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Quantification of Red Myotomal Muscle Volume and Geometry in the Shortfin Mako Shark (Isurus Oxyrinchus) and the Salmon Shark (L

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Quantification of Red Myotomal Muscle Volume and Geometry in the Shortfin Mako Shark (Isurus Oxyrinchus) and the Salmon Shark (L JOURNAL OF MORPHOLOGY 268:284–292 (2007) Quantification of Red Myotomal Muscle Volume and Geometry in the Shortfin Mako Shark (Isurus oxyrinchus) and the Salmon Shark (Lamna ditropis) using T1-weighted Magnetic Resonance Imaging Cameron N. Perry,2 Daniel P. Cartamil,4 Diego Bernal,5 Chugey A. Sepulveda,6 Rebecca J. Theilmann,2 Jeffrey B. Graham,4 and Lawrence R. Frank1,2,3* 1Center for Scientific Computation in Imaging, University of California, San Diego, La Jolla, California 92093 2Center for Functional Magnetic Resonance Imaging, University of California, San Diego, La Jolla, California 92093 3VA San Diego Health Care System, San Diego, California 92161 4Marine Biology Research Division and Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California 92093-0204 5Department of Biology, University of Massachusetts, Dartmouth, Dartmouth, Massachusetts 02747 6Pfleger Institute of Environmental Research, Oceanside, California 92054 ABSTRACT T1-weighted magnetic resonance imaging tomes of fishes is of key importance in understanding (MRI) in conjunction with image and segmentation anal- specializations in morphology, locomotion, and phys- ysis (i.e., the process of digitally partitioning tissues iology (Graham et al., 1983; Carey et al., 1985; Shad- based on specified MR image characteristics) was eval- wick et al., 1999; Ellerby et al., 2000; Bernal et al., uated as a noninvasive alternative for differentiating 2003; Donley et al., 2004; Sepulveda et al., 2005). muscle fiber types and quantifying the amounts of slow, red aerobic muscle in the shortfin mako shark (Isurus Fishes of particular interest in this respect include oxyrinchus) and the salmon shark (Lamna ditropis). the tunas (Scombridae) and lamnid sharks (Lam- MRI-determinations of red muscle quantity and position nidae) in which a unique anterior and medial posi- made for the mid-body sections of three mako sharks tion of red muscle within the body myotome is one of (73.5–110 cm fork length, FL) are in close agreement several specializations contributing to a capacity for (within the 95% confidence intervals) with data obtained regional endothermy (elevation of red muscle tem- for the same sections by the conventional dissection perature above that of ambient water) (Carey and method involving serial cross-sectioning and volumetric Teal, 1969; Carey et al., 1971; Graham and Dickson, analyses, and with previously reported findings for this 2001; Bernal et al., 2001a; Bernal et al., 2003) and species. The overall distribution of salmon shark red utilization of the unique thunniform swimming muscle as a function of body fork length was also found to be consistent with previously acquired serial dissec- mode (Graham and Dickson, 2004; Shadwick, 2005). tion data for this species; however, MR imaging revealed Past studies of fish muscular anatomy have an anterior shift in peak red muscle cross-sectional area most often utilized the conventional method of se- corresponding to an increase in body mass. Moreover, rial, transverse sectioning of the entire specimen MRI facilitated visualization of the intact and anatomi- followed by the dissection, removal, and either the cally correct relationship of tendon linking the red mus- weighing (Graham et al., 1983) or estimation of cle and the caudal peduncle. This study thus demon- mass by volume displacement (Woodhead et al., strates that MRI is effective in acquiring high-resolution 2001) of the tissue or muscle groups of interest three-dimensional digital data with high contrast within each section. Or, as an option to volume between different fish tissue types. Relative to serial dis- displacement, the surface area of each tissue in section, MRI allows more precise quantification of the position, volume, and other details about the types of muscle within the fish myotome, while conserving speci- Contract grant sponsor: NSF; Contract grant number: DBI- men structural integrity. J. Morphol. 268:284–292, 2007. 0446389; Contact grant sponsor: California Sea Grant; Contract Ó 2007 Wiley-Liss, Inc. grant number: RF-193; Contact grant sponsor: UCSD Academic Senate. KEY WORDS: magnetic resonance imaging; tissue segmentation; red muscle volume; mako shark; salmon *Correspondence to: Lawrence R. Frank, Center for Scientific shark; myotome anatomy Computation in Imaging, UCSD, 9500 Gilman Dr no. 0854, La Jolla, Ca 92093-0854. E-mail: [email protected] The ability to distinguish the two major muscle Published online 13 February 2007 in types (i.e., the aerobic, slow twitch red muscle and Wiley InterScience (www.interscience.wiley.com) the glycolytic, fast-twitch white muscle) in the myo- DOI: 10.1002/jmor.10516 Ó 2007 WILEY-LISS, INC. MRI ANALYSIS OF SHARK RED MUSCLE 285 each section could be calculated using photographs the MR signal and can be accentuated by altering the of the cut surface, followed by mathematical parameters of the MR acquisition (i.e., echo time, extrapolation of tissue volume by multiplying the flip angle) to provide image contrast between tis- surface area by slice thickness. Photography often sues of different types. MRI can acquire fully 3D aids quantitative morphological descriptions of red data at user-defined resolutions (Frank, 2002). The muscle in relation to structural features such as individual volume resolution elements, or voxels, the vertebral column and position along the body are often chosen to be cubical in high resolution axis (Bernal et al., 2003; Graham and Dickson, studies such as the present one to facilitate accu- 2004; Sepulveda et al., 2005). rate measurements during postprocessing. However, serial sectioning and dissection have Two MR signal parameters that are particularly several disadvantages. One of these is the assump- useful for distinguishing different tissues are the tion that objective, visual distinction of different rate at which the RF-excited signal decays, and muscle types for dissection will be possible, which rate at which thermal equilibrium is restored to is not always the case. Further, elucidation of ana- the sample within the large, static field, following tomical detail through careful dissection is excitation. Both of these signal changes are char- extremely labor intensive and, because cutting the acterized by simple exponential functions. The specimen can introduce distortions due to shear rate of thermal equilibrium restoration is charac- and tearing, even the best dissections seldom offer terized by the parameter T1 according to (1-exp(t/ the possibility of reconstructing the specimen to T1). The RF signal decay as a function of time t is visualize basic design features of the intact, three- characterized by the decay rate T2, as exp(-t/T2). dimensional (3D) state. Finally, dissection usually Because of differences in their microstructure, tis- results in nearly complete destruction of speci- sues have different intrinsic T1 and T2 values and mens, precluding further analysis and making can be distinguished on this basis (Frank, 2002). work on rare and valuable material problematic. Image contrast between different tissues is done One alternative method to serial dissection is by accentuating T1 and T2 differences through magnetic resonance imaging (MRI), a noninvasive manipulation of the user-controlled parameters of 3D radiographic modality particularly well-suited the MR image acquisition. Emphasizing T2 varia- for the imaging of soft tissues including muscle tions, called ‘‘T2-weighted imaging,’’ is useful in (Kirschner-Hermanns et al., 1997; Hodgson et al., distinguishing between tissue and fluids. T1-weighted 2006). An earlier MRI study on sharks (Waller imaging is a standard way in which to distinguish et al., 1994) demonstrated its capacity to qualita- different tissues (Kirschner-Hermanns et al., 1997) tively contrast images of cartilage and various soft including muscle (Bonney et al., 1998) and is the tissues including brain, digestive tract, and muscle. method used in the current study. Once these are The objective of the present study is to evaluate the acquired, the data can be digitally partitioned into relative effectiveness of MRI and segmentation virtual, 3D objects whose location and geometry analysis (the process of digitally partitioning tissues (including volumes, cross-sectional areas, relative based upon specific MR image characteristics) in orientation) can be quantitatively assessed. quantifying red muscle position and volume in two species of lamnids, the mako (Isurus oxyrinchus) MATERIALS AND METHODS and the salmon shark (Lamna ditropis). This evalu- Mako Shark ation entails the comparison of results obtained by MRI with results obtained, for the same material, Three juvenile shortfin mako sharks (Isurus oxyrinchus) (fork by conventional dissection, and the comparison of length [FL] 73.5 cm [3.8 kg body mass], 99 cm [9.7 kg body the red muscle data obtained by both of these meth- mass], and 110 cm [13.5 kg body mass]) were captured off the coast of southern California using methods described by Bernal ods with red muscle data recently published for the et al. (2001b), and approved by the Institutional Animal Care mako and salmon sharks (Bernal et al., 2003). and Use Committee, University of California, San Diego. Fol- lowing the use of these specimens in other experimental studies (Bernal et al., 2001b), they were euthanized and frozen whole MRI SYNOPSIS until MRI analysis was performed. Prior to imaging, specimens were thawed and a large section was removed from the mid-
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