In ovo serial skeletal muscle diffusion tractography of the developing chick embryo using DTI: feasibility and correlation with histology

BMC Developmental Biology

E Mark Haacke¹  Jiani Hu¹  Zishu Zhang¹  Yongquan Ye¹  Yan Zhou²  Jia Hua²  Jianrong Xu²  Lianming Wu¹  Zachary DelProposto³  Zien Zhou² 

[1] Department of Radiology, Wayne State University, Detroit, MI, USA;Department of Radiology, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China;Department of Radiology, Henry Ford Hospital, Detroit, MI, USA

关键词: Chick embryo;    Skeletal muscle;    Diffusion tensor imaging;    Magnetic resonance imaging;   

Others  :  1086155
DOI  :  10.1186/1471-213X-12-38

 received in 2012-06-09, accepted in 2012-12-14,  发布年份 2012

【 摘 要 】

Background

Magnetic resonance imaging is a noninvasive method of evaluating embryonic development. Diffusion tensor imaging (DTI), based on the directional diffusivity of water molecules, is an established method of evaluating tissue structure. Yet embryonic motion degrades the in vivo acquisition of long-duration DTI. We used a dual-cooling technique to avoid motion artifact and aimed to investigate whether DTI can be used to monitor chick embryonic skeletal muscle development in ovo, and to investigate the correlation between quantitative DTI parameters fractional anisotropy (FA) and fiber length and quantitative histologic parameters fiber area percentage (FiberArea%) and limb length.

Results

From 84 normally developing chick embryos, 5 were randomly chosen each day from incubation days 5 to 18 and scanned using 3.0 Tesla magnetic resonance imaging. A dual-cooling technique is used before and during imaging. Eggs were cracked for making histological specimen after imaging. 3 eggs were serially imaged from days 5 to 18. We show that skeletal muscle fibers can be tracked in hind limb in DTI beginning with incubation day 8. Our data shows a good positive correlation between quantitative DTI and histologic parameters (FA vs FiberArea%: r= 0.943, p<0.0001; Fiber_length vs Limb_length: r=0.974, p<0.0001). The result of tracked fibers in DTI during incubation corresponds to the development of chick embryonic skeletal muscle as reported in the literature.

Conclusion

Diffusion tensor imaging can provide a noninvasive means of evaluating skeletal muscle development in ovo.

【 授权许可】

   
2012 Zhou et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Rashidi H, Sottile V: The chick embryo: hatching a model for contemporary biomedical research. Bioessays 2009, 31:459-465.
• [2]Pain B, Clark ME, Shen M, Nakazawa H, Sakurai M, Samarut J, Etches RJ: Long-term in vitro culture and characterisation of avian embryonic stem cells with multiple morphogenetic potentialities. Development 1996, 122:2339-2348.
• [3]Wobus AM, Boheler KR: Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev 2005, 85:635-678.
• [4]Bone SN, Johnson GA, Thompson MB: Three-dimensional magnetic resonance microscopy of the developing chick embryo. Invest Radiol 1986, 21:782-787.
• [5]Bain MM, Fagan AJ, Mullin JM, McNaught I, McLean J, Condon B: Noninvasive monitoring of chick development in ovo using a 7T MRI system from day 12 of incubation through to hatching. J Magn Reson Imaging 2007, 26:198-201.
• [6]Boss A, Oppitz M, Wehrl HF, Rossi C, Feuerstein M, Claussen CD, Drews U, Pichler BJ, Schick F: Measurement of T1, T2, and magnetization transfer properties during embryonic development at 7 Tesla using the chicken model. J Magn Reson Imaging 2008, 28:1510-1514.
• [7]Holmes WM, McCabe C, Mullin JM, Condon B, Bain MM: Images in cardiovascular medicine. Noninvasive self-gated magnetic resonance cardiac imaging of developing chick embryos in ovo. Circulation 2008, 117:e346-347.
• [8]Holmes WM, McCabe C, Mullin JM, Condon B, Bain MM: In ovo non-invasive quantification of the myocardial function and mass of chick embryos using magnetic resonance imaging. NMR Biomed 2009, 22:745-752.
• [9]Coen M, Wevers RA, Lindon JC, Blom HJ: High-resolution 1H NMR spectroscopic investigation of a chick embryo model of neural tube development. Magn Reson Chem 2009, 47:S62-S67.
• [10]Peebles DM, Dixon JC, Thornton JS, Cady EB, Priest A, Miller SL, Blanco CE, Mulder TL, Ordidge RJ, Rodeck CH: Magnetic resonance proton spectroscopy and diffusion weighted imaging of chick embryo brain in ovo. Dev Brain Res 2003, 141:101-107.
• [11]Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, Chabriat H: Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 2001, 13:534-546.
• [12]Fan RH, Does MD: Compartmental relaxation and diffusion tensor imaging measurements in vivo in lambda-carrageenan-induced edema in rat skeletal muscle. NMR Biomed 2008, 21:566-573.
• [13]Christ B, Brand-Saberi B: Limb muscle development. Int J Dev Biol 2002, 46:905-914.
• [14]Halevy O, Piestun Y, Rozenboim I, Yablonka-Reuveni Z: In ovo exposure to monochromatic green light promotes skeletal muscle cell proliferation and affects myofiber growth in posthatch chicks. Am J Physiol Regul Integr Comp Physiol 2006, 290:R1062-R1070.
• [15]Shimada Y, Fischman DA, Moscona AA: The fine structure of embryonic chick skeletal muscle cells differentiated in vitro. J Cell Biol 1967, 35:445-453.
• [16]Buckingham M, Bajard L, Chang T, Daubas P, Hadchouel J, Meilhac S, Montarras D, Rocancourt D, Relaix F: The formation of skeletal muscle: from somite to limb. J Anat 2003, 202:59-68.
• [17]Stockdale FE: Mechanisms of formation of muscle fiber types. Cell Struct Funct 1997, 22:37-43.
• [18]Bober E, Franz T, Arnold HH, Gruss P, Tremblay P: Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 1994, 120:603-612.
• [19]Rudnicki MA, Schnegelsberg PN, Stead RH, Braun T, Arnold HH, Jaenisch R: MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 1993, 75:1351-1359.
• [20]Tyszka JM, Readhead C, Bearer EL, Pautler RG, Jacobs RE: Statistical diffusion tensor histology reveals regional dysmyelination effects in the shiverer mouse mutant. Neuroimage 2006, 29:1058-1065.
• [21]Herrera JJ, Chacko T, Narayana PA: Histological correlation of diffusion tensor imaging metrics in experimental spinal cord injury. J Neurosci Res 2008, 86:443-447.