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Clinical Reviews in Allergy & Immunology

, Volume 48, Issue 1, pp 97–103 | Cite as

Pulmonary Vasculature and Critical Asthma Syndromes: a Comprehensive Review

  • Mark AvdalovicEmail author
Article

Abstract

One of the important factors and consequences in persistent asthma is the change in the vasculature of the airways and lung parenchyma. These changes could contribute to worsening asthma control and predispose asthmatics to critical asthma syndromes. For many years, the contribution of vasculature to severe asthma was limited to discussion of small and medium vessel vasculitis commonly referred to as Churg − Strauss syndrome. This comprehensive review will explore the known mechanisms that are associated with remodeling of the vasculature in a variety of critical asthma presentations. Inflammation of pulmonary and bronchial small blood vessels may contribute significantly but silently to asthma pathobiology. Inflammation in the vasculature of the lung parenchyma can decrease lung capacity while inflammation in airway vasculature can decrease airflow. This review will provide a modern perspective on Churg–Strauss syndromes with a focus on phenotyping, mechanism, and ultimately modern therapeutic approaches. Vascular remodeling and airway remodeling are not mutually exclusive concepts in understanding the progression of asthma and frequency of acute exacerbations. Furthermore, the contribution of vascular leak, particularly in the parenchymal vasculature, has become an increasingly recognized component of certain presentations of poorly controlled, severe persistent asthmatic and during exacerbations. We highlight how these mechanisms can contribute to some the severe presentations of influenza infection in patients with a history of asthma. The ultimate aim of this review is to summarize the current literature concerning vasculitis and the contribution of airway and parenchymal vascular remodeling to presentation of persistent asthma and its consequences during acute exacerbations and critical asthma syndromes.

Keywords

Asthma Churg–Strauss syndromes Vasculature Eosinophilic granulomatosis polyangiitis 

References

  1. 1.
    Churg J, Strauss L (1951) Allergic granulomatosis, allergic angiitis, and periarteritis nodosa. Am J Pathol 27:277–301PubMedCentralPubMedGoogle Scholar
  2. 2.
    Tervaert JW, Limburg PC, Elema JD, Huitema MG, Horst G, The TH, Kallenberg CG (1991) Detection of autoantibodies against myeloid lysosomal enzymes: a useful adjunct to classification of patients with biopsy-proven necrotizing arteritis. Am J Med 91:59–66PubMedCrossRefGoogle Scholar
  3. 3.
    Sinico RA, Di Toma L, Maggiore U, Bottero P, Radice A, Tosoni C, Grasselli C et al (2005) Prevalence and clinical significance of antineutrophil cytoplasmic antibodies in Churg–Strauss syndrome. Arthritis Rheum 52:2926–2935PubMedCrossRefGoogle Scholar
  4. 4.
    Sable-Fourtassou R, Cohen P, Mahr A, Pagnoux C, Mouthon L, Jayne D, Blockmans D et al (2005) Antineutrophil cytoplasmic antibodies and the Churg–Strauss syndrome. Ann Intern Med 143:632–638PubMedCrossRefGoogle Scholar
  5. 5.
    Keogh KA, Specks U (2003) Churg–Strauss syndrome: clinical presentation, antineutrophil cytoplasmic antibodies, and leukotriene receptor antagonists. Am J Med 115:284–290PubMedCrossRefGoogle Scholar
  6. 6.
    Ramentol-Sintas M, Martinez-Valle F, Solans-Laque R (2012) Churg–Strauss syndrome: an evolving paradigm. Autoimmun Rev 12:235–240PubMedCrossRefGoogle Scholar
  7. 7.
    Lanham JG, Elkon KB, Pusey CD, Hughes GR (1984) Systemic vasculitis with asthma and eosinophilia: a clinical approach to the Churg–Strauss syndrome. Medicine (Baltimore) 63:65–81CrossRefGoogle Scholar
  8. 8.
    Hayakawa H, Sato A, Yagi T, Shimizu T, Miyajima H, Taniguchi M, Akiyama J (1993) Clinical features and prognosis of Churg–Strauss syndrome. Nihon Kyobu Shikkan Gakkai Zasshi 31:59–64PubMedGoogle Scholar
  9. 9.
    Knoell DL, Lucas J, Allen JN (1998) Churg–Strauss syndrome associated with zafirlukast. Chest 114:332–334PubMedCrossRefGoogle Scholar
  10. 10.
    Hauser T, Mahr A, Metzler C, Coste J, Sommerstein R, Gross WL, Guillevin L et al (2008) The leucotriene receptor antagonist montelukast and the risk of Churg–Strauss syndrome: a case-crossover study. Thorax 63:677–682PubMedCrossRefGoogle Scholar
  11. 11.
    Kiene M, Csernok E, Muller A, Metzler C, Trabandt A, Gross WL (2001) Elevated interleukin-4 and interleukin-13 production by T cell lines from patients with Churg–Strauss syndrome. Arthritis Rheum 44:469–473PubMedCrossRefGoogle Scholar
  12. 12.
    Jakiela B, Sanak M, Szczeklik W, Sokolowska B, Plutecka H, Mastalerz L, Musial J et al (2011) Both Th2 and Th17 responses are involved in the pathogenesis of Churg–Strauss syndrome. Clin Exp Rheumatol 29:S23–S34PubMedGoogle Scholar
  13. 13.
    Dallos T, Heiland GR, Strehl J, Karonitsch T, Gross WL, Moosig F, Holl-Ulrich C et al (2010) CCL17/thymus and activation-related chemokine in Churg–Strauss syndrome. Arthritis Rheum 62:3496–3503PubMedCrossRefGoogle Scholar
  14. 14.
    Muschen M, Warskulat U, Perniok A, Even J, Moers C, Kismet B, Temizkan N et al (1999) Involvement of soluble CD95 in Churg–Strauss syndrome. Am J Pathol 155:915–925PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Vaglio A, Buzio C, Zwerina J (2013) Eosinophilic granulomatosis with polyangiitis (Churg–Strauss): state of the art. Allergy 68:261–273PubMedCrossRefGoogle Scholar
  16. 16.
    Ribi C, Cohen P, Pagnoux C, Mahr A, Arene JP, Lauque D, Puechal X et al (2008) Treatment of Churg–Strauss syndrome without poor-prognosis factors: a multicenter, prospective, randomized, open-label study of seventy-two patients. Arthritis Rheum 58:586–594PubMedCrossRefGoogle Scholar
  17. 17.
    Thiel J, Hassler F, Salzer U, Voll RE, Venhoff N (2013) Rituximab in the treatment of refractory or relapsing eosinophilic granulomatosis with polyangiitis (Churg–Strauss syndrome). Arthritis Res Ther 15:R133PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Jennette JC, Falk RJ, Andrassy K, Bacon PA, Churg J, Gross WL, Hagen EC et al (1994) Nomenclature of systemic vasculitides. Proposal of an international consensus conference. Arthritis Rheum 37:187–192PubMedCrossRefGoogle Scholar
  19. 19.
    Zwerina J, Axmann R, Jatzwauk M, Sahinbegovic E, Polzer K, Schett G (2009) Pathogenesis of Churg–Strauss syndrome: recent insights. Autoimmunity 42:376–379PubMedCrossRefGoogle Scholar
  20. 20.
    Comarmond C, Pagnoux C, Khellaf M, Cordier JF, Hamidou M, Viallard JF, Maurier F et al (2013) Eosinophilic granulomatosis with polyangiitis (Churg–Strauss): clinical characteristics and long-term followup of the 383 patients enrolled in the French Vasculitis Study Group cohort. Arthritis Rheum 65:270–281PubMedCrossRefGoogle Scholar
  21. 21.
    Hashimoto M, Tanaka H, Abe S (2005) Quantitative analysis of bronchial wall vascularity in the medium and small airways of patients with asthma and COPD. Chest 127:965–972PubMedCrossRefGoogle Scholar
  22. 22.
    Li X, Wilson JW (1997) Increased vascularity of the bronchial mucosa in mild asthma. Am J Respir Crit Care Med 156:229–233PubMedCrossRefGoogle Scholar
  23. 23.
    Salvato G (2001) Quantitative and morphological analysis of the vascular bed in bronchial biopsy specimens from asthmatic and non-asthmatic subjects. Thorax 56:902–906PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Avdalovic MV, Putney LF, Schelegle ES, Miller L, Usachenko JL, Tyler NK, Plopper CG et al (2006) Vascular remodeling is airway generation-specific in a primate model of chronic asthma. Am J Respir Crit Care Med 174:1069–1076PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Dunnill MS (1960) The pathology of asthma, with special reference to changes in the bronchial mucosa. J Clin Pathol 13:27–33PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Evans MJ, Van Winkle LS, Fanucchi MV, Plopper CG (1999) The attenuated fibroblast sheath of the respiratory tract epithelial–mesenchymal trophic unit. Am J Respir Cell Mol Biol 21:655–657PubMedCrossRefGoogle Scholar
  27. 27.
    Lee CG, Link H, Baluk P, Homer RJ, Chapoval S, Bhandari V, Kang MJ et al (2004) Vascular endothelial growth factor (VEGF) induces remodeling and enhances TH2-mediated sensitization and inflammation in the lung. Nat Med 10:1095–1103PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Textor B, Licht AH, Tuckermann JP, Jessberger R, Razin E, Angel P, Schorpp-Kistner M et al (2007) JunB is required for IgE-mediated degranulation and cytokine release of mast cells. J Immunol 179:6873–6880PubMedCrossRefGoogle Scholar
  29. 29.
    Abdel-Majid RM, Marshall JS (2004) Prostaglandin E2 induces degranulation-independent production of vascular endothelial growth factor by human mast cells. J Immunol 172:1227–1236PubMedCrossRefGoogle Scholar
  30. 30.
    Hoshino M, Takahashi M, Aoike N (2001) Expression of vascular endothelial growth factor, basic fibroblast growth factor, and angiogenin immunoreactivity in asthmatic airways and its relationship to angiogenesis. J Allergy Clin Immunol 107:295–301PubMedCrossRefGoogle Scholar
  31. 31.
    Carroll NG, Cooke C, James AL (1997) Bronchial blood vessel dimensions in asthma. Am J Respir Crit Care Med 155:689–695PubMedCrossRefGoogle Scholar
  32. 32.
    Tseliou E, Bakakos P, Kostikas K, Hillas G, Mantzouranis K, Emmanouil P, Simoes D et al (2012) Increased levels of angiopoietins 1 and 2 in sputum supernatant in severe refractory asthma. Allergy 67:396–402PubMedCrossRefGoogle Scholar
  33. 33.
    Papadaki G, Bakakos P, Kostikas K, Hillas G, Tsilogianni Z, Koulouris NG, Papiris S, Loukides S (2013) Vascular endothelial growth factor and cysteinyl leukotrienes in sputum supernatant of patients with asthma. Respir Med 107(9):1339–1345Google Scholar
  34. 34.
    Hossny E, El-Awady H, Bakr S, Labib A (2009) Vascular endothelial growth factor overexpression in induced sputum of children with bronchial asthma. Pediatr Allergy Immunol 20:89–96PubMedCrossRefGoogle Scholar
  35. 35.
    Abdel-Rahman AM, el-Sahrigy SA, Bakr SI (2006) A comparative study of two angiogenic factors: vascular endothelial growth factor and angiogenin in induced sputum from asthmatic children in acute attack. Chest 129:266–271PubMedCrossRefGoogle Scholar
  36. 36.
    Bhandari V, Choo-Wing R, Lee CG, Yusuf K, Nedrelow JH, Ambalavanan N, Malkus H et al (2008) Developmental regulation of NO-mediated VEGF-induced effects in the lung. Am J Respir Cell Mol Biol 39:420–430PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Stalcup SA, Mellins RB (1977) Mechanical forces producing pulmonary edema in acute asthma. N Engl J Med 297:592–596PubMedCrossRefGoogle Scholar
  38. 38.
    Pendino JC, Nannini LJ, Chapman KR, Slutsky A, Molfino NA (1998) Effect of inhaled furosemide in acute asthma. J Asthma 35:89–93PubMedCrossRefGoogle Scholar
  39. 39.
    McKenna JJ, Bramley AM, Skarbinski J, Fry AM, Finelli L, Jain S (2013) Asthma in patients hospitalized with pandemic influenza A(H1N1)pdm09 virus infection-United States, 2009. BMC Infect Dis 13:57PubMedCrossRefGoogle Scholar
  40. 40.
    Mauad T, Hajjar LA, Callegari GD, da Silva LF, Schout D, Galas FR, Alves VA et al (2010) Lung pathology in fatal novel human influenza A (H1N1) infection. Am J Respir Crit Care Med 181:72–79PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Division of Pulmonary, Critical Care, and Sleep MedicineUniversity of California, Davis, School of MedicineDavisUSA
  2. 2.Division of Pulmonary, Critical Care, and Sleep Medicine, Department of Internal MedicineUniversity of California, DavisSacramentoUSA

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