkchiev D, Kalinova D, Reshkova V, Kopchev A, Rashkov R (2016) A wide immunological profile in the diagnosis of progressive systemic sclerosis. Revmatologiia (Bulgaria) 24(2):35–51
Allanore Y, Matucci-Cerinic M, Distler O (2016) Treatment of systemic sclerosis: is there any hope for the future? RMD Open 2:e000260. https://doi.org/10.1136/rmdopen-2016-000260
Kowal-Bielecka O, Fransen J, Avouac J et al (2017) Update of EULAR recommendations for the treatment of systemic sclerosis. Ann Rheum Dis 76:1327–1339
Dalakas MC (1991) Polymyositis, dermatomyositis, and inclusion-body myositis. N Engl J Med 325(21):1487–1498. https://doi.org/10.1056/NEJM199111213252107
Dalakas MC, Hohlfeld R (2003) Polymyositis and dematomyositis. Lancet 362(9388):971–982. https://doi.org/10.1016/S0140-6736(03)14368-1
Kalinova D, Kopchev A, Nikolaeva S, Rashkov R (2016) Autoimmune myositis—histological features in the skin and muscle biopsies. Revmatologiia (Bulgaria) 24(4):28–34
Dourmishev LA, Guleva DV, Miteva LG (2018) Intravenous immunoglobulins for treatment of connective tissue diseases in dermatology. Wien Med Wochenschr 168:213. https://doi.org/10.1007/s10354-017-0595-x
Jennette J, Falk R, Bacon P, Basu N, Cid MC, Ferrario F et al (2013) 2012 revised International Chapel Hill consensus conference nomenclature of vasculitides. Arthritis Rheum 65:1–11
Arend WP, Michel BA, Bloch DA, Hunder GG, Calabrese LH, Edworthy SM et al (1990) The American College of Rheumatology 1990 criteria for the classification of Takayasu arteritis. Arthritis Rheum 33:1129–1134
Hunder GG, Bloch DA, Michel BA, Stevens MB, Arend WP, Calabrese LH et al (1990) The American College of Rheumatology 1990 criteria for the classification of giant cell arteritis. Arthritis Rheum 33:1122–1128
Dourmishev AL, Serafimova DK, Vassileva SG, Dourmishev LA, Schwartz RA (2005) Segmental ulcerative vasculitis: a cutaneous manifestation of Takayasu’s arteritis. Int Wound J 2(4):340–345
Petrov IS et al (2018) Late outcomes after interventional treatment—successful stenting of Takayasu arteritis lesions. Single center experience in Bulgaria. Cor Vasa 60(2):e114–e121
European Medicines Agency-Find medicine-RoActemra (Internet). http://www.ema.europa.eu/ema/index.jsp?curl=pages/medicines/human/medicines/000955/human_med_001042.jsp&mid=WC0b01ac058001d124. Accessed 25 July 2018
US Food and Drug Administration (2017) FDA approves first drug to specifically treat giant cell arteritis (Internet). https://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm559791.htm. Accessed 25 July 2018
Hatemi G, Christensen R, Bang D et al (2018) 2018 update of the EULAR recommendations for the management of Behçet’s syndrome. Ann Rheum Dis. https://doi.org/10.1136/annrheumdis-2018-213225
Leonardo NM, McNeil J (2015) Behçet’s disease: is there geographical variation? A review far from the Silk Road. Int J Rheumatol. https://doi.org/10.1155/2015/945262
Yoneva T, Rashkov R, Zdravkova Y (2015) Clinical and immunological analysis of the patients with ANCA associated vasculitides in the rheumatology clinic. Revmatologiia (Bulgaria) 23(4):31–47
Funding
No funding was received for this study.
Author information
Authors and Affiliations
Contributions
Both TG and RS took part in the conception and design of the study, data management, analysis, and logical interpretation. TG drafted the article, while RS revised it critically for important intellectual content. Both authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
Tsvetoslav Georgiev declares that he has no conflict of interest. Rumen Stoilov declares that he has no conflict of interest.
Rights and permissions
About this article
Cite this article
Georgiev, T., Stoilov, R. Bulgarian rheumatology: science and practice in a cost-constrained environment. Rheumatol Int 39, 417–429 (2019). https://doi.org/10.1007/s00296-018-4202-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00296-018-4202-2