3D MRI Modeling of Thin and Spatially Complex Soft Tissue Structures without Shrinkage: Lamprey Myosepta as an Example

3D imaging techniques enable the nondestructive analysis and modeling of complex structures. Among these, MRI exhibits good soft tissue contrast, but is currently less commonly used for nonclinical research than X‐ray CT, even though the latter requires contrast‐staining that shrinks and distorts soft tissues. When the objective is the creation of a realistic and complete 3D model of soft tissue structures, MRI data are more demanding to acquire and visualize and require extensive post‐processing because they comprise noncubic voxels with dimensions that represent a trade‐off between tissue contrast and image resolution. Therefore, thin soft tissue structures with complex spatial configurations are not always visible in a single MRI dataset, so that standard segmentation techniques are not sufficient for their complete visualization. By using the example of the thin and spatially complex connective tissue myosepta in lampreys, we developed a workflow protocol for the selection of the appropriate parameters for the acquisition of MRI data and for the visualization and 3D modeling of soft tissue structures. This protocol includes a novel recursive segmentation technique for supplementing missing data in one dataset with data from another dataset to produce realistic and complete 3D models. Such 3D models are needed for the modeling of dynamic processes, such as the biomechanics of fish locomotion. However, our methodology is applicable to the visualization of any thin soft tissue structures with complex spatial configurations, such as fasciae, aponeuroses, and small blood vessels and nerves, for clinical research and the further exploration of tensegrity. Anat Rec, 301:1745–1763, 2018. © 2018 Wiley Periodicals, Inc.

[1]  Michael R Hamblin,et al.  Down‐regulation of glutatione S‐transferase α 4 (hGSTA4) in the muscle of thermally injured patients is indicative of susceptibility to bacterial infection , 2012, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[2]  D. Homberger The Avian Lingual and Laryngeal Apparatus Within the Context of the Head and Jaw Apparatus, with Comparisons to the Mammalian Condition: Functional Morphology and Biomechanics of Evaporative Cooling, Feeding, Drinking, and Vocalization , 2017 .

[3]  Dominique G. Homberger,et al.  Models and Tests in Functional Morphology: The Significance of Description and Integration , 1988 .

[4]  D Van Loo,et al.  An exploratory study of contrast agents for soft tissue visualization by means of high resolution X‐ray computed tomography imaging , 2013, Journal of microscopy.

[5]  G. Giribet,et al.  Application of magnetic resonance imaging in zoology , 2011, Zoomorphology.

[6]  Michelle L. Osborn,et al.  The shoulder suspension of bipedal humans and the head suspension of quadrupedal cats : a reconstruction of macroevolutionary changes of complex systems based on nautral experiments, comparative anatomy, and biomechanical analyses of extant organisms , 2013 .

[7]  B. Metscher MicroCT for developmental biology: A versatile tool for high‐contrast 3D imaging at histological resolutions , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[8]  M. Knopp,et al.  Performance comparison of 1.5-T endorectal coil MRI with 3.0-T nonendorectal coil MRI in patients with prostate cancer. , 2015, Academic radiology.

[9]  Zheng Liu,et al.  Three-dimensional Imaging and Scanning: Current and Future Applications for Pathology , 2017, Journal of pathology informatics.

[10]  Axel Gelfert,et al.  How to Do Science with Models , 2016 .

[11]  W. Middlesworth,et al.  Ultrasonography/MRI Versus CT for Diagnosing Appendicitis , 2014, Pediatrics.

[12]  J. Epstein,et al.  Rapid 3D Phenotyping of Cardiovascular Development in Mouse Embryos by Micro-CT With Iodine Staining , 2010, Circulation. Cardiovascular imaging.

[13]  C. G. Faulkes,et al.  Digital dissection of the masticatory muscles of the naked mole-rat, Heterocephalus glaber (Mammalia, Rodentia) , 2014, PeerJ.

[14]  W. Bock,et al.  A staining method for gross dissection of vertebrate muscles. , 1972, Anatomischer Anzeiger.

[15]  Miriam A. Hankins,et al.  Effects of Clove Oil as a Euthanasia Agent on Blood Collection Efficiency and Serum Cortisol Levels in Danio rerio. , 2015, Journal of the American Association for Laboratory Animal Science : JAALAS.

[16]  Fernanda Bribiesca-Contreras,et al.  Three-dimensional visualisation of the internal anatomy of the sparrowhawk (Accipiter nisus) forelimb using contrast-enhanced micro-computed tomography , 2017, PeerJ.

[17]  W. Garvey,et al.  Improved Movat pentachrome stain. , 1986, Stain technology.

[18]  R. McN. Alexander,et al.  The orientation of muscle fibres in the myomeres of fishes , 1969, Journal of the Marine Biological Association of the United Kingdom.

[19]  Doreen Schweizer,et al.  Scientific Models In Philosophy Of Science , 2016 .

[20]  Franz Pfeiffer,et al.  Three-dimensional non-destructive soft-tissue visualization with X-ray staining micro-tomography , 2015, Scientific Reports.

[21]  Richard N. Boyd,et al.  Realism, approximate truth, and philosophical method , 1990 .

[22]  V. H. Wallingford The development of organic iodine compounds as x-ray contrast media. , 1953, Journal of the American Pharmaceutical Association. American Pharmaceutical Association.

[23]  Dominique G. Homberger,et al.  The Lingual Apparatus of the African Grey Parrot, Psittacus erithacus Linné (Aves: Psittacidae): Description and Theoretical mechanical Analysis , 1986 .

[24]  A. Peters,et al.  The structure and innervation of the myotomes of the lamprey. , 1961, Journal of anatomy.

[25]  Stephen W Carmichael,et al.  Functional Atlas of the Human Fascial System. , 2016, Clinical anatomy.

[26]  R. Shadwick,et al.  Structure, Kinematics, And Muscle Dynamics In Undulatory Swimming , 2005 .

[27]  Paul M Gignac,et al.  Iodine-enhanced micro-CT imaging: methodological refinements for the study of the soft-tissue anatomy of post-embryonic vertebrates. , 2014, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[28]  J. Soto,et al.  Blunt abdominal trauma: performance of CT without oral contrast material. , 2004, Radiology.

[29]  S. Gemballa,et al.  Locomotory design of ‘cyclostome’ fishes: Spatial arrangement and architecture of myosepta and lamellae , 2001 .

[30]  Gregory T. Baxter,et al.  The Digital Fish Library: Using MRI to Digitize, Database, and Document the Morphological Diversity of Fish , 2012, PloS one.

[31]  Selin Carkaci,et al.  Inflammatory breast cancer: PET/CT, MRI, mammography, and sonography findings , 2008, Breast Cancer Research and Treatment.

[32]  Dominique Adriaens,et al.  Soft tissue discrimination with contrast agents using micro-CT scanning , 2020 .

[33]  S. Faulwetter,et al.  Exploring methods to remove iodine and phosphotungstic acid stains from zoological specimens , 2015 .

[34]  Gregor Harih,et al.  Justification for a 2D versus 3D fingertip finite element model during static contact simulations , 2016, Computer methods in biomechanics and biomedical engineering.

[35]  R. Jong,et al.  Breast MRI as an adjunct to mammography for breast cancer screening in high-risk patients: retrospective review. , 2015, AJR. American journal of roentgenology.

[36]  R Mark Henkelman,et al.  Diffusible iodine‐based contrast‐enhanced computed tomography (diceCT): an emerging tool for rapid, high‐resolution, 3‐D imaging of metazoan soft tissues , 2016, Journal of anatomy.

[37]  S. Halliburton,et al.  The role of advanced reconstruction algorithms in cardiac CT. , 2017, Cardiovascular diagnosis and therapy.

[38]  I. Potter,et al.  Arrangement, histochemistry and fine structure of the connective tissue architecture of lampreys , 1992 .

[39]  C. Neu Displacements under Applied Loading by MRI in Soft Biomaterials and Tissues , 2014 .

[40]  Michelle L. Osborn,et al.  The Human Shoulder Suspension Apparatus: A Causal Explanation for Bilateral Asymmetry and a Fresh Look at the Evolution of Human Bipedality , 2015, Anatomical record.

[41]  Philip G Cox,et al.  Micro-computed tomography with iodine staining resolves the arrangement of muscle fibres. , 2011, Journal of biomechanics.

[42]  Tobias Wang,et al.  Inside Out: Modern Imaging Techniques to Reveal Animal Anatomy , 2011, PloS one.

[43]  S. Iwasaki,et al.  Three-dimensional observation of mouse tongue muscles using micro-computed tomography , 2013, Odontology.

[44]  Marzena Wylezinska,et al.  Speech MRI: morphology and function. , 2014, Physica medica : PM : an international journal devoted to the applications of physics to medicine and biology : official journal of the Italian Association of Biomedical Physics.

[45]  Qimeng Quan,et al.  The value of magnetic resonance imaging in the detection of prostate cancer in patients with previous negative biopsies and elevated prostate-specific antigen levels: a meta-analysis. , 2014, Academic radiology.

[46]  Stephen M. Levin,et al.  Tensegrity: the new biomechanics , 2015 .

[47]  M. Haider,et al.  The expanding role of MRI in prostate cancer. , 2013, AJR. American journal of roentgenology.

[48]  D. B. Baier,et al.  X-ray reconstruction of moving morphology (XROMM): precision, accuracy and applications in comparative biomechanics research. , 2010, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[49]  N. Südkamp,et al.  Long-term T2 and Qualitative MRI Morphology After First-Generation Knee Autologous Chondrocyte Implantation , 2014, The American journal of sports medicine.

[50]  A. Shirazi-Adl,et al.  3D active-passive response of human knee joint in gait is markedly altered when simulated as a planar 2D joint , 2017, Biomechanics and modeling in mechanobiology.

[51]  J. Soto,et al.  Evaluation of a sequential multi-modality imaging algorithm for the diagnosis of acute appendicitis in the pregnant female , 2015, Emergency Radiology.

[52]  J. Jarvis,et al.  Concentration‐dependent specimen shrinkage in iodine‐enhanced microCT , 2013, Journal of anatomy.

[53]  N. Danos,et al.  The musculotendinous system of an anguilliform swimmer: Muscles, myosepta, dermis, and their interconnections in Anguilla rostrata , 2008, Journal of morphology.

[54]  D. Beyersdorff,et al.  MRI morphology of the levator ani muscle, endopelvic fascia, and urethra in women with stress urinary incontinence. , 2006, European journal of obstetrics, gynecology, and reproductive biology.

[55]  R. Mark Henkelman,et al.  Structural Stabilization of Tissue for Embryo Phenotyping Using Micro-CT with Iodine Staining , 2013, PloS one.

[56]  Mark A. Brown,et al.  MRI Basic Principles and Applications: Dale/MRI Basic Principles and Applications , 2015 .

[57]  M. Mitchell Anesthetic Considerations for Amphibians , 2009 .

[58]  C. B. Renaud Lampreys of the world unite. An annotated and illustrated catalogue of lamprey species known to date. , 2011 .

[59]  Peter Aerts,et al.  Volume Shrinkage of Bone, Brain and Muscle Tissue in Sample Preparation for Micro-CT and Light Sheet Fluorescence Microscopy (LSFM) , 2014, Microscopy and Microanalysis.

[60]  L. Braunack-Mayer How to Do Science with Models: A Philosophical Primer , 2017, Annals of science.

[61]  A. Bokulich Models and Explanation , 2017 .

[62]  J. Leipsic,et al.  State of the Art: Iterative CT Reconstruction Techniques. , 2015, Radiology.

[63]  E. Heyderman Histotechnology. A self‐instructional text , 1992 .

[64]  K. Mardon,et al.  Testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials , 2017, Scientific Reports.