Ultrashort-TE MRI longitudinal study and characterization of a chronic model of asthma in mice: Inflammation and bronchial remodeling assessment

NMR in Biomedicine

Volumn 26, Issue 11, 2013, Pages 1451-1459

  Bianchi, Andrea ^a,b   Ozier, Annaïg ^a   Ousova, Olga ^a   Raffard, Gérard ^b   Crémillieux, Yannick ^a,b  

^a CENTRE DE RECHERCHE CARDIO THORACIQUE DE BORDEAUX   (France)

^b CNRS University Bordeaux Segalen   (France)

Author keywords

Asthma; Bronchial remodeling; Inflammation; Lung 1H MRI; UTE

Indexed keywords

ASTHMA; BRONCHIAL REMODELING; FUNCTIONAL PARAMETERS; INFLAMMATION; LONGITUDINAL STUDY; PARENCHYMAL TISSUE; SIGNAL INTENSITIES; UTE;

BIOLOGICAL ORGANS; ESTERS; MAGNETIC RESONANCE IMAGING; MAMMALS; PATHOLOGY;

DISEASES;

METHACHOLINE; OVALBUMIN;

AIRWAY REMODELING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CONTROLLED STUDY; FEMALE; LONGITUDINAL STUDY; MOUSE; NONHUMAN; PLETHYSMOGRAPHY; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SENSITIZATION;

MURINAE; MUS;

ASTHMA; BRONCHIAL REMODELING; INFLAMMATION; LUNG 1H MRI; UTE;

AIRWAY REMODELING; ANIMALS; ASTHMA; BRONCHI; DISEASE MODELS, ANIMAL; FEMALE; MAGNETIC RESONANCE IMAGING; MICE; MICE, INBRED BALB C; PLETHYSMOGRAPHY; PNEUMONIA; REPRODUCIBILITY OF RESULTS; TIME FACTORS;

EID: 84885955172     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.2975     Document Type: Article

References (53)

1. Busse WW, Lemanske RF. Asthma. N. Engl. J. Med. 2001; 344: 350-362.
2. Ozier A, Allard B, Bara I, Girodet P-O, Trian T, Marthan R, Berger P. The pivotal role of airway smooth muscle in asthma pathophysiology. J. Allergy 2011; 2011: 1-20.
3. McParland BE, Macklem PT, Paré PD. Airway wall remodeling: friend or foe? J. Appl. Physiol. 2003; 95: 426-434.
4. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma. From bronchoconstriction to airways inflammation and remodeling. Am. J. Respir. Crit. Care Med. 2000; 161: 1720-1745.
5. Laitinen LA, Heino M, Laitinen A, Kava T, Haahtela T. Damage of the airway epithelium and bronchial reactivity in patients with asthma. Am. Rev. Respir. Dis. 1986; 131: 599-606.
6. Bousquet J, Lacoste JY, Chanez P, Vic P, Godard P, Michel FB. Bronchial elastic fibers in normal subjects and asthmatic patients. Am. J. Respir. Crit. Care Med. 1996; 153: 1648-1654.
7. Dunnill MS, Massarella GR, Anderson JA. A comparison of the quantitative anatomy of the bronchi in normal subjects, in status asthmaticus, in chronic bronchitis, and in emphysema. Thorax 1969; 24: 176-179.
8. Carroll NG, Cooke C, James AL. Bronchial blood vessel dimensions in asthma. Am. J. Respir. Crit. Care M. 1997; 155: 689-695.
9. Carroll N, Elliot J, Morton A, James A. The structure of large and small airways in nonfatal and fatal asthma. Am. Rev. Respir. Dis. 1993; 147: 405-441.
10. Bara I, Ozier A, Tunon de Lara JM, Marthan R, Berger P. Pathophysiology of bronchial smooth muscle remodelling in asthma. Eur. Respir. J. 2010; 36: 1174-1184.
11. Girodet P-O, Ozier A, Bara I, Tunon de Lara JM, Marthan R, Berger P. Airway remodeling in asthma: new mechanisms and potential for pharmacological intervention. Pharmacol. Ther. 2011; 130: 325-337.
12. Henderson RW Jr, Tang L-O, Chu S-J, Tsao S-M, Chiang GKS, Jones F, Jonas M, Pae C, Wang H, Chi EY. A role for cysteinyl leukotrienes in airway remodeling in a mouse asthma model. Am. J. Respir. Crit. Care Med. 2002; 165: 108-116.
13. Gelfand EW. Pro: mice are a good model of human airway disease. Am. J. Respir. Crit. Care Med. 2002; 166: 5-6.
14. Kumar RK, Foster PS. Modeling allergic asthma in mice: pitfalls and opportunities. Am. J. Respir. Cell Mol. Biol. 2002; 27: 267-272.
15. Leong KP, Huston DP. Understanding the pathogenesis of allergic asthma using mouse models. Ann. Allergy Asthma Immunol. 2001; 87: 96-109.
16. Wills-Karp M. Murine models of asthma in understanding immune dysregulation in human asthma. Immunopharmacology 2000; 48: 263-268.
17. Kannan MS, Deshpande DA. Allergic asthma in mice: what determines the phenotype? Am. J. Physiol. Lung Cell. Mol. Physiol. 2003; 285: L29-L31.
18. Kips J, Anderson G, Fredberg JJ, Herz U, Inman MD, Jordana M, Kemeny DM, Lotvall J, Pauwels RA, Plopper CG, Schmidt D, Sterk PJ, Van Oosterhout AJM, Vargaftig BB, Chung KF. Murine models of asthma. Eur. Respir. J. 2003; 22: 374-382.
19. Fulkerson PC, Rothenberg ME, Hogan SP. Building a better mouse model: experimental models of chronic asthma. Clin. Exp. Allergy 2005; 35: 1251-1253.
20. Wagers S. Polarized helium: changing our view of asthma. J. Allergy Clin. Immunol. 2003; 111: 1201-1202.
21. Aysola R, de Lange EE, Castro M, Altes TA. Demonstration of the heterogeneous distribution of asthma in the lungs using CT and hyperpolarized helium-3 MRI. J. Magn. Reson. Imaging 2010; 32: 1379-1387.
22. Ohno Y, Koyama H, Matsumoto K, Onishi Y, Nogami M, Takenaka D, Matsumoto S, Sugimura K. Oxygen-enhanced MRI vs. quantitatively assessed thin-section CT: pulmonary functional loss assessment and clinical stage classification of asthmatics. Eur. J. Radiol. 2011; 77: 85-91.
23. Lederlin M, Ozier A, Montaudon M, Begueret H, Ousova O, Marthan R, Berger P, Laurent F. Airway remodeling in a mouse asthma model assessed by in-vivo respiratory-gated micro-computed tomography. Eur. Radiol. 2010; 20: 128-137.
24. Lederlin M, Ozier A, Dournes G, Ousova O, Girodet P-O, Begueret H, Marthan R, Montaudon M, Laurent F, Berger P. In vivo micro-CT assessment of airway remodeling in a flexible OVA-sensitized murine model of asthma. PLoS One 2012; 7: e48493.
25. Beckmann N, Tigani B, Mazzoni L, Fozard JR. Techniques: magnetic resonance imaging of the lung provides potential for non-invasive preclinical evaluation of drugs. Trends Pharmacol. Sci. 2003; 24: 550-554.
26. 3He MRI. J. Appl. Physiol. 2009; 106: 813-822.
27. 3He MRI. NMR Biomed. 2009; 22: 502-515.
28. 3He MRI in mouse models of asthma. Magn. Reson. Med. 2007; 58: 893-900.
29. Peterson ET, Dai J, Holmes JH, Fain SB. Measurement of lung airways in three dimensions using hyperpolarized helium-3 MRI. Phys. Med. Biol. 2011; 56: 3107-3122.
30. 3He magnetic resonance imaging utility in examining human airway diameter behavior in asthma through comparison with high-resolution computed tomography. Acad. Radiol. 2008; 15: 799-808.
31. 3He diffusion MRI at two time scales: comparison with healthy subjects and patients with COPD. J. Magn. Reson. Imaging 2008; 28: 80-88.
32. Fain S, Schiebler ML, McCormack DG, Parraga G. Imaging of lung function using hyperpolarized helium-3 magnetic resonance imaging: review of current and emerging translational methods and applications. J. Magn. Reson. Imaging 2010; 32: 1398-1408.
33. Beckmann N, Cannet C, Zurbruegg S, Rudin M, Tigani B. Proton MRI of lung parenchyma reflects allergen-induced airway remodeling and endotoxin-aroused hyporesponsiveness: a step toward ventilation studies in spontaneously breathing rats. Magn. Reson. Med. 2004; 52: 258-268.
34. Beckmann N, Tigani B, Ekatodramis D, Borer R, Mazzoni L, Fozard JR. Pulmonary edema induced by allergen challenge in the rat: noninvasive assessment by magnetic resonance imaging. Magn. Reson. Med. 2001; 45: 88-95.
35. Beckmann N, Tigani B, Mazzoni L, Fozard JR. MRI of lung parenchyma in rats and mice using a gradient-echo sequence. NMR Biomed. 2001; 14: 297-306.
36. Blé F-X, Cannet C, Zurbruegg S, Karmouty-Quintana H, Bergmann R, Frossard N, Trifilieff A, Beckmann N. Allergen-induced lung inflammation in actively sensitized mice assessed with MR imaging. Radiology 2008; 248: 834-843.
37. Zurek M, Bessaad A, Cieslar K, Crémillieux Y. Validation of simple and robust protocols for high-resolution lung proton MRI in mice. Magn. Reson. Med. 2010; 64: 401-407.
38. Gewalt SL, Glover GH, Hedlund LW, Cofer GP, Macfall JR, Johnson GA. MR microscopy of the rat lung using projection reconstruction. Magn. Reson. Med. 1993; 29: 99-106.
39. 3He magnetic resonance microscopy of the lung. Magn. Reson. Med. 2001; 45: 365-370.
40. Jackson J, Meyer C, Nishimura D, Macovski A. Selection of a convolution function for Fourier inversion using gridding. IEEE Trans. Med. Imaging 1991; 10: 473-478.
41. Hamelmann E, Schwarze J, Takeda K, Oshiba A, Larsen GL, Irvin CG, Gelfand EW. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 1997; 156: 766-775.
42. Dohi M, Tsukamoto S, Nagahori T, Shinagawa K, Saitoh K, Tanaka Y, Kobayashi S, Tanaka R, To Y, Yamamoto K. Noninvasive system for evaluating the allergen-specific airway response in a murine model of asthma. Lab. Invest. 1999; 79: 1559-1571.
43. Adler A, Cieslewicz G, Irvin CG. Unrestrained plethysmography is an unreliable measure of airway responsiveness in BALB/c and C57BL/6 mice. J. Appl. Physiol. 2004; 97: 286-292.
44. Quintana HK, Cannet C, Schaeublin E, Zurbruegg S, Sugar R, Mazzoni L, Page CP, Fozard JR, Beckmann N. Identification with MRI of the pleura as a major site of the acute inflammatory effects induced by ovalbumin and endotoxin challenge in the airways of the rat. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006; 291: L651-L657.
45. Tigani B, Schaeublin E, Sugar R, Jackson AD, Fozard JR, Beckmann N. Pulmonary inflammation monitored noninvasively by MRI in freely breathing rats. Biochem. Biophys. Res. Commun. 2002; 292: 216-221.
46. Tigani B, Cannet C, Zurbrügg S, Schaeublin E, Mazzoni L, Fozard JR, Beckmann N. Resolution of the oedema associated with allergic pulmonary inflammation in rats assessed noninvasively by magnetic resonance imaging. Br. J. Pharmacol. 2003; 140: 239-246.
47. Beckmann N, Tigani B, Sugar R, Jackson AD, Jones G, Mazzoni L, Fozard JR. Noninvasive detection of endotoxin-induced mucus hypersecretion in rat lung by MRI. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002; 283: L22-L30.
48. Jeffrey PK. Remodeling in asthma and chronic obstructive lung disease. Am. J. Respir. Crit. Care Med. 2001; 164: S28-S38.
49. Walder B, Fontao E, Totsch M, Morel DR. Time and tidal volume-dependent ventilator-induced lung injury in healthy rats. Eur. J. Anaesthesiol. 2005; 22: 785-794.
50. Leigh R, Ellis R, Wattie J, Southam DS, De Hoogh M, Gauldie J, O'Byrne PM, Inman MD. Dysfunction and remodeling of the mouse airway persist after resolution of acute allergen-induced airway inflammation. Am. J. Respir. Cell Mol. Biol. 2002; 27: 526-535.
51. Lundblad LK, Irvin CG, Hantos Z, Sly P, Mitzner W, Bates JHT. Penh is not a measure of airway resistance! Eur. Respir. J. 2007; 30: 805.
52. Lundblad LK, Irvin CG, Adler A, Bates JHT. A reevaluation of the validity of unrestrained plethysmography in mice. J. Appl. Physiol. 2002; 93: 1198-1207.
53. Lambert RK, Paré PD. Lung parenchymal shear modulus, airway wall remodeling, and bronchial hyperresponsiveness. J. Appl. Physiol. 1997; 83: 140-147.