Anti-inflammatory and immunomodulatory properties of azithromycin involved in treatment and prevention of chronic lung allograft rejection

Transplantation

Volumn 94, Issue 2, 2012, Pages 101-109

  Vos, Robin ^a   Vanaudenaerde, Bart M ^a   Verleden, Stijn E ^a   Ruttens, David ^a   Vaneylen, Annemie ^a   Van Raemdonck, Dirk E ^a   Dupont, Lieven J ^a   Verleden, Geert M ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Azithromycin; Bronchiolitis obliterans syndrome; Chronic lung allograft rejection; Lung transplantation; Obliterative bronchiolitis

Indexed keywords

AZATHIOPRINE; AZITHROMYCIN; CLARITHROMYCIN; CYCLOSPORIN A; EVEROLIMUS; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 8; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PLACEBO; PREDNISOLONE; RAPAMYCIN; TACROLIMUS;

ABDOMINAL PAIN; ADAPTIVE IMMUNITY; ANTIBIOTIC RESISTANCE; ANTIINFLAMMATORY ACTIVITY; BRONCHIECTASIS; BRONCHIOLITIS OBLITERANS; CELLULAR IMMUNITY; CHRONIC GRAFT REJECTION; CYSTIC FIBROSIS; CYTOKINE RESPONSE; DIARRHEA; DOSE RESPONSE; DRUG DOSE REDUCTION; DRUG ELIMINATION; DRUG FECES LEVEL; DRUG HYPERSENSITIVITY; DRUG SAFETY; DRUG WITHDRAWAL; FORCED EXPIRATORY VOLUME; FUNCTIONAL ASSESSMENT; GASTROINTESTINAL SYMPTOM; HEARING LOSS; HLA TYPING; HOST RESISTANCE; HUMAN; HYPONATREMIA; IMMUNOMODULATION; IMMUNOPATHOGENESIS; IMMUNOSTIMULATION; INNATE IMMUNITY; INTERSTITIAL NEPHRITIS; LIVER DISEASE; LOW DRUG DOSE; LUNG GRAFT REJECTION; LUNG LAVAGE; LUNG TRANSPLANTATION; MYASTHENIA GRAVIS; NAUSEA; NEUTROPHILIA; NONHUMAN; OBSTRUCTIVE JAUNDICE; PATIENT SAFETY; PRIORITY JOURNAL; PSEUDOMONAS INFECTION; QT PROLONGATION; REVIEW; RISK ASSESSMENT; RISK FACTOR; SIDE EFFECT; SPIROMETRY; SURVIVAL RATE; SURVIVAL TIME; TH17 CELL; TINNITUS; TORSADE DES POINTES; TREATMENT OUTCOME; VOMITING;

ANTI-BACTERIAL AGENTS; ANTI-INFLAMMATORY AGENTS; AZITHROMYCIN; BRONCHIOLITIS OBLITERANS; CHRONIC DISEASE; GRAFT REJECTION; HUMANS; IMMUNOLOGIC FACTORS; LUNG TRANSPLANTATION; TRANSPLANTATION, HOMOLOGOUS;

EID: 84864278385     PISSN: 00411337     EISSN: None     Source Type: Journal    
DOI: 10.1097/TP.0b013e31824db9da     Document Type: Review

References (97)

1. Estenne M, Maurer JR, Boehler A, et al. Bronchiolitis obliterans syndrome 2001: An update of the diagnostic criteria. J Heart Lung Transplant 2002; 21: 297.
2. Hagedorn PH, Burton CM, Carlsen J, et al. Chronic rejection of a lung transplant is characterized by a profile of specific autoantibodies. Immunology 2010; 130: 427.
3. Sharples LD, McNeil K, Stewart S, et al. Risk factors for bronchiolitis obliterans: A systematic review of recent publications. J Heart Lung Transplant 2002; 21: 271.
4. Vos R, Vanaudenaerde BM, Geudens N, et al. Pseudomonal airway colonisation: Risk factor for bronchiolitis obliterans syndrome after lung transplantation? Eur Respir J 2008; 31: 1037.
5. Nawrot TS, Vos R, Jacobs L, et al. The impact of traffic air pollution on chronic rejection and mortality after lung transplantation. Thorax 2011; 66: 748.
6. Blondeau K, Mertens V, Vanaudenaerde BA, et al. Gastro-oesophageal reflux and gastric aspiration in lung transplant patients with or without chronic rejection. Eur Respir J 2008; 31: 707.
7. Boehler A, Kesten S, Weder W, et al. Bronchiolitis obliterans after lung transplantation: A review. Chest 1998; 114: 1411.
8. Borthwick LA, McIlroy El, Gorowiec MR, et al. Inflammation and epithelial to mesenchymal transition in lung transplant recipients: Role in dysregulated epithelial wound repair. Am J Transplant 2010; 10: 498.
9. Vanaudenaerde BM, De Vleeschauwer SI, Vos R, et al. The role of the IL23/IL17 axis in bronchiolitis obliterans syndrome after lung transplantation. Am J Transplant 2008; 8: 1911.
10. DiGiovine B, Lynch JP 3rd, Martinez FJ, et al. Bronchoalveolar lavage neutrophilia is associated with obliterative bronchiolitis after lung transplantation: Role of IL-8. J Immunol 1996; 157: 4194.
11. Stewart S, Fishbein MC, Snell GI, et al. Revision of the 1996 working formulation for the standardization of nomenclature in the diagnosis of lung rejection. J Heart Lung Transplant 2007; 26: 1229.
12. Retsema J, Fu W. Macrolides: Structures and microbial targets. Int J Antimicrob Agents 2001; 18: S3.
13. Kobayashi H, Ohgaki N, Takeda H. Therapeutic possibilities for diffuse panbronchiolitis. Int J Antimicrob Agents 1993; 3: S81.
14. Saiman L, Marshall BC, Mayer-Hamblett N, et al. Azithromycin in patients with cystic fibrosis chronically infected with Pseudomonas aeruginosa: A randomized controlled trial. JAMA 2003; 290: 1749.
15. Anwar GA, Bourke SC, Afolabi G, et al. Effects of long-term low-dose azithromycin in patients with non-CF bronchiectasis. Respir Med 2008; 102: 1494.
16. Vos R, Vanaudenaerde BM, Dupont LJ, et al. Transient airway colonization is associated with airway inflammation after lung transplantation. Am J Transplant 2007; 7: 1278.
17. Gielen V, Johnston SL, Edwards MR. Azithromycin induces anti-viral responses in bronchial epithelial cells. Eur Respir J 2010; 36: 646.
18. Weinberg A, Lyu DM, Li S, et al. Incidence and morbidity of human metapneumovirus and other community-acquired respiratory viruses in lung transplant recipients. Transpl Infect Dis 2010; 12: 330.
19. Kai T, Tateda K, Kimura S, et al. A low concentration of azithromycin inhibits the mRNA expression of N-acyl homoserine lactone synthesis enzymes, upstream of lasI or rhlI, in Pseudomonas aeruginosa. Pulm Pharmacol Ther 2009; 22: 483.
20. Hoffmann N, Lee B, Hentzer M, et al. Azithromycin blocks quorum sensing and alginate polymer formation and increases the sensitivity to serum and stationary-growth-phase killing of Pseudomonas aeruginosa and attenuates chronic P. aeruginosa lung infection in Cftr(-/-) mice. Antimicrob Agents Chemother 2007; 51: 3677.
21. Sugimura M, Maseda H, Hanaki H, et al. Macrolide antibiotic-mediated downregulation of MexAB-OprM efflux pump expression in Pseudomonas aeruginosa. Antimicrob Agents Chemother 2008; 52: 4141.
22. Kawamura-Sato K, Iinuma Y, Hasegawa T, et al. Effect of subinhibitory concentrations of macrolides on expression of flagellin in Pseudomonas aeruginosa and Proteus mirabilis. Antimicrob Agents Chemother 2000; 44: 2869.
23. Halldorsson S, Gudjonsson T, Gottfredsson M, et al. Azithromycin maintains airway epithelial integrity during Pseudomonas aeruginosa infection. Am J Respir Cell Mol Biol 2010; 42: 62.
24. Imamura Y, Yanagihara K, Mizuta Y, et al. Azithromycin inhibits MUC5AC production induced by the Pseudomonas aeruginosa autoinducer N-(3-Oxododecanoyl) homoserine lactone in NCI-H292 Cells. Antimicrob Agents Chemother 2004; 48: 3457.
25. Murphy DM, Forrest IA, Corris PA, et al. Azithromycin attenuates effects of lipopolysaccharide on lung allograft bronchial epithelial cells. J Heart Lung Transplant 2008; 27: 1210.
26. Ribeiro CM, Hurd H, Wu Y, et al. Azithromycin treatment alters gene expression in inflammatory, lipid metabolism, and cell cycle pathways in well-differentiated human airway epithelia. PLoS One 2009; 4: e5806.
27. Millrose M, Kruse M, Flick B, et al. Effects of macrolides on proinflammatory epitopes on endothelial cells in vitro. Arch Toxicol 2009; 83: 469.
28. Khair OA, Devalia JL, Abdelaziz MM, et al. Effect of erythromycin on Haemophilus influenzae endotoxin-induced release of IL-6, IL-8 and sICAM-1 by cultured human bronchial epithelial cells. Eur Respir J 1995; 8: 1451.
29. Lin HC, Wang CH, Liu CY, et al. Erythromycin inhibits beta2- integrins (CD11b/CD18) expression, interleukin-8 release and intracellular oxidative metabolism in neutrophils. Respir Med 2000; 94: 654.
30. Vanaudenaerde BM, Wuyts WA, Geudens N, et al. Macrolides inhibit IL17-induced IL8 and 8-isoprostane release from human airway smooth muscle cells. Am J Transplant 2007; 7: 76.
31. Willems-Widyastuti A, Vanaudenaerde BM, Vos R, et al. Azithromycin attenuates fibroblast growth factors induced vascular endothelial growth factor via p38(MAPK) signaling in human airway smoothmuscle cells. Cell Biochem Biophys 2011; [published ahead of print December 29, 2011].
32. Daenas C, Hatziefthimiou AA, Gourgoulianis KI, et al. Azithromycin has a direct relaxant effect on precontracted airway smooth muscle. Eur J Pharmacol 2006; 553: 280.
33. Stamatiou R, Paraskeva E, Boukas K, et al. Azithromycin has an antiproliferative and autophagic effect on airway smooth muscle cells. Eur Respir J 2009; 34: 721.
34. McDonald PJ, Pruul H. Phagocyte uptake and transport of azithromycin. Eur J Clin Microbiol Infect Dis 1991; 10: 828.
35. Meyer M, Huaux F, Gavilanes X, et al. Azithromycin reduces exaggerated cytokine production by M1 alveolar macrophages in cystic fibrosis. Am J Respir Cell Mol Biol 2009; 41: 590.
36. Bosnar M, Cuzic S, Bosnjak B, et al. Azithromycin inhibits macrophage interleukin-1A production through inhibition of AP-1 in lipopolysaccharide- induced murine pulmonary neutrophilia. Int Immunopharmacol 2011; 11: 424.
37. Hodge S, Hodge G, Jersmann H, et al. Azithromycin improves macrophage phagocytic function and expression of mannose receptor in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2008; 178: 139.
38. Yamauchi K, Shibata Y, Kimura T, et al. Azithromycin suppresses interleukin-12p40 expression in lipopolysaccharide and interferongamma stimulated macrophages. Int J Biol Sci 2009; 5: 667.
39. Murphy BS, Sundareshan V, Cory TJ, et al. Azithromycin alters macrophage phenotype. J Antimicrob Chemother 2008; 61: 554.
40. Wilms EB, Touw DJ, Heijerman HG. Pharmacokinetics of azithromycin in plasma, blood, polymorphonuclear neutrophils and sputum during long-term therapy in patients with cystic fibrosis. Ther Drug Monit 2006; 28: 219.
41. Miossec-Bartoli C, Pilatre L, Peyron P, et al. The new ketolideHMR3647 accumulates in the azurophil granules of human polymorphonuclear cells. Antimicrob Agents Chemother 1999; 43: 2457.
42. Tsai WC, Standiford TJ. Immunomodulatory effects of macrolides in the lung: Lessons from in-vitro and in-vivo models. Curr Pharm Des 2004; 10: 3081.
43. Tamaoki J, Kadota J, Takizawa H. Clinical implications of the immunomodulatory effects of macrolides. Am J Med 2004; 117: 5S.
44. Miyazaki M, Zaitsu M, Honjo K, et al. Macrolide antibiotics inhibit prostaglandin E2 synthesis and mRNA expression of prostaglandin synthetic enzymes in human leukocytes. Prostaglandins Leukot Essent Fatty Acids 2003; 69: 229.
45. Mizunoe S, Kadota J, Tokimatsu I, et al. Clarithromycin and azithromycin induce apoptosis of activated lymphocytes via downregulation of Bcl-xL. Int Immunopharmacol 2004; 4: 1201.
46. Khan AA, Slifer TR, Araujo FG, et al. Effect of clarithromycin and azithromycin on production of cytokines by human monocytes. Int J Antimicrob Agents 1999; 11: 121.
47. Stupin Polancec D, Munic VK, Banjanac M, et al. Azithromycin drives in vitro GM-CSF/IL-4-induced differentiation of human blood monocytes toward dendritic-like cells with regulatory properties. J Leukoc Biol 2012; 91: 229.
48. Sugiyama K, Shirai R, Mukae H, et al. Differing effects of clarithromycin and azithromycin on cytokine production by murine dendritic cells. Clin Exp Immunol 2007; 147: 540.
49. Iwamoto S, Kumamoto T, Azuma E, et al. The effect of azithromycin on the maturation and function of murine bone marrow-derived dendritic cells. Clin Exp Immunol 2011; 166: 385.
50. Geudens N, Timmermans L, Vanhooren H, et al. Azithromycin reduces airway inflammation in a murine model of lung ischaemia reperfusion injury. Transpl Int 2008; 21: 688.
51. Remund K, Rechsteiner T, Guo Z, et al. The macrolide clarithromycin inhibits experimental post-transplant bronchiolitis obliterans. Exp Lung Res 2009; 35: 830.
52. Verleden S, Vandooren J, Vos R, et al. Azithromycin decreases MMP-9 expression in the airways of lung transplant recipients. Transpl Immunol 2011; 25: 159.
53. Fietta AM, Meloni F. Lung transplantation: The role of azithromycin in the management of patients with bronchiolitis obliterans syndrome. Curr Med Chem 2008; 15: 716.
54. Frederica M, Nadia S, Monica M, et al. Clinical and immunological evaluation of 12-month azithromycin therapy in chronic lung allograft rejection. Clin Transplant 2011; 25: E381.
55. Glojnaric I, Cuzic S, Erakovic-Haber V, et al. The serum amyloid A response to sterile silver nitrate in mice and its inhibition by dexamethasone and macrolide antibiotics. Int Immunopharmacol 2007; 7: 1544.
56. Wolter J, Seeney S, Bell S, et al. Effect of long term treatment with azithromycin on disease parameters in cystic fibrosis: A randomised trial. Thorax 2002; 57: 212.
57. Togami K, Chono S, Morimoto K. Distribution characteristics of clarithromycin and azithromycin, macrolide anti-microbial agents used for treatment of respiratory infections, in lung epithelial lining fluid and alveolar macrophages. Biopharm Drug Dispos 2011; 32: 389.
58. Zuckerman JM, Qamar F, Bono BR. Macrolides, ketolides, and glycylcyclines: Azithromycin, clarithromycin, telithromycin, tigecycline. Infect Dis Clin North Am 2009; 23: 997, ixYx.
59. Beigelman A, Gunsten S, Mikols CL, et al. Azithromycin attenuates airway inflammation in a noninfectious mouse model of allergic asthma. Chest 2009; 136: 498.
60. Martinez FJ, Curtis JL, Albert R. Role of macrolide therapy in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis 2008; 3: 331.
61. Sarahrudi K, Carretta A, Wisser W, et al. The value of switching from cyclosporine to tacrolimus in the treatment of refractory acute rejection and obliterative bronchiolitis after lung transplantation. Transpl Int 2002; 15: 24.
62. Gerhardt SG, McDyer JF, Girgis RE, et al. Maintenance azithromycin therapy for bronchiolitis obliterans syndrome: Results of a pilot study. Am J Respir Crit Care Med 2003; 168: 121.
63. Verleden GM, Dupont LJ. Azithromycin therapy for patients with bronchiolitis obliterans syndrome after lung transplantation. Transplantation 2004; 77: 1465.
64. Yates B, Murphy DM, Forrest IA, et al. Azithromycin reverses airflow obstruction in established bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 2005; 172: 772.
65. Shitrit D, Bendayan D, Gidon S, et al. Long-term azithromycin use for treatment of bronchiolitis obliterans syndrome in lung transplant recipients. J Heart Lung Transplant 2005; 24: 1440.
66. Verleden GM, Vanaudenaerde BM, Dupont LJ, et al. Azithromycin reduces airway neutrophilia and interleukin-8 in patients with bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 2006; 174: 566.
67. Vos R, Vanaudenaerde BM, Ottevaere A, et al. Long-term azithromycin for bronchiolitis obliterans syndrome: Divide and conquer? J Heart Lung Transplant 2010; 29: 1358.
68. Porhownik NR, Batobara W, Kepron W, et al. Effect of maintenance azithromycin on established bronchiolitis obliterans syndrome in lung transplant patients. Can Respir J 2008; 15: 199.
69. Gottlieb J, Szangolies J, Koehnlein T, et al. Long-term azithromycin for bronchiolitis obliterans syndrome after lung transplantation. Transplantation 2008; 85: 36.
70. Jain R, Hachem RR, Morrell MR, et al. Azithromycin is associated with increased survival in lung transplant recipients with bronchiolitis obliterans syndrome. J Heart Lung Transplant 2010; 29: 531.
71. Benden C, Boehler A. Long-term clarithromycin therapy in the management of lung transplant recipients. Transplantation 2009; 87: 1538.
72. Verleden GM, Dupont LJ, Vanhaecke J, et al. Effect of azithromycin on bronchiectasis and pulmonary function in a heart-lung transplant patient with severe chronic allograft dysfunction: A case report. J Heart Lung Transplant 2005; 24: 1155.
73. de Jongh PA, Vos R, Verleden GM, et al. Thin-section Computed Tomography findings before and after azithromycin treatment of neutrophilic reversible lung allograft dysfunction. Eur Radiol 2011; 21: 2466.
74. Verleden SE, Vos R, Mertens V, et al. Airway protein diversity in bronchiolitis obliterans syndrome after lung transplantation. J Heart Lung Transplant 2011; 30: 667.
75. Mertens V, Blondeau K, Pauwels A, et al. Azithromycin reduces gastroesophageal reflux and aspiration in lung transplant recipients. Dig Dis Sci 2009; 54: 972.
76. Williams TJ, Verleden GM. Azithromycin: A plea for multicenter randomized studies in lung transplantation.AmJ Respir Crit CareMed 2005; 172: 657
77. Vanaudenaerde BM, Vos R, Meyts I, et al. A dichotomy in bronchiolitis obliterans syndrome after lung transplantation revealed by azithromycin therapy. Eur Respir J 2008; 32: 832.
78. Vanaudenaerde BM, Vos R, Meyts I, et al. Macrolide therapy targets a specific phenotype in respiratory medicine: From clinical experience to basic science and back. Inflamm Allergy Drug Targets 2008; 7: 279.
79. Vos R, Vanaudenaerde BM, Verleden SE, et al. A randomised controlled trial of azithromycin to prevent chronic rejection after lung transplantation. Eur Respir J 2011; 37: 164.
80. Brown BA, Griffith DE, Girard W, et al. Relationship of adverse events to serum drug levels in patients receiving high-dose azithromycin for mycobacterial lung disease. Clin Infect Dis 1997; 24: 958.
81. Griffith DE, Brown BA, Girard WM, et al. Azithromycin-containing regimens for treatment of Mycobacterium avium complex lung disease. Clin Infect Dis 2001; 32: 1547.
82. Rubinstein E. Comparative safety of the different macrolide. Int J Antimicrob Agents 2001; 18: 71.
83. Westphal JF. Macrolide-induced clinically relevant drug interactions with cytochrome P-450A (CYP) 3A4: An update focused on clarithromycin, azithromycin and dirithromycin. Br J Clin Pharmacol 2000; 50: 285.
84. Granowitz EV, Tabor KJ, Kirchhoffer JB. Potentially fatal interaction between azithromycin and disopyramide. Pacing Clin Electrophysiol 2000; 23: 1433.
85. Hickey AJ, Lu D, Ashley ED, et al. Inhaled azithromycin therapy. J Aerosol Med 2006; 19: 54.
86. Zhang Y, Wang X, Lin X, et al. High azithromycin loading powders for inhalation and their in vivo evaluation in rats. Int J Pharm 2010; 395: 205.
87. Malhotra-Kumar S, Lammens C, Coenen S, et al. Effect of azithromycin and clarithromycin therapy on pharyngeal carriage of macrolide-resistant streptococci in healthy volunteers: A randomised, double-blind, placebo-controlled study. Lancet 2007; 369: 482.
88. Tait-Kamradt A, Clancy J, Cronan M, et al. mefE is necessary for the erythromycin-resistant M phenotype in Streptococcus pneumoniae. Antimicrob Agents Chemother 1997; 41: 2251.
89. Vanhoof R, Camps K, Carpentier M, et al. 10th Survey of antimicrobial resistance in noninvasive clinical isolates of Streptococcus pneumoniae collected in Belgium during winter 2007-2008. Pathol Biol 2010; 58: 147.
90. Tramper-Stranders GA, Wolfs TF, Fleer A, et al. Maintenance azithromycin treatment in pediatric patients with cystic fibrosis: Longterm outcomes related to macrolide resistance and pulmonary function. Pediatr Infect Dis J 2007; 26: 8.
91. Phaff SJ, Tiddens HA, Verbrugh HA, et al. Macrolide resistance of Staphylococcus aureus and Haemophilus species associated with longterm azithromycin use in cystic fibrosis. J Antimicrob Chemother 2006; 57: 741.
92. Gillis RJ, White KG, Choi KH, et al. Molecular basis of azithromycinresistant Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 2005; 49: 3858.
93. Stover DE, Mangino D. Macrolides: A treatment alternative for bronchiolitis obliterans organizing pneumonia? Chest 2005; 128: 3611.
94. Mann JM, Sha KK, Kline G, et al. World Trade Center dyspnea: Bronchiolitis obliterans with functional improvement: A case report. Am J Ind Med 2005; 48: 225.
95. Khalid M, Al Saghir A, Saleemi S, et al. Azithromycin in bronchiolitis obliterans complicating bone marrow transplantation: A preliminary study. Eur Respir J 2005; 25: 490.
96. Wuyts WA, Willems S, Vos R, et al. Azithromycin reduces pulmonary fibrosis in a bleomycin mouse model. Exp Lung Res 2010; 36: 602.
97. Verleden GM, Vos R, De Vleeschauwer S, et al. Neutrophilic reversible airways dysfunction after liver transplantation: A case report. Transplant Proc 2011; 43: 2078.