Skip to main content

Advertisement

SpringerLink
Log in

Diagnostic/classification criteria in pediatric Behçet’s disease

  • Review
  • Published:
Rheumatology International Aims and scope Submit manuscript

Abstract

Behçet’s disease (BD) is a variable vessel vasculitis characterized by recurrent oral and genital aphthosis accompanied by skin, ocular, gastrointestinal, neurologic, and articular involvement. BD is not common in childhood and the disease characteristics considerably differ between adults and children. 18 diagnostic/classification criteria have been published for BD to date. The pediatric BD (PEDBD) criteria, published in 2015, focused on pediatric BD, while the others mainly based on adult studies and are not validated for children. The aim of this review is to summarize the data about diagnostic/classification criteria for BD and to discuss the use and performance of the current criteria in pediatric BD. The covered topics are the characteristics of the diagnostic/classification criteria sets for BD, the factors restricting the universal use/acceptance of these criteria, and pediatric studies testing the performance of BD criteria sets. Having valid and universally accepted criteria with high performance is very important in pediatric BD as they help us determine patients for our studies and guide us through our clinical practice. There are less than 10 pediatric studies testing the performances of BD diagnostic/classification criteria. Their results suggest that revised ICBD (The International Criteria for BD) has the highest sensitivity, while ISG (The International Study Group) criteria remain as the most specific criteria set. Larger multinational pediatric BD cohorts with adequate control groups are required to compare the performance of the different criteria sets in children and to improve the performance of the existing PEDBD criteria.

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

Similar content being viewed by others

References

  1. Batu ED, Ozen S (2012) Pediatric vasculitis. Curr Rheumatol Rep 14(2):121–129. https://doi.org/10.1007/s11926-011-0232-4

    Article  CAS  PubMed  Google Scholar 

  2. Jennette JC, Falk RJ, Bacon PA, Basu N, Cid MC, Ferrario F, Flores-Suarez LF, Gross WL, Guillevin L, Hagen EC, Hoffman GS, Jayne DR, Kallenberg CG, Lamprecht P, Langford CA, Luqmani RA, Mahr AD, Matteson EL, Merkel PA, Ozen S, Pusey CD, Rasmussen N, Rees AJ, Scott DG, Specks U, Stone JH, Takahashi K, Watts RA (2013) 2012 revised International Chapel Hill Consensus Conference Nomenclature of Vasculitides. Arthritis Rheum 65(1):1–11. https://doi.org/10.1002/art.37715

    Article  CAS  PubMed  Google Scholar 

  3. Kone-Paut I (2016) Behcet’s disease in children, an overview. Pediatr Rheumatol 14(1):10. https://doi.org/10.1186/s12969-016-0070-z

    Article  Google Scholar 

  4. Davatchi F, Chams-Davatchi C, Shams H, Shahram F, Nadji A, Akhlaghi M, Faezi T, Ghodsi Z, Sadeghi Abdollahi B, Ashofteh F, Mohtasham N, Kavosi H, Masoumi M (2017) Behcet’s disease: epidemiology, clinical manifestations, and diagnosis. Expert Rev Clin Immunol 13(1):57–65. https://doi.org/10.1080/1744666X.2016.1205486

    Article  CAS  PubMed  Google Scholar 

  5. Atmaca L, Boyvat A, Yalcindag FN, Atmaca-Sonmez P, Gurler A (2011) Behcet disease in children. Ocul Immunol Inflamm 19(2):103–107. https://doi.org/10.3109/09273948.2011.555592

    Article  PubMed  Google Scholar 

  6. Ishido T, Horita N, Takeuchi M, Kawagoe T, Shibuya E, Yamane T, Hayashi T, Meguro A, Ishido M, Minegishi K, Yoshimi R, Kirino Y, Kato S, Arimoto J, Ishigatsubo Y, Takeno M, Kurosawa M, Kaneko T, Mizuki N (2017) Clinical manifestations of Behcet’s disease depending on sex and age: results from Japanese nationwide registration. Rheumatology 56(11):1918–1927. https://doi.org/10.1093/rheumatology/kex285

    Article  PubMed  Google Scholar 

  7. Shahram F, Nadji A, Akhlaghi M, Faezi ST, Chams-Davatchi C, Shams H, Ghodsi SZ, Davatchi F (2018) Paediatric Behcet’s disease in Iran: report of 204 cases. Clin Exp Rheumatol 36

  8. Koné-Paut IBJ (1993) La maladie de Behçet chez l’enfant en France. Arch Fr Pediatr 50:561–563

    PubMed  Google Scholar 

  9. Borlu M, Uksal U, Ferahbas A, Evereklioglu C (2006) Clinical features of Behcet’s disease in children. Int J Dermatol 45(6):713–716. https://doi.org/10.1111/j.1365-4632.2006.02754.x

    Article  PubMed  Google Scholar 

  10. Nanthapisal S, Klein NJ, Ambrose N, Eleftheriou D, Brogan PA (2016) Paediatric Behcet’s disease: a UK tertiary centre experience. Clin Rheumatol 35(10):2509–2516. https://doi.org/10.1007/s10067-016-3187-z

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kone-Paut I, Shahram F, Darce-Bello M, Cantarini L, Cimaz R, Gattorno M, Anton J, Hofer M, Chkirate B, Bouayed K, Tugal-Tutkun I, Kuemmerle-Deschner J, Agostini H, Federici S, Arnoux A, Piedvache C, Ozen S, Group P (2015) Consensus classification criteria for paediatric Behcet’s disease from a prospective observational cohort: PEDBD. Ann Rheum Dis 75(6):958–964. https://doi.org/10.1136/annrheumdis-2015-208491

    Article  PubMed  Google Scholar 

  12. Karincaoglu Y, Borlu M, Toker SC, Akman A, Onder M, Gunasti S, Usta A, Kandi B, Durusoy C, Seyhan M, Utas S, Saricaoglu H, Ozden MG, Uzun S, Tursen U, Cicek D, Donmez L, Alpsoy E (2008) Demographic and clinical properties of juvenile-onset Behcet’s disease: a controlled multicenter study. J Am Acad Dermatol 58(4):579–584. https://doi.org/10.1016/j.jaad.2007.10.452

    Article  PubMed  Google Scholar 

  13. Kitaichi N, Ohno S (2008) Behcet disease in children. Int Ophthalmol Clin 48(3):87–91. https://doi.org/10.1097/IIO.0b013e31817d8393

    Article  PubMed  Google Scholar 

  14. Davatchi F (2014) Behcet’s disease. Int J Rheum Dis 17(4):355–357. https://doi.org/10.1111/1756-185X.12378

    Article  PubMed  Google Scholar 

  15. Saadoun D, Wechsler B (2012) Behcet’s disease. Orphanet J Rare Dis 7:20. https://doi.org/10.1186/1750-1172-7-20

    Article  PubMed  PubMed Central  Google Scholar 

  16. Chang HK, Kim SY (2003) Survey and validation of the criteria for Behcet’s disease recently used in Korea: a suggestion for modification of the International Study Group criteria. J Korean Med Sci 18(1):88–92. https://doi.org/10.3346/jkms.2003.18.1.88

    Article  PubMed  PubMed Central  Google Scholar 

  17. Chang HK, Lee SS, Bai HJ, Lee YW, Yoon BY, Lee CH, Lee YH, Song GG, Chung WT, Lee SW, Choe JY, Kim CG, Chang DK (2004) Validation of the classification criteria commonly used in Korea and a modified set of preliminary criteria for Behcet’s disease: a multi-center study. Clin Exp Rheumatol 22(4 Suppl 34):S21–S26

    CAS  PubMed  Google Scholar 

  18. Hewitt J, Escande JP, Lauret P, Perlemuter L (1969) Criteria for diagnosis of Behcet’s syndrome. Bull Soc Fr Dermatol Syphiligr 76(4):565–568

    CAS  PubMed  Google Scholar 

  19. Hewitt J, Escande JP, Manesse S (1971) Revision of the diagnostic criteria of Behcet’s syndrome. Presse Med 79(20):901

    CAS  PubMed  Google Scholar 

  20. Mason RM, Barnes CG (1969) Behcet’s syndrome with arthritis. Ann Rheum Dis 28(2):95–103

    Article  CAS  Google Scholar 

  21. Mizushima Y (1988) Recent research into Behcet’s disease in Japan. Int J Tissue React 10(2):59–65

    CAS  PubMed  Google Scholar 

  22. International Team for the Revision of the International Criteria for Behcet’s D (2014) The International Criteria for Behcet’s Disease (ICBD): a collaborative study of 27 countries on the sensitivity and specificity of the new criteria. J EurAcad Dermatol Venereol 28(3):338–347. https://doi.org/10.1111/jdv.12107

    Article  Google Scholar 

  23. International Study Group for Behcet’s Disease (1990) Criteria for diagnosis of Behcet’s disease. Lancet 335(8697):1078–1080

    Google Scholar 

  24. The International Study Group for Behcet’s disease (1992) Evaluation of diagnostic (‘classification’) criteria in Behcet’s disease–towards internationally agreed criteria. Br J Rheumatol 31(5):299–308

    Article  Google Scholar 

  25. Curth HO (1946) Recurrent genito-oral aphthosis with hypopion (Behcet’s syndrome). Arch Dermatol 54:179–196

    CAS  Google Scholar 

  26. Behcet’s Disease Research Committee of Japan (1974) Behcet’s disease guide to the diagnosis of Behcet’s disease. Japan J Ophthalmol 18:291–294

    Google Scholar 

  27. Hubault A, Hamza M (1974) La maladie de Behçet en 1974. In: de Seze S et al (eds) L’actualite rhumatologique, vol 15. Expension Scientifique, Paris, pp 43–55

    Google Scholar 

  28. O’Duffy JD (1974) Critères proposés pour le diagnostique de la maladie de Behçet et notes therapeutiques. Rev Med (Paris) 36:2371–2379

    Google Scholar 

  29. Cheng SP, Zhang X-Q (1980) Some special clinical manifestations of Behçet’s disease-report of illustrative cases and review of the literature (author’s transl). Chinese J Intern Med 19:15–22

    Google Scholar 

  30. Dilsen N, Konice M, Aral O (1986) Our diagnostic criteria of Behcet’s disease-an overview. In: Lehner T, Barnes CG (eds) Recent advances in Behçet’s disease, vol International Congress and Symposium Series 103. London Royal Society of Medicine Services, London, pp 177–180

  31. Davatchi F, Shahram F, Akbarian M et al (1993) Accuracy of existing diagnostic criteria for Behçet’s disease. In: Wechsler B, Godeau P (eds) Behcet’s disease. Excerpta Medica International Congress Series 1037, Amsterdam, pp 225–228

  32. International Team for the Revision of the International Criteria for Behçet’s disease (2006) Revision of the International Criteria for Behçet’s disease (ICBD). Clin Exp Rheumatol 24(Suppl. 42):S14–S15

    Google Scholar 

  33. Dilsen N (2000) About diagnostic criteria for Behcet’s Disease: our new proposal. In: Bang D, Lee ES, Lee S (eds) Behçet’s Disease. Design Mecca Publishing Co., Seoul, pp 101–104

    Google Scholar 

  34. Davatchi F, Shahram F, Akbarian M et al (1993) Classification tree for the diagnosis of Behçet’s disease. In: Wechsler B, Godeau P (eds) Behçet’s Disease. Excerpta Medica International Congress Series 1037, Amsterdam, pp 245–248

  35. Davatchi F, Sadeghi Abdollahi B, Chams-Davatchi C, Shahram F, Shams H, Nadji A, Faezi T, Akhlaghi M, Ghodsi Z, Mohtasham N, Ashofteh F (2015) The saga of diagnostic/classification criteria in Behcet’s disease. Int J Rheum Dis 18(6):594–605. https://doi.org/10.1111/1756-185X.12520

    Article  PubMed  Google Scholar 

  36. Davatchi F, Chams-Davatchi C, Shahram F, Nadji A, Shams H, Ghodsi Z, Akhlaghi M, Naderi N, Sadeghi-Abdolahi B (2007) Pathergy test in Behçet’s disease: change in incidence over the time. APLAR J Rheumatol 10:333–335

    Article  Google Scholar 

  37. Batu ED, Ozen S (2015) Vasculitis: do we know more to classify better? Pediatr Nephrol 30(9):1425–1432. https://doi.org/10.1007/s00467-014-3015-0

    Article  PubMed  Google Scholar 

  38. 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):1409–1417. https://doi.org/10.1007/s00296-011-1999-3

    Article  PubMed  Google Scholar 

  39. Treudler R, Orfanos CE, Zouboulis CC (1999) Twenty-eight cases of juvenile-onset Adamantiades-Behcet disease in Germany. Dermatology 199(1):15–19. https://doi.org/10.1159/000018197

    Article  CAS  PubMed  Google Scholar 

  40. Kotter I, Vonthein R, Muller CA, Gunaydin I, Zierhut M, Stubiger N (2004) Behcet’s disease in patients of German and Turkish origin living in Germany: a comparative analysis. J Rheumatol 31(1):133–139

    PubMed  Google Scholar 

  41. Davatchi F, Chams-Davatchi C, Shams H, Nadji A, Faezi T, Akhlaghi M, Sadeghi Abdollahi B, Ashofteh F, Ghodsi Z, Mohtasham N, Shahram F (2016) Adult Behcet’s disease in Iran: analysis of 6075 patients. Int J Rheum Dis 19(1):95–103. https://doi.org/10.1111/1756-185X.12691

    Article  CAS  PubMed  Google Scholar 

  42. Gallizzi R, Pidone C, Cantarini L, Finetti M, Cattalini M, Filocamo G, Insalaco A, Rigante D, Consolini R, Maggio MC, Civino A, Martino S, Olivieri AN, Fabio G, Pastore S, Mauro A, Sutera D, Trimarchi G, Ruperto N, Gattorno M, Cimaz R (2017) A national cohort study on pediatric Behcet’s disease: cross-sectional data from an Italian registry. Pediatr Rheumatol Online J 15(1):84. https://doi.org/10.1186/s12969-017-0213-x

    Article  PubMed  PubMed Central  Google Scholar 

  43. Kim DY, Choi MJ, Cho S, Kim DW, Bang D (2014) Changing clinical expression of Behcet disease in Korea during three decades (1983–2012): chronological analysis of 3674 hospital-based patients. Br J Dermatol 170(2):458–461. https://doi.org/10.1111/bjd.12661

    Article  CAS  PubMed  Google Scholar 

  44. Kone-Paut I, Yurdakul S, Bahabri SA, Shafae N, Ozen S, Ozdogan H, Bernard JL (1998) Clinical features of Behcet’s disease in children: an international collaborative study of 86 cases. J Pediatr 132(4):721–725

    Article  CAS  Google Scholar 

  45. Aeschlimann FA, Batu ED, Canna SW, Go E, Gul A, Hoffmann P, Leavis HL, Ozen S, Schwartz DM, Stone DL, van Royen-Kerkof A, Kastner DL, Aksentijevich I, Laxer RM (2018) A20 haploinsufficiency (HA20): clinical phenotypes and disease course of patients with a newly recognised NF-kB-mediated autoinflammatory disease. Ann Rheum Dis 77(5):728–735. https://doi.org/10.1136/annrheumdis-2017-212403

    Article  CAS  PubMed  Google Scholar 

  46. Ozen S, Batu ED (2018) Vasculitis Pathogenesis: can we talk about precision medicine? Front Immunol 9:1892. https://doi.org/10.3389/fimmu.2018.01892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Alpsoy E, Elpek GO, Yilmaz F, Ciftcioglu MA, Akman A, Uzun S, Karakuzu A (2005) Androgen receptor levels of oral and genital ulcers and skin pathergy test in patients with Behcet’s disease. Dermatology 210(1):31–35. https://doi.org/10.1159/000081480

    Article  CAS  PubMed  Google Scholar 

  48. Bonitsis NG, Luong Nguyen LB, LaValley MP, Papoutsis N, Altenburg A, Kotter I, Micheli C, Maldini C, Mahr A, Zouboulis CC (2015) Gender-specific differences in Adamantiades-Behcet’s disease manifestations: an analysis of the German registry and meta-analysis of data from the literature. Rheumatology 54(1):121–133. https://doi.org/10.1093/rheumatology/keu247

    Article  CAS  PubMed  Google Scholar 

  49. Kural-Seyahi E, Fresko I, Seyahi N, Ozyazgan Y, Mat C, Hamuryudan V, Yurdakul S, Yazici H (2003) The long-term mortality and morbidity of Behcet syndrome: a 2-decade outcome survey of 387 patients followed at a dedicated center. Medicine 82(1):60–76

    Article  Google Scholar 

  50. Saadoun D, Wechsler B, Desseaux K, Le Thi Huong D, Amoura Z, Resche-Rigon M, Cacoub P (2010) Mortality in Behcet’s disease. Arthritis Rheum 62(9):2806–2812. https://doi.org/10.1002/art.27568

    Article  CAS  PubMed  Google Scholar 

  51. Kim DK, Chang SN, Bang D, Lee ES, Lee S (1994) Clinical analysis of 40 cases of childhood-onset Behcet’s disease. Pediatr Dermatol 11(2):95–101

    Article  CAS  Google Scholar 

  52. Kone-Paut I, Darce-Bello M, Shahram F, Gattorno M, Cimaz R, Ozen S, Cantarini L, Tugal-Tutktun I, Assaad-Khalil S, Hofer M, Kuemmerle-Deschner J, Benamour S, Al Mayouf S, Pajot C, Anton J, Faye A, Bono W, Nielsen S, Letierce A, Tran TA, Committee P-BIE (2011) Registries in rheumatological and musculoskeletal conditions. Paediatric Behcet’s disease: an international cohort study of 110 patients. One-year follow-up data. Rheumatology 50(1):184–188. https://doi.org/10.1093/rheumatology/keq324

    Article  PubMed  Google Scholar 

  53. Krause I, Uziel Y, Guedj D, Mukamel M, Harel L, Molad Y, Weinberger A (1999) Childhood Behcet’s disease: clinical features and comparison with adult-onset disease. Rheumatology 38(5):457–462

    Article  CAS  Google Scholar 

  54. Sibley C, Yazici Y, Tascilar K, Khan N, Bata Y, Yazici H, Goldbach-Mansky R, Hatemi G (2014) Behcet syndrome manifestations and activity in the United States versus Turkey—a cross-sectional cohort comparison. J Rheumatol 41(7):1379–1384. https://doi.org/10.3899/jrheum.131227

    Article  PubMed  PubMed Central  Google Scholar 

  55. Kobayashi T, Kishimoto M, Swearingen CJ, Filopoulos MT, Ohara Y, Tokuda Y, Oshikawa H, Yoshida K, Utsunomiya M, Kimura M, Okada M, Matsui K, Yazici Y (2013) Differences in clinical manifestations, treatment, and concordance rates with two major sets of criteria for Behcet’s syndrome for patients in the US and Japan: data from a large, three-center cohort study. Mod Rheumatol 23(3):547–553. https://doi.org/10.1007/s10165-012-0696-8

    Article  PubMed  Google Scholar 

  56. Moosmann T, Veraar C, Brunner J, Fraedrich G, Frech A, Horninger W, Ratzinger G, Streif W, Teuchner B, Willeit J, Zlamy M, De Zordo T, Schirmer M (2018) Differential clinical presentation of Adamantiades-Behcet’s disease in non-endemic and endemic areas: retrospective data from a Middle-European cohort study. Int J Rheum Dis. https://doi.org/10.1111/1756-185X.13306

    Article  PubMed  PubMed Central  Google Scholar 

  57. Davatchi F, Shahram F, Chams-Davatchi C, Shams H, Nadji A, Akhlaghi M, Faezi T, Ghodsi Z, Faridar A, Ashofteh F, Sadeghi Abdollahi B (2010) Behcet’s disease: from East to West. Clin Rheumatol 29(8):823–833. https://doi.org/10.1007/s10067-010-1430-6

    Article  PubMed  Google Scholar 

  58. Batu ED, Sonmez HE, Sozeri B, Butbul Aviel Y, Bilginer Y, Ozen S (2017) The performance of different classification criteria in paediatric Behcet’s disease. Clin Exp Rheumatol 35(6):119–123

    PubMed  Google Scholar 

  59. Assar S, Sadeghi B, Davatchi F, Ghodsi SZ, Nadji A, Shahram F, Ashofte F, Larimi SR, Sadeghi M (2017) The association of pathergy reaction and active clinical presentations of Behcet’s disease. Reumatologia 55(2):79–83. https://doi.org/10.5114/reum.2017.67602

    Article  PubMed  PubMed Central  Google Scholar 

  60. Davatchi F, Sadeghi Abdollahi B, Chams-Davatchi C, Shahram F, Ghodsi Z, Nadji A, Akhlaghi M, Faezi T, Shams H, Larimi R, Ashofteh F (2013) Impact of the positive pathergy test on the performance of classification/diagnosis criteria for Behcet’s disease. Mod Rheumatol 23(1):125–132. https://doi.org/10.1007/s10165-012-0626-9

    Article  PubMed  Google Scholar 

  61. Faezi ST, Paragomi P, Shahram F, Shams H, Shams-Davatchi C, Ghodsi Z, Nadji A, Akhlaghi M, Davatchi F (2014) Clinical features of Behcet’s disease in patients without oral aphthosis. Mod Rheumatol 24(4):637–639. https://doi.org/10.3109/14397595.2013.844400

    Article  PubMed  Google Scholar 

  62. Mat MC, Goksugur N, Engin B, Yurdakul S, Yazici H (2006) The frequency of scarring after genital ulcers in Behcet’s syndrome: a prospective study. Int J Dermatology 45(5):554–556. https://doi.org/10.1111/j.1365-4632.2006.02859.x

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Rheumatology, Department of Pediatrics, Ankara Training and Research Hospital, University of Health Sciences, 06100, Ankara, Turkey

    Ezgi Deniz Batu

Authors
  1. Ezgi Deniz Batu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

BED designed the structure of the article, drafted and critically revised the text, and approved the final version of the manuscript.

Corresponding author

Correspondence to Ezgi Deniz Batu.

Ethics declarations

Conflict of interest

Ezgi Deniz Batu declares that she has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by the author.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Batu, E.D. Diagnostic/classification criteria in pediatric Behçet’s disease. Rheumatol Int 39, 37–46 (2019). https://doi.org/10.1007/s00296-018-4208-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00296-018-4208-9

Keywords

Search

Navigation