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Vascular and Cardiac Involvement

  • Yesim Ozguler
  • Sinem Nihal Esatoglu
  • Emire Seyahi
  • Melike Melikoglu
Chapter

Abstract

As is true for other major organ involvement in Behçet syndrome (BS), vascular involvement is more common and runs a more severe course among males. It is a major cause of morbidity and mortality and has significant characteristic features that can be considered pathognomonic even without the concomitant presence of skin-mucosa lesions. It affects mostly veins, with a significant tendency for thrombosis and as a rule runs a relapsing course. As a result, patients tend to have several clusters of vascular involvement through their disease course. Vascular involvement either venous or arterial occurs diffusely in large segments through the vessel wall. We have now become aware of vein walls that may be thickened without overt vein disease among young patients with solo skin-mucosa lesions indicating that venous inflammation is the key feature in BS. The associated thrombus is strongly adherent to long segments of the wall with a low propensity for the development of emboli. Lower extremity deep vein thrombosis (LEDVT) is the earliest and most frequent manifestation, followed by vena cava inferior thrombosis. Dural sinuses and pulmonary arteries, structurally similar to veins, are also commonly involved, while pulmonary artery aneurysms are almost specific for BS. Despite intensive and early immunosuppressive treatment, mortality especially due to pulmonary artery involvement and Budd-Chiari syndrome is still increased. Additionally, the young male patient population with LEDVT alone is exposed to severe clinical and social consequences such as post-thrombotic syndrome and increased unemployment.

Keywords

Behçet syndrome Thrombosis Lower extremity vein thrombosis Vena cava thrombosis Pulmonary artery aneurysms Immunosuppressive treatment 

Abbreviations

AZA

Azathioprine

BCS

Budd-Chiari syndrome

BS

Behçet syndrome

CTA

Contrast-enhanced computed tomography angiography

CTEPH

Chronic thromboembolic pulmonary hypertension

CVST

Cerebral venous sinus thrombosis

Cyc-A

Cyclosporine-A

DVT

Deep vein thrombosis

IFN-alpha

Interferon-alpha

ISG

International Study Group

IVC

Inferior vena cava

IVCS

Inferior vena cava syndrome

LEDVT

Lower extremity deep vein thrombosis

MRA

Magnetic resonance angiography

MR

Magnetic resonance

PAA

Pulmonary artery aneurysm

PAI

Pulmonary artery involvement

PAT

Pulmonary artery thrombosis

PET/CT

Positron emission tomography/computed tomography

PTS

Post-thrombotic syndrome

sPAP

Systolic pulmonary artery pressure

SVC

Superior vena cava

SVCS

Superior vena cava syndrome

TA

Takayasu arteritis

TNFi

Tumor necrosis factor inhibitor

USG

Ultrasonography

VWT

Vein wall thickness

References

  1. 1.
    Seyahi E. Behcet’s disease: how to diagnose and treat vascular involvement. Best Pract Res Clin Rheumatol. 2016;30(2):279–95.CrossRefGoogle Scholar
  2. 2.
    Yazici H, Seyahi E, Hatemi G, Yazici Y. Behcet syndrome: a contemporary view. Nat Rev Rheumatol. 2018;14(2):119.CrossRefGoogle Scholar
  3. 3.
    Hughes JP, Stovin PG. Segmental pulmonary artery aneurysms with peripheral venous thrombosis. Br J Dis Chest. 1959;53(1):19–27.PubMedCrossRefGoogle Scholar
  4. 4.
    Koc Y, Gullu I, Akpek G, Akpolat T, Kansu E, Kiraz S, et al. Vascular involvement in Behcet’s disease. J Rheumatol. 1992;19(3):402–10.Google Scholar
  5. 5.
    Kuzu MA, Ozaslan C, Koksoy C, Gurler A, Tuzuner A. Vascular involvement in Behcet’s disease: 8-year audit. World J Surg. 1994;18(6):948–53. discussion 953–4CrossRefGoogle Scholar
  6. 6.
    Sarica-Kucukoglu R, Akdag-Kose A, Kayabal IM, Yazganoglu KD, Disci R, Erzengin D, Azizlerli G. Vascular involvement in Behcet’s disease: a retrospective analysis of 2319 cases. Int J Dermatol. 2006;45(8):919–21.PubMedCrossRefGoogle Scholar
  7. 7.
    Kural-Seyahi E, Fresko I, Seyahi N, Ozyazgan Y, Mat C, Hamuryudan V, et al. The long-term mortality and morbidity of Behcet syndrome: a 2-decade outcome survey of 387 patients followed at a dedicated center. Medicine (Baltimore). 2003;82(1):60–76.CrossRefGoogle Scholar
  8. 8.
    Tascilar K, Melikoglu M, Ugurlu S, Sut N, Caglar E, Yazici H. Vascular involvement in Behcet’s syndrome: a retrospective analysis of associations and the time course. Rheumatology (Oxford). 2014;53(11):2018–22.CrossRefGoogle Scholar
  9. 9.
    Desbois AC, Wechsler B, Resche-Rigon M, Piette JC, Huong Dle T, Amoura Z, et al. Immunosuppressants reduce venous thrombosis relapse in Behcet’s disease. Arthritis Rheum. 2012;64(8):2753–60.CrossRefGoogle Scholar
  10. 10.
    Alibaz-Oner F, Karadeniz A, Ylmaz S, Balkarl A, Kimyon G, Yazc A, et al. Behcet disease with vascular involvement: effects of different therapeutic regimens on the incidence of new relapses. Medicine (Baltimore). 2015;94(6):e494.CrossRefGoogle Scholar
  11. 11.
    Tursen U, Gurler A, Boyvat A. Evaluation of clinical findings according to sex in 2313 Turkish patients with Behcet’s disease. Int J Dermatol. 2003;42(5):346–51.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Silman A, Gul A. Is there a place for large vessel disease in the diagnostic criteria of Behcet’s disease? J Rheumatol. 2000;27(8):2050–1.PubMedGoogle Scholar
  13. 13.
    Schirmer M, Calamia KT, O'Duffy JD. Is there a place for large vessel disease in the diagnostic criteria of Behcet’s disease? J Rheumatol. 1999;26(12):2511–2.PubMedGoogle Scholar
  14. 14.
    International Study Group for Behcet’s Disease. Criteria for diagnosis of Behcet’s disease. Lancet. 1990;335(8697):1078–80.Google Scholar
  15. 15.
    Tunc R, Keyman E, Melikoglu M, Fresko I, Yazici H. Target organ associations in Turkish patients with Behcet’s disease: a cross sectional study by exploratory factor analysis. J Rheumatol. 2002;29(11):2393–6.Google Scholar
  16. 16.
    Krause I, Leibovici L, Guedj D, Molad Y, Uziel Y, Weinberger A. Disease patterns of patients with Behcet’s disease demonstrated by factor analysis. Clin Exp Rheumatol. 1999;17(3):347–50.Google Scholar
  17. 17.
    Ozguler Y, Hatemi G, Cetinkaya F, Tascilar K, Ugurlu S, Seyahi E, et al. Interferon-alpha for the Management of Lower Extremity Deep Vein Thrombosis in Behcet’s syndrome: a case series. Arthritis Rheumatol. 2018;70(suppl 10).Google Scholar
  18. 18.
    Ahn JK, Lee YS, Jeon CH, Koh EM, Cha HS. Treatment of venous thrombosis associated with Behcet’s disease: immunosuppressive therapy alone versus immunosuppressive therapy plus anticoagulation. Clin Rheumatol. 2008;27(2):201–5.PubMedCrossRefGoogle Scholar
  19. 19.
    Ozguler Y, Leccese P, Christensen R, Esatoglu SN, Bang D, Bodaghi B, et al. Management of major organ involvement of Behcet’s syndrome: a systematic review for update of the EULAR recommendations. Rheumatology (Oxford). 2018;57(12):2200–12.CrossRefGoogle Scholar
  20. 20.
    Lakhanpal S, Tani K, Lie JT, Katoh K, Ishigatsubo Y, Ohokubo T. Pathologic features of Behcet’s syndrome: a review of Japanese autopsy registry data. Hum Pathol. 1985;16(8):790–5.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Kobayashi M, Ito M, Nakagawa A, Matsushita M, Nishikimi N, Sakurai T, et al. Neutrophil and endothelial cell activation in the vasa vasorum in vasculo-Behcet disease. Histopathology. 2000;36(4):362–71.PubMedCrossRefGoogle Scholar
  22. 22.
    Matsumoto T, Uekusa T, Fukuda Y. Vasculo-Behcet’s disease: a pathologic study of eight cases. Hum Pathol. 1991;22(1):45–51.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Espinosa G, Font J, Tassies D, Vidaller A, Deulofeu R, Lopez-Soto A, et al. Vascular involvement in Behcet’s disease: relation with thrombophilic factors, coagulation activation, and thrombomodulin. Am J Med. 2002;112(1):37–43.PubMedCrossRefGoogle Scholar
  24. 24.
    Leiba M, Seligsohn U, Sidi Y, Harats D, Sela BA, Griffin JH, et al. Thrombophilic factors are not the leading cause of thrombosis in Behcet’s disease. Ann Rheum Dis. 2004;63(11):1445–9.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Chambers JC, Haskard DO, Kooner JS. Vascular endothelial function and oxidative stress mechanisms in patients with Behcet’s syndrome. J Am Coll Cardiol. 2001;37(2):517–20.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Labropoulos N, Summers KL, Sanchez IE, Raffetto J. Saphenous vein wall thickness in age and venous reflux-associated remodeling in adults. J Vasc Surg Venous Lymphat Disord. 2017;5(2):216–23.PubMedCrossRefGoogle Scholar
  27. 27.
    Chandrashekar A, Garry J, Gasparis A, Labropoulos N. Vein wall remodeling in patients with acute deep vein thrombosis and chronic postthrombotic changes. J Thromb Haemost. 2017;15(10):1989–93.PubMedCrossRefGoogle Scholar
  28. 28.
    Lau GT, Ridley LJ, Bannon PG, Wong LA, Trieu J, Brieger DB, et al. Lumen loss in the first year in saphenous vein grafts is predominantly a result of negative remodeling of the whole vessel rather than a result of changes in wall thickness. Circulation. 2006;114(1. Suppl):I435–40.PubMedGoogle Scholar
  29. 29.
    Ambrose N, Pierce IT, Gatehouse PD, Haskard DO, Firmin DN. Magnetic resonance imaging of vein wall thickness in patients with Behcet’s syndrome. Clin Exp Rheumatol. 2014;32(4. Suppl 84):S99–102.Google Scholar
  30. 30.
    Alibaz-Oner F, Ergelen R, Mutis A, Erturk Z, Asadova R, Ergun T, et al. Venous Vessel Wall thickness in lower extremity is increased in male Behcet’s disease patients. Arthritis Rheumatol. 2018;70.(suppl 10).Google Scholar
  31. 31.
    Seyahi E, Gjoni M, Durmaz ES, Akbas S, Sut N, Dikici AS, et al. Increased vein wall thickness in Behçet’s syndrome. J Vas Surgery. 2019;Seyahi E, Gjoni M, Durmaz ES, Akbas S, Sut N, Dikici AS, et al. Increased vein wall thickness in Behçet’s syndrome. J Vas Surgery. 2019.Google Scholar
  32. 32.
    Seyahi E, Cakmak OS, Tutar B, Arslan C, Dikici AS, Sut N, et al. Clinical and Ultrasonographic evaluation of lower-extremity vein thrombosis in Behcet syndrome: an observational study. Medicine (Baltimore). 2015;94(44):e1899.CrossRefGoogle Scholar
  33. 33.
    Jung JY, Kim DY, Bang D. Leg ulcers in Behcet’s disease. Br J Dermatol. 2008;158(1):178–9.PubMedGoogle Scholar
  34. 34.
    Ozguler Y, Kutlubay Z, Dikici AS, Melikoglu M, Mat C, Yazici H, et al. Leg ulcers in Behçet’s syndrome: an observational survey in 24 patients. Arthritis Rheumatol. 2018;70.(suppl 10).Google Scholar
  35. 35.
    Seyahi E, Hallac M, Vatankulu B, Ugurlu S, Melikoglu M, Yurdakul S, et al. 18F-FDG PET/CT in vascular disease due to Behçet’s syndrome. Arthritis Rheumatol. 2014;66(Suppl 10).Google Scholar
  36. 36.
    Kansu E, Ozer FL, Akalin E, Guler Y, Zileli T, Tanman E, et al. Behcet’s syndrome with obstruction of the venae cavae. A report of seven cases. Q J Med. 1972;41(162):151–68.PubMedGoogle Scholar
  37. 37.
    Houman H, Lamloum M, Ben Ghorbel I, Khiari-Ben Salah I, Miled M. Vena cava thrombosis in Behcet’s disease. Analysis of a series of 10 cases. Ann Med Interne (Paris). 1999;150(8):587–90.Google Scholar
  38. 38.
    Oh SH, Lee JH, Shin JU, Bang D. Dermatological features in Behcet disease-associated vena cava obstruction. Br J Dermatol. 2008;159(3):555–60.CrossRefGoogle Scholar
  39. 39.
    Gokturk A, Esatoglu SN, Ozguler Y, Atahan E, Musellim B, Hamuryudan V, et al. Increased frequency of obstructive sleep apnea syndrome in Behcet’s syndrome patients with vena cava superior thrombosis. Arthritis Rheumatol. 2018;70(suppl 10).Google Scholar
  40. 40.
    Benjilali L, Harmouche H, Alaoui-Bennesser H, Mezalek ZT, Adnaoui M, Aouni M, et al. Chylothorax and chylopericardium in a young man with Behcet’s disease. Joint Bone Spine. 2008;75(6):743–5.PubMedCrossRefGoogle Scholar
  41. 41.
    Tunaci A, Berkmen YM, Gokmen E. Thoracic involvement in Behcet’s disease: pathologic, clinical, and imaging features. AJR Am J Roentgenol. 1995;164(1):51–6.PubMedCrossRefGoogle Scholar
  42. 42.
    Desbois AC, Rautou PE, Biard L, Belmatoug N, Wechsler B, Resche-Rigon M, et al. Behcet’s disease in Budd-Chiari syndrome. Orphanet J Rare Dis. 2014;9:104.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Uskudar O, Akdogan M, Sasmaz N, Yilmaz S, Tola M, Sahin B. Etiology and portal vein thrombosis in Budd-Chiari syndrome. World J Gastroenterol. 2008;14(18):2858–62.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Harmanci O, Kav T, Peynircioglu B, Buyukasik Y, Sokmensuer C, Bayraktar Y. Long-term follow-up study in Budd-Chiari syndrome: single-center experience in 22 years. J Clin Gastroenterol. 2013;47(8):706–12.PubMedCrossRefGoogle Scholar
  45. 45.
    Sakr M, Barakat E, Abdelhakam S, Dabbous H, Yousuf S, Shaker M, et al. Epidemiological aspects of Budd-Chiari in Egyptian patients: a single-center study. World J Gastroenterol. 2011;17(42):4704–10.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Seyahi E, Caglar E, Ugurlu S, Kantarci F, Hamuryudan V, Sonsuz A, et al. An outcome survey of 43 patients with Budd-Chiari syndrome due to Behcet’s syndrome followed up at a single, dedicated center. Semin Arthritis Rheum. 2015;44(5):602–9.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Bayraktar Y, Balkanci F, Bayraktar M, Calguneri M. Budd-Chiari syndrome: a common complication of Behcet’s disease. Am J Gastroenterol. 1997;92(5):858–62.Google Scholar
  48. 48.
    Cantini F, Salvarani C, Niccoli L, Padula A, Arena AI, Bellandi F, et al. Treatment of thrombophlebitis of Behcet’s disease with low dose cyclosporin A. Clin Exp Rheumatol. 1999;17(3):391–2.Google Scholar
  49. 49.
    Calguneri M, Ozturk MA, Ertenli I, Kiraz S, Apras S, Ozbalkan Z. Effects of interferon alpha treatment on the clinical course of refractory Behcet’s disease: an open study. Ann Rheum Dis. 2003;62(5):492–3.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Emmi G, Vitale A, Silvestri E, Boddi M, Becatti M, Fiorillo C, et al. Adalimumab-based treatment versus disease-modifying Antirheumatic drugs for venous thrombosis in Behcet’s syndrome: a retrospective study of seventy patients with vascular involvement. Arthritis Rheumatol. 2018;70(9):1500–7.PubMedCrossRefGoogle Scholar
  51. 51.
    Hatemi G, Christensen R, Bang D, Bodaghi B, Celik AF, Fortune F, et al. 2018 update of the EULAR recommendations for the management of Behcet’s syndrome. Ann Rheum Dis. 2018;77(6):808–18.Google Scholar
  52. 52.
    Ko GY, Byun JY, Choi BG, Cho SH. The vascular manifestations of Behcet’s disease: angiographic and CT findings. Br J Radiol. 2000;73(876):1270–4.PubMedCrossRefGoogle Scholar
  53. 53.
    Saadoun D, Asli B, Wechsler B, Houman H, Geri G, Desseaux K, et al. Long-term outcome of arterial lesions in Behcet disease: a series of 101 patients. Medicine (Baltimore). 2012;91(1):18–24.CrossRefGoogle Scholar
  54. 54.
    Tohme A, Aoun N, El-Rassi B, Ghayad E. Vascular manifestations of Behcet’s disease. Eighteen cases among 140 patients. Joint Bone Spine. 2003;70(5):384–9.PubMedCrossRefGoogle Scholar
  55. 55.
    Kabbaj N, Benjelloun G, Gueddari FZ, Dafiri R, Imani F. Vascular involvements in Behcet disease. Based on 40 patient records. J Radiol. 1993;74(12):649–56.PubMedPubMedCentralGoogle Scholar
  56. 56.
    Duzgun N, Ates A, Aydintug OT, Demir O, Olmez U. Characteristics of vascular involvement in Behcet’s disease. Scand J Rheumatol. 2006;35(1):65–8.PubMedCrossRefGoogle Scholar
  57. 57.
    Fei Y, Li X, Lin S, Song X, Wu Q, Zhu Y, et al. Major vascular involvement in Behcet’s disease: a retrospective study of 796 patients. Clin Rheumatol. 2013;32(6):845–52.PubMedCrossRefGoogle Scholar
  58. 58.
    Hamuryudan V, Yurdakul S, Moral F, Numan F, Tuzun H, Tuzuner N, et al. Pulmonary arterial aneurysms in Behcet’s syndrome: a report of 24 cases. Br J Rheumatol. 1994;33(1):48–51.CrossRefGoogle Scholar
  59. 59.
    al-Dalaan AN, al Balaa SR, el Ramahi K, al-Kawi Z, Bohlega S, Bahabri S, et al. Behcet’s disease in Saudi Arabia. J Rheumatol. 1994;21(4):658–61.PubMedGoogle Scholar
  60. 60.
    Gurler A, Boyvat A, Tursen U. Clinical manifestations of Behcet’s disease: an analysis of 2147 patients. Yonsei Med J. 1997;38(6):423–7.PubMedCrossRefGoogle Scholar
  61. 61.
    Saba D, Saricaoglu H, Bayram AS, Erdogan C, Dilek K, Gebitekin C, et al. Arterial lesions in Behcet’s disease. Vasa. 2003;32(2):75–81.PubMedCrossRefGoogle Scholar
  62. 62.
    Hamuryudan V, Er T, Seyahi E, Akman C, Tuzun H, Fresko I, et al. Pulmonary artery aneurysms in Behcet syndrome. Am J Med. 2004;117(11):867–70.CrossRefGoogle Scholar
  63. 63.
    B'Chir Hamzaoui S, Harmel A, Bouslama K, Abdallah M, Ennafaa M, M'Rad S, et al. Behcet’s disease in Tunisia. Clinical study of 519 cases. Rev Med Interne. 2006;27(10):742–50.PubMedCrossRefGoogle Scholar
  64. 64.
    Neves FS, Caldas CA, Lage LV, Goldenstein-Schainberg C, Goncalves CR. Faraway from the silk route: demographic and clinical features of Behcet’s disease in 106 Brazilian patients. Clin Rheumatol. 2009;28(5):543–6.PubMedCrossRefGoogle Scholar
  65. 65.
    Davatchi F, Shahram F, Chams-Davatchi C, Shams H, Nadji A, Akhlaghi M, et al. Behcet’s disease in Iran: analysis of 6500 cases. Int J Rheum Dis. 2010;13(4):367–73.PubMedCrossRefGoogle Scholar
  66. 66.
    Ideguchi H, Suda A, Takeno M, Ueda A, Ohno S, Ishigatsubo Y. Characteristics of vascular involvement in Behcet’s disease in Japan: a retrospective cohort study. Clin Exp Rheumatol. 2011;29(4 Suppl 67):S47–53.PubMedGoogle Scholar
  67. 67.
    Seyahi E, Melikoglu M, Akman C, Hamuryudan V, Ozer H, Hatemi G, et al. Pulmonary artery involvement and associated lung disease in Behcet disease: a series of 47 patients. Medicine (Baltimore). 2012;91(1):35–48.CrossRefGoogle Scholar
  68. 68.
    Li S. Analysis of 27 cases of large vascular lesions in 161 cases of Behcet’s disease: clinical manifestations and treatment outcome. Clin Rheumatol. 2014;33(5):671–5.PubMedCrossRefGoogle Scholar
  69. 69.
    Lennikov A, Alekberova Z, Goloeva R, Kitaichi N, Denisov L, Namba K, Takeno M, Ishigatsubo Y, Mizuki N, Nasonov E, Ishida S, Ohno S. Single center study on ethnic and clinical features of Behcet’s disease in Moscow, Russia. Clin Rheumatol. 2015;34(2):321–7.CrossRefGoogle Scholar
  70. 70.
    Zhang X, Dai H, Ma Z, Yang Y, Liu Y. Pulmonary involvement in patients with Behcet’s disease: report of 15 cases. Clin Respir J. 2015;9(4):414–22.PubMedCrossRefGoogle Scholar
  71. 71.
    Liu Q, Ye W, Liu C, Li Y, Zeng R, Ni L. Outcomes of vascular intervention and use of perioperative medications for nonpulmonary aneurysms in Behcet disease. Surgery. 2016;159(5):1422–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Wechsler B, Le Thi Huong Du LT, de Gennes C, Bletry O, Piette JC, Mathieu A, et al. Arterial manifestations of Behcet’s disease. 12 cases. Rev Med Interne. 1989;10(4):303–11.PubMedCrossRefGoogle Scholar
  73. 73.
    Uzun O, Akpolat T, Erkan L. Pulmonary vasculitis in behcet disease: a cumulative analysis. Chest. 2005;127(6):2243–53.PubMedCrossRefGoogle Scholar
  74. 74.
    Erkan F, Gul A, Tasali E. Pulmonary manifestations of Behcet’s disease. Thorax. 2001;56(7):572–8.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Saadoun D, Wechsler B, Desseaux K, Le Thi Huong D, Amoura Z, Resche-Rigon M, et al. Mortality in Behcet’s disease. Arthritis Rheum. 2010;62(9):2806–12.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Uzun O, Erkan L, Akpolat I, Findik S, Atici AG, Akpolat T. Pulmonary involvement in Behcet’s disease. Respiration. 2008;75(3):310–21.PubMedCrossRefGoogle Scholar
  77. 77.
    Yuan S. Pulmonary artery aneurysms in Behçet disease. J Vasc Bras. 2014;13(3):217–28.CrossRefGoogle Scholar
  78. 78.
    Tunaci M, Ozkorkmaz B, Tunaci A, Gul A, Engin G, Acunas B. CT findings of pulmonary artery aneurysms during treatment for Behcet’s disease. AJR Am J Roentgenol. 1999;172(3):729–33.PubMedCrossRefGoogle Scholar
  79. 79.
    Esatoglu SN, Seyahi E, Ugurlu S, Gulsen F, Akman C, Cantasdemir M, et al. Bronchial artery enlargement may be the cause of recurrent haemoptysis in Behcet’s syndrome patients with pulmonary artery involvement during follow-up. Clin Exp Rheumatol. 2016;34(6 Suppl 102):92–6.PubMedGoogle Scholar
  80. 80.
    Mehdipoor G, Davatchi F, Ghoreishian H, Arjmand Shabestari A. Imaging manifestations of Behcet’s disease: key considerations and major features. Eur J Radiol. 2018;98:214–25.PubMedCrossRefGoogle Scholar
  81. 81.
    Trad S, Bensimhon L, El Hajjam M, Chinet T, Wechsler B, Saadoun D. 18F-fluorodeoxyglucose-positron emission tomography scanning is a useful tool for therapy evaluation of arterial aneurysm in Behcet’s disease. Joint Bone Spine. 2013;80(4):420–3.PubMedCrossRefGoogle Scholar
  82. 82.
    Cho SB, Yun M, Lee JH, Kim J, Shim WH, Bang D. Detection of cardiovascular system involvement in Behcet’s disease using fluorodeoxyglucose positron emission tomography. Semin Arthritis Rheum. 2011;40(5):461–6.PubMedCrossRefGoogle Scholar
  83. 83.
    Toz BEB, Kamali S, Inanc M, Ocal L, Gul A. PET/CT imaging in patients with vascular Behcet disease [abstract]. Arthritis Rheumatol. 2016;68(suppl 10).Google Scholar
  84. 84.
    Seyahi E, Baskurt M, Melikoglu M, Akman C, Olgun DC, Simsek E, et al. The estimated pulmonary artery pressure can be elevated in Behcet’s syndrome. Respir Med. 2011;105(11):1739–47.PubMedCrossRefGoogle Scholar
  85. 85.
    Hamuryudan V, Oz B, Tuzun H, Yazici H. The menacing pulmonary artery aneurysms of Behcet’s syndrome. Clin Exp Rheumatol. 2004;22(4 Suppl 34):S1–3.PubMedGoogle Scholar
  86. 86.
    Serra G, Brun AL, Toledano D, Cluzel P, Grenier PA. Thoracic involvement in systemic primary vasculitis: radiological patterns and follow-up. JBR-BTR. 2014;97(2):57–68.PubMedGoogle Scholar
  87. 87.
    Gul A, Yilmazbayhan D, Buyukbabani N, Lie JT, Tunaci M, Tunaci A, et al. Organizing pneumonia associated with pulmonary artery aneurysms in Behcet’s disease. Rheumatology (Oxford). 1999;38(12):1285–9.CrossRefGoogle Scholar
  88. 88.
    Leccese P, Ozguler Y, Christensen R, Esatoglu SN, Bang D, Bodaghi B, et al. Management of skin, mucosa and joint involvement of Behcet’s syndrome: a systematic review for update of the EULAR recommendations for the management of Behcet’s syndrome. Semin Arthritis Rheum. 2018. pii: S0049-0172(18)30240-3.Google Scholar
  89. 89.
    Hamuryudan V, Seyahi E, Ugurlu S, Melikoglu M, Hatemi G, Ozguler Y, et al. Pulmonary artery involvement in Behcets syndrome: effects of anti-Tnf treatment. Semin Arthritis Rheum. 2015;45(3):369–73.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Maurer B, Hensel M, Max R, Fiehn C, Ho AD, Lorenz HM. Autologous haematopoietic stem cell transplantation for Behcet’s disease with pulmonary involvement: analysis after 5 years of follow up. Ann Rheum Dis. 2006;65(1):127–9.PubMedCrossRefGoogle Scholar
  91. 91.
    Voiriot G, Parrot A, Antoine M, Gibelin A, Haddad S, Carette MF. Transcatheter embolotherapy of pulmonary artery aneurysms as emergency treatment of hemoptysis in Behcet patients: experience of a referral center and a review of the literature. Intern Emerg Med. 2018;13(4):491–500.CrossRefGoogle Scholar
  92. 92.
    Tuzun H, Seyahi E, Guzelant G, Oz B, Batur S, Demirhan O, et al. Surgical treatment of pulmonary complications in Behcet’s syndrome. Semin Thorac Cardiovasc Surg. 2018;30(3):369–78.PubMedCrossRefGoogle Scholar
  93. 93.
    Yildizeli SO, Yanartas M, Tas S, Direskeneli H, Mutlu B, Ceyhan B, et al. Outcomes of patients with Behcet’s syndrome after pulmonary endarterectomy. Thorac Cardiovasc Surg. 2018;66(2):187–92.PubMedCrossRefGoogle Scholar
  94. 94.
    Chae EJ, Do KH, Seo JB, Park SH, Kang JW, Jang YM, et al. Radiologic and clinical findings of Behcet disease: comprehensive review of multisystemic involvement. Radiographics. 2008;28(5):e31.PubMedCrossRefGoogle Scholar
  95. 95.
    Suzuki K, Kazui T, Yamashita K, Terada H, Washiyama N, Suzuki T. Emergency operation for distal aortic arch aneurysm in Behcet’s disease. Jpn J Thorac Cardiovasc Surg. 2005;53(7):389–92.PubMedCrossRefGoogle Scholar
  96. 96.
    Tuzun H, Seyahi E, Arslan C, Hamuryudan V, Besirli K, Yazici H. Management and prognosis of nonpulmonary large arterial disease in patients with Behcet disease. J Vasc Surg. 2012;55(1):157–63.CrossRefGoogle Scholar
  97. 97.
    Tuzun H, Besirli K, Sayin A, Vural FS, Hamuryudan V, Hizli N, et al. Management of aneurysms in Behcet’s syndrome: an analysis of 24 patients. Surgery. 1997;121(2):150–6.PubMedCrossRefGoogle Scholar
  98. 98.
    Hoffman GS. (2003) Large-vessel vasculitis: unresolved issues. Arthritis Rheum. 2003;48(9):2406–14.PubMedCrossRefGoogle Scholar
  99. 99.
    Stone JR, Bruneval P, Angelini A, Bartoloni G, Basso C, Batoroeva L, et al. Consensus statement on surgical pathology of the aorta from the Society for Cardiovascular Pathology and the Association for European Cardiovascular Pathology: I. inflammatory diseases. Cardiovasc Pathol. 2015;24(5):267–78.PubMedCrossRefGoogle Scholar
  100. 100.
    Le Thi Huong D, Wechsler B, Papo T, Piette JC, Bletry O, Vitoux JM, et al. Arterial lesions in Behcet’s disease. A study in 25 patients. J Rheumatol. 1995;22(11):2103–13.PubMedGoogle Scholar
  101. 101.
    Kim WH, Choi D, Kim JS, Ko YG, Jang Y, Shim WH. Effectiveness and safety of endovascular aneurysm treatment in patients with vasculo-Behcet disease. J Endovasc Ther. 2009;16(5):631–6.PubMedCrossRefGoogle Scholar
  102. 102.
    Ozeren M, Mavioglu I, Dogan OV, Yucel E. Reoperation results of arterial involvement in Behcet’s disease. Eur J Vasc Endovasc Surg. 2000;20(6):512–9.PubMedCrossRefGoogle Scholar
  103. 103.
    Koksoy C, Gyedu A, Alacayir I, Bengisun U, Uncu H, Anadol E. Surgical treatment of peripheral aneurysms in patients with Behcet’s disease. Eur J Vasc Endovasc Surg. 2011;42(4):525–30.PubMedCrossRefGoogle Scholar
  104. 104.
    Hosaka A, Miyata T, Shigematsu H, Shigematsu K, Okamoto H, Ishii S, et al. Long-term outcome after surgical treatment of arterial lesions in Behcet disease. J Vasc Surg. 2005;42(1):116–21.PubMedCrossRefGoogle Scholar
  105. 105.
    Yin H, Li S, Wang M, Hu Z, Wang J, Yao C, et al. The value of endografts in the surgical management of arterial lesions secondary to Behcet disease. J Vasc Surg. 2017;65(2):471–7.PubMedCrossRefGoogle Scholar
  106. 106.
    Merashli M, Ster IC, Ames PR. Subclinical atherosclerosis in Behcet’s disease: a systematic review and meta-analysis. Semin Arthritis Rheum. 2016;45(4):502–10.PubMedCrossRefGoogle Scholar
  107. 107.
    Yazici H, Seyahi E. Behcet syndrome: the vascular cluster. Turk J Med Sci. 2016;46(5):1277–80.PubMedCrossRefGoogle Scholar
  108. 108.
    Farouk H, Zayed HS, El-Chilali K. Cardiac findings in patients with Behcet’s disease: facts and controversies. Anatol J Cardiol. 2016;16(7):529–33.PubMedPubMedCentralGoogle Scholar
  109. 109.
    Geri G, Wechsler B, Thi Huong d L, Isnard R, Piette JC, Amoura Z, et al. Spectrum of cardiac lesions in Behcet disease: a series of 52 patients and review of the literature. Medicine (Baltimore). 2012;91(1):25–34.CrossRefGoogle Scholar
  110. 110.
    Mogulkoc N, Burgess MI, Bishop PW. Intracardiac thrombus in Behcet’s disease: a systematic review. Chest. 2000;118(2):479–87.PubMedCrossRefGoogle Scholar
  111. 111.
    Seyahi E, Memisoglu E, Hamuryudan V, Tepe S, Aker UT, Balci H, et al. Coronary atherosclerosis in Behcet’s syndrome: a pilot study using electron-beam computed tomography. Rheumatology (Oxford). 2004;43(11):1448–50.CrossRefGoogle Scholar
  112. 112.
    Yue C, Li J, Li M, Zhang F, Zhao D, Cui Q. Cardiac mass in Behcet’s disease. Clin Exp Rheumatol. 2012;30(3 Suppl 72):S27–31.PubMedGoogle Scholar
  113. 113.
    Lee I, Park S, Hwang I, Kim MJ, Nah SS, Yoo B, et al. Cardiac Behcet disease presenting as aortic valvulitis/aortitis or right heart inflammatory mass: a clinicopathologic study of 12 cases. Am J Surg Pathol. 2008;32(3):390–8.PubMedCrossRefGoogle Scholar
  114. 114.
    Sacre K, Ducrocq G, Hernigou A, Laissy JP, Papo T. Unusual cardiovascular events in Behcet’s disease. Clin Exp Rheumatol. 2010;28(4 Suppl 60):S82–5.PubMedGoogle Scholar
  115. 115.
    Emmungil H, Yasar Bilge NS, Kucuksahin O, Kilic L, Okutucu S, Gucenmez S, et al. A rare but serious manifestation of Behcet’s disease: intracardiac thrombus in 22 patients. Clin Exp Rheumatol. 2014;32(4 Suppl 84):S87–92.PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Yesim Ozguler
    • 1
  • Sinem Nihal Esatoglu
    • 1
  • Emire Seyahi
    • 1
  • Melike Melikoglu
    • 1
  1. 1.Division of Rheumatology, Department of Internal MedicineIstanbul University-CerrahpasaIstanbulTurkey

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