- Email: [email protected]
In vivo magnetic resonance micro-imaging of the human toe at 3 tesla
Magnetic Resonance Imaging 19 (2001) 1235–1238
Technical Note
In vivo magnetic resonance micro-imaging of the human toe at 3 tesla Jo´zsef Constantin Sze´lesa, Bence Csapo´a, Markus Klarho¨ferb, Csilla Bala´ssya, Raschid Hodaa, Andreas Bergb, Michael Rodenc, Peter Polterauera, Werner Waldha¨uslc, Ewald Moserb,d,* a
Department of Vascular Surgery, University of Vienna Medical School, Vienna, Austria b Institute for Medical Physics, University of Vienna, Vienna, Austria c Department of Internal Medicine III, Division of Endocrinology and Metabolism, University of Vienna Medical School, Vienna, Austria d Department of Radiology, University of Vienna Medical School, Vienna, Austria
Abstract The feasibility of in vivo high-resolution magnetic resonance micro-imaging of fine anatomic structures of human toes was tested. Five healthy subjects were investigated on an experimental 3 Tesla whole body scanner, using standard 3D gradient echo sequences. A radio-frequency surface coil was used for signal detection. Feet, toes and surface coil were comfortably fixed using a home built device for positioning and reduction of motion artifacts. The spatial resolution of 117 ⫻ 313 ⫻ 375 m3 allowed detailed visualization of anatomic structures like skin layers, vessels and nerves. In addition, oval structures with diameters ranging from 500 to 1000 m were observed in all subjects, which could represent the sensory nerve endings of Vater-Pacinian bodies. Thus, high resolution MR micro-imaging at 3 Tesla may provide improved morphologic information in distal extremities of humans in vivo. © 2001 Elsevier Science Inc. All rights reserved. Keywords: MRI; Micro-imaging; Human toe; Vater-Pacinian bodies; 3 Tesla
1. Introduction Since its first application magnetic resonance imaging (MRI) rapidly developed into one of the most versatile diagnostic tools in medicine, yielding far better contrast in soft tissues than other imaging modalities like conventional X-ray, or computed tomography. Both the fast progress in magnetic resonance (MR) and computer technology as well as the growing interest in better spatial resolution led to MR microscopy, a field with many promising prospects. MR imaging at spatial resolutions better than those achievable with the naked human eye (i.e., better than 100 –200 m) are referred to as MR micro-imaging or microscopy, depending on voxel size [1]. In animal and plant experiments, or investigations on cell cultures, exceptionally high resolutions of 4 –10 m have been obtained [2,3]. These experiments require ultrahigh magnetic field strengths and, therefore, small bore magnets to achieve reasonable signal-to-noise ratios (SNR). Unfortunately, such equipment is inappropriate * Corresponding author. Tel.: ⫹431-4277-60713; fax: ⫹431-42779607. E-mail address: [email protected] (E. Moser).
for human medical applications in vivo. In human skin studies on whole body MRI systems spatial resolutions from 19 ⫻ 78 ⫻ 800 m3 to 156 ⫻ 936 ⫻ 1500 m3 have been reported [4 – 6]. High-resolution imaging of human extremities so far commonly concentrated on the human finger [7–9], whereas MRI investigations of the human toe were conducted only at field strengths of 1–1.5 T for the description of rare morphologic disorders [10 – 13]. The present study focused on designing a method to investigate the structure and fine morphology of the distal parts of human extremities. A number of pathologies manifest in this anatomic region whose early non-invasive detection could carry particular significance in preservation of general health condition by enabling early therapy for prevention of associated complications. Consequently, this study was designed to evaluate the feasibility and practicability of in vivo high resolution MR investigation of fine anatomic details within the human toe on high-field whole body MRI equipment. In particular, attempts were made to detect Vater-Pacini sensory nerve endings [14] in healthy subjects to define normal MR based anatomy as a basis for future in vivo exploration of pathology in this confined region by MR microimaging.
0730-725X/01/$ – see front matter © 2001 Elsevier Science Inc. All rights reserved. PII: S 0 7 3 0 - 7 2 5 X ( 0 1 ) 0 0 4 6 1 - 1
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J. Constantin Sze´les et al. / Magnetic Resonance Imaging 19 (2001) 1235–1238
Fig. 1. Foot holder applied for toe measurements. The device consists of a plastic plate at 20° of the vertical, with a wedge supporting it in the center from the back. Four plastic screws pushing against the gradient wall provide further fixation. Soft foam padding of different size covers the feet, while the toes are fixed with a wide Velcro tape. The surface coil is also fastened with the same Velcro tape allowing adequate freedom in positioning.
2. Material and methods Big toes of five healthy individuals (male/female: 4/1, 25– 46 years) were imaged at 3 T. Measurements were performed on a Bruker Medspec 30/80 (Bruker Medical Inc., Ettlingen, Germany), equipped with an asymmetric head gradient system B-GA33 (inner diameter 33 cm, Gmax ⫽ 29 mT/m) and a small radio-frequency (rf) surface coil (coil diameter 3 cm). A custom built positioning device was constructed (Fig. 1), enabling exact positioning and fixation of feet and surface coil, markedly reducing motion artifacts and also compensating for different foot shapes and sizes. Imaging was carried out on subjects lying in supine position with their feet placed comfortably in the bore of the gradient system. A standard 3D gradient echo sequence with the following parameters was used for imaging: FOV: 30 ⫻ 30 ⫻ 18 mm3, matrix: 256 ⫻ 96 ⫻ 48, spatial resolution: 117 ⫻ 313 ⫻ 625 m3, TR: 100 ms, TE: 10 ms, flip angle 25°, aquisition bandwidth: 50 kHz, number of averages: 4, total acquisition time: 30.7 min. The Ethics Committee of the Medical School of the University of Vienna and the General Hospital of Vienna (EK-No. 394/ 97) approved the protocol.
3. Results High-resolution 3 T MR images permit identification not only of macro-anatomic but also of some finer structures. Progressing from the skin toward deeper tissues the following structures were found (see Fig. 2): hyperintense epidermis (e); relatively homogeneous, but less signal-intensive dermis (d), and the heterogeneous, but predominantly hyperintense subcutis, whose intensity is determined by the proportion and signal quality of the anatomic structures
Fig. 2. Single sagittal slice of a 3D GE image data set of the human toe. The spatial resolution achieved was 117 ⫻ 313 ⫻ 625 m3 and allowed the identification of several anatomic structures: e-epidermis; d-dermis; isinterphalangeal space; c-cartilage; bm-bone marrow; n-nerve; v-vessel. Arrows point at structures most likely representing Vater Pacinian corpuscles. The thin cartilage lining of about 300 m thickness, the interphalangeal joint and the narrow articular space are also clearly visible.
within (vessels, nerves and their components, tendons, connective tissue trabeculae and fat). The epidermis has a varying thickness between 400 and 800 m, while the dermis displays an average transverse thickness of 7003000 m. A precapillary vessel of the subcutis is labeled (v), which is seen as a line of hyperintensity with a diameter of about 600 m. Numerous hyperintense fat cells and the markedly hypointense connective tissue trabeculae separating them occupy major parts of the subcutis. The interphalangeal joint (is) is seen with its narrow articular cavity and fine hyperintense cartilage (c), covering the adjoining articular surfaces. The large structures of the cortical bone are seen in negative contrast (i.e., lack of signal in signal rich surroundings) and also the fine trabeculae of the hyperintense structure of the bone marrow (bm) are visible. Additionally, oblong objects of 500-1000 m in diameter, at increased signal intensity are recurring observations in all investigated subjects, mostly located close to joints, or in the immediate vicinity of vessels. In some cases they seem to form small clusters of 2– 4 per image. In selected slices a connecting hyperintense stem is visible between the identified bodies and a longitudinal structure of intermediate signal intensity (a nerve) running nearby. Based on the known morphology and local visualization these structures could represent Vater Pacini corpuscles.
J. Constantin Sze´ les et al. / Magnetic Resonance Imaging 19 (2001) 1235–1238
4. Discussion Despite recent progress in in-vivo MR microscopy, the term MR microscopy remains somewhat ambiguous as it is not clearly defined. Isotropic spatial resolution of below 100 m is limited mostly to in vitro, or special in vivo animal or plant investigations, but are not generally available for human studies. Thus any high-resolution studies not achieving such high in plane resolutions, should rather be termed MR micro-imaging. The feasibility of MR micro-imaging for small structures of the toe is demonstrated in this study. In order to minimize motion artifacts a special fixation device was constructed which allows exact positioning of rf coil and feet of different sizes and shapes. Such a supporting device not only has to provide proper fixation, but will also be required to prevent any ischemic injuries during the measurements, particularly in patients suffering from occlusive vascular disease. On all images acquired the standard macro-anatomy of the human toes is identifiable with certainty, such as skeletal structures and the different layers of the skin— epidermis, dermis, subcutis. The high proportion of keratinocytes in the epidermis in various stages of their development are responsible for the bright signal [4]. Within the subcutis the ample amount of fat cells gather in smaller or larger hyperintense groups, separated by hypointense connective tissue trabeculas. As water in connective tissue of the dermis and subcutis is tightly bound it has too short T2 values to be visible with conventional imaging protocols. Small vessels of the toes running in the subcutis are also well detectable and give an intermediate signal, as the strong signal intensity caused by the high proton density of blood is somewhat decreased due to flow related dephasing effects. These vessels can serve as important landmarks for orientation and detection of other, smaller structures. In comparison, peripheral nerves running mostly along larger vessels yield only a slightly higher signal intensity than their surroundings and so are difficult to identify. Different parts of the long bones in the toes are also observable. The cortical substance (stratum compactum, consisting of predominantly calcium-hydroxyapatite crystals) gives hardly any signal with the applied pulse-sequences, and thus appears dark in all images. In sharp contrast bone marrow appears bright, demonstrating an inner structure of high signal intensity stroma (bone marrow) and low intensity trabeculae. The articulating joint between two adjacent bones is also clearly presented, as the articular cartilage gives a hyperintense signal, whereas the intraarticular liquid provides only intermediate signal intensity. The MR presentation of the described structures corresponds well to that observed by high resolution studies of the upper extremity [7]. Vater-Pacini sensory bodies in the subcutis of distal human extremities are known to be terminal nerve endings responsible for sensation of vibration [15]. Their inner structure consists of a terminal nerve ending with its own capillary supply, surrounded by a capsule of gel-like material [16] of high water content, separated into two distinct
1237
compartments. The inner core is built up from up to 20 concentric Schwann cell membranes, while the outer core of similar arrangement is continuous with the perineurinum of the innervating axon, but with up to 70 layers. Their size ranges between 50 –100 m [17] and 1500 –2000 m [18] depending on their location. Their special morphology (compartments of high water content) results in hyperintense presentation of these small oblong structures in the typical location (i.e., close to vessels and joints) on applied MR micro-images, indicating the educible location of Vater-Pacini bodies. This applies in particular to structures that are apparent to be connecting with a narrow stem to an adjoining peripheral nerve. Since the largest diameter of the sensory bodies and the direction of their stem do not always fall into the same plane, their simultaneous presentation within an image can not always be expected. Alternatively several other structures have to be considered as possible candidates for differential diagnosis. These include Meissner bodies (⬃40 –100 m in diameter) and Golgi-Mazzoni bodies (similar to Vater-Pacini bodies but without outer core: 20 – 40 m in size). Differentiation is predominantly based on size, as all these structures are markedly smaller than Vater-Pacinian bodies. Despite the fact that the nominal resolution is better than the expected diameter of neural structures investigated, it is estimated that for the positive identification of any homogeneous structure on a MR image a minimal coverage of at least 1 pixel, for the identification of shape at least 6 – 8 pixels are needed. The identification of the latter, however, is accessible by the resolution of 117 ⫻ 313 ⫻ 375 m3 achieved in this study. In conclusion, MR micro-imaging offers the potential of in vivo visualization of small anatomic structures at a resolution and with contrast not achievable by other imaging modalities. To achieve this, special instrumentation high field strength and strong gradients are required. Visualization of fine structures of the human toe by MR microimaging may become a helpful tool for strengthening the diagnosis of some diseases including diabetic angio- and neuropathy, Raynaud’s phenomenon, alcoholic neuropathy as well as spondyloarthropathy and tophaceous gout, or other systemic diseases presenting in the lower extremities, in particular as 3 Tesla whole body systems are currently tested for routine clinical work.
Acknowledgments Grant sponsor: Fonds zur Fo¨ rderung der wissenschaftlichen Forschung (FWF), grant number P12041MED.
References [1] Lauterbur P. MR microscopy using projection reconstruction. In: Blu¨ mich B, Kuhn W, editors. Magnetic resonance microscopy. Weinheim: VCH, 1992. p. 3–25.
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J. Constantin Sze´ les et al. / Magnetic Resonance Imaging 19 (2001) 1235–1238
[2] Aguayo JB, Blackband SJ, Schoeniger J. Nuclear Magnetic Resonance imaging in a single cell. Nature 1986;322:190 –1. [3] Cho ZH, Ahn CB, Juh SC, Lee HK, Jacobs RE, Lee S, Yi JH, Jo JM. Nuclear magnetic resonance microscopy with 4-m resolution: theoretical study and experimental results. Med Phys 1989;15:815–24. [4] Song HK, Wehrli FW, Ma J. In vivo MR microscopy of the human skin. Magn Reson Med 1997;37:85–91. [5] Richard SB, Querleux BG, Bittoun J. Characterization of the skin in vivo by high resolution magnetic resonance imaging: water behavior and age-related effects. J Invest Dermatol 1993;100:705–9. [6] Ablett S, Burdett NG, Carpenter TA, Hall LD, Salter DC. Short echo time MRI enables visualisation of the natural state of human stratum corneum water in vivo. Magn Res Imaging 1996;14:357– 60. [7] Blackband SJ, Chakrabarti I, Gibbs P, Buckley DL, Horsman A. Fingers: three-dimensional MR imaging, and angiography with a local gradient coil. Radiology 1994;190:895–9. [8] Erickson SJ, Kneeland JB, Middleton WD, Jesmanowicz A, Hyde J, Lawson TL, Foley WD. MR imaging of the finger: correlation with normal anatomic sections. Am J Roentgenol 1989;152:1013–9. [9] Klarho¨ fer M, Csapo B, Balassy C, Szeles JC, Moser E. Blood flow velocities in the human finger. Magn Reson Med 2001;45:716 –19.
[10] Drape JL, Idy-Peretti I, Goettmann S, Guerin-Surville H, Bittoun J. Standard and high resolution magnetic resonance imaging of glomus tumors of toes and fingertips. J Am Acad Dermatol 1996;35:550 –5. [11] Zanetti M, Ledermann T, Zollinger H, Hodler J. Efficacy of MR imaging in patients suspected of having Morton’s neuroma. Am J Roentgenol 1997;168:529 –32. [12] D’Souza D, McDiarmid J, Tickle C. A polydactylous human foot with ‘double-dorsal’ toes. J Anat 1998;193:121–30. [13] Katz JB. Progressive macrodactyly. J Foot Ankle Surg 1999;38:143– 6. [14] Vater A. Dissertatio de consensu partium corporis humani. Haller. isputationum Anatomicarum selectarum. Gottingaeh, vol. 2, pp. 953– 72; 1741. [15] Iggo A. Is the physiology of cutaneous receptors determined by morphology? Prog Brain Res 1976;43:15–31. [16] Fawcett DW, Jensh RP. Bloom & Fawcett: concise histology. New York: Chapman and Hall, 1997. p. 179. [17] Bistevins R, Awad E. A structure and ultrastructure of mechanoreceptors at the human musculotendinous junction. Arch Phys Med Rehabil 1981;62:74 – 83. [18] Stark B Carlstedt T, Hallin RG. Distribution of human Pacinian corpuscules in the hand. A cadaver study. Br J Hand Surg 1998;23: 370 –2.
Technical Note
In vivo magnetic resonance micro-imaging of the human toe at 3 tesla Jo´zsef Constantin Sze´lesa, Bence Csapo´a, Markus Klarho¨ferb, Csilla Bala´ssya, Raschid Hodaa, Andreas Bergb, Michael Rodenc, Peter Polterauera, Werner Waldha¨uslc, Ewald Moserb,d,* a
Department of Vascular Surgery, University of Vienna Medical School, Vienna, Austria b Institute for Medical Physics, University of Vienna, Vienna, Austria c Department of Internal Medicine III, Division of Endocrinology and Metabolism, University of Vienna Medical School, Vienna, Austria d Department of Radiology, University of Vienna Medical School, Vienna, Austria
Abstract The feasibility of in vivo high-resolution magnetic resonance micro-imaging of fine anatomic structures of human toes was tested. Five healthy subjects were investigated on an experimental 3 Tesla whole body scanner, using standard 3D gradient echo sequences. A radio-frequency surface coil was used for signal detection. Feet, toes and surface coil were comfortably fixed using a home built device for positioning and reduction of motion artifacts. The spatial resolution of 117 ⫻ 313 ⫻ 375 m3 allowed detailed visualization of anatomic structures like skin layers, vessels and nerves. In addition, oval structures with diameters ranging from 500 to 1000 m were observed in all subjects, which could represent the sensory nerve endings of Vater-Pacinian bodies. Thus, high resolution MR micro-imaging at 3 Tesla may provide improved morphologic information in distal extremities of humans in vivo. © 2001 Elsevier Science Inc. All rights reserved. Keywords: MRI; Micro-imaging; Human toe; Vater-Pacinian bodies; 3 Tesla
1. Introduction Since its first application magnetic resonance imaging (MRI) rapidly developed into one of the most versatile diagnostic tools in medicine, yielding far better contrast in soft tissues than other imaging modalities like conventional X-ray, or computed tomography. Both the fast progress in magnetic resonance (MR) and computer technology as well as the growing interest in better spatial resolution led to MR microscopy, a field with many promising prospects. MR imaging at spatial resolutions better than those achievable with the naked human eye (i.e., better than 100 –200 m) are referred to as MR micro-imaging or microscopy, depending on voxel size [1]. In animal and plant experiments, or investigations on cell cultures, exceptionally high resolutions of 4 –10 m have been obtained [2,3]. These experiments require ultrahigh magnetic field strengths and, therefore, small bore magnets to achieve reasonable signal-to-noise ratios (SNR). Unfortunately, such equipment is inappropriate * Corresponding author. Tel.: ⫹431-4277-60713; fax: ⫹431-42779607. E-mail address: [email protected] (E. Moser).
for human medical applications in vivo. In human skin studies on whole body MRI systems spatial resolutions from 19 ⫻ 78 ⫻ 800 m3 to 156 ⫻ 936 ⫻ 1500 m3 have been reported [4 – 6]. High-resolution imaging of human extremities so far commonly concentrated on the human finger [7–9], whereas MRI investigations of the human toe were conducted only at field strengths of 1–1.5 T for the description of rare morphologic disorders [10 – 13]. The present study focused on designing a method to investigate the structure and fine morphology of the distal parts of human extremities. A number of pathologies manifest in this anatomic region whose early non-invasive detection could carry particular significance in preservation of general health condition by enabling early therapy for prevention of associated complications. Consequently, this study was designed to evaluate the feasibility and practicability of in vivo high resolution MR investigation of fine anatomic details within the human toe on high-field whole body MRI equipment. In particular, attempts were made to detect Vater-Pacini sensory nerve endings [14] in healthy subjects to define normal MR based anatomy as a basis for future in vivo exploration of pathology in this confined region by MR microimaging.
0730-725X/01/$ – see front matter © 2001 Elsevier Science Inc. All rights reserved. PII: S 0 7 3 0 - 7 2 5 X ( 0 1 ) 0 0 4 6 1 - 1
1236
J. Constantin Sze´les et al. / Magnetic Resonance Imaging 19 (2001) 1235–1238
Fig. 1. Foot holder applied for toe measurements. The device consists of a plastic plate at 20° of the vertical, with a wedge supporting it in the center from the back. Four plastic screws pushing against the gradient wall provide further fixation. Soft foam padding of different size covers the feet, while the toes are fixed with a wide Velcro tape. The surface coil is also fastened with the same Velcro tape allowing adequate freedom in positioning.
2. Material and methods Big toes of five healthy individuals (male/female: 4/1, 25– 46 years) were imaged at 3 T. Measurements were performed on a Bruker Medspec 30/80 (Bruker Medical Inc., Ettlingen, Germany), equipped with an asymmetric head gradient system B-GA33 (inner diameter 33 cm, Gmax ⫽ 29 mT/m) and a small radio-frequency (rf) surface coil (coil diameter 3 cm). A custom built positioning device was constructed (Fig. 1), enabling exact positioning and fixation of feet and surface coil, markedly reducing motion artifacts and also compensating for different foot shapes and sizes. Imaging was carried out on subjects lying in supine position with their feet placed comfortably in the bore of the gradient system. A standard 3D gradient echo sequence with the following parameters was used for imaging: FOV: 30 ⫻ 30 ⫻ 18 mm3, matrix: 256 ⫻ 96 ⫻ 48, spatial resolution: 117 ⫻ 313 ⫻ 625 m3, TR: 100 ms, TE: 10 ms, flip angle 25°, aquisition bandwidth: 50 kHz, number of averages: 4, total acquisition time: 30.7 min. The Ethics Committee of the Medical School of the University of Vienna and the General Hospital of Vienna (EK-No. 394/ 97) approved the protocol.
3. Results High-resolution 3 T MR images permit identification not only of macro-anatomic but also of some finer structures. Progressing from the skin toward deeper tissues the following structures were found (see Fig. 2): hyperintense epidermis (e); relatively homogeneous, but less signal-intensive dermis (d), and the heterogeneous, but predominantly hyperintense subcutis, whose intensity is determined by the proportion and signal quality of the anatomic structures
Fig. 2. Single sagittal slice of a 3D GE image data set of the human toe. The spatial resolution achieved was 117 ⫻ 313 ⫻ 625 m3 and allowed the identification of several anatomic structures: e-epidermis; d-dermis; isinterphalangeal space; c-cartilage; bm-bone marrow; n-nerve; v-vessel. Arrows point at structures most likely representing Vater Pacinian corpuscles. The thin cartilage lining of about 300 m thickness, the interphalangeal joint and the narrow articular space are also clearly visible.
within (vessels, nerves and their components, tendons, connective tissue trabeculae and fat). The epidermis has a varying thickness between 400 and 800 m, while the dermis displays an average transverse thickness of 7003000 m. A precapillary vessel of the subcutis is labeled (v), which is seen as a line of hyperintensity with a diameter of about 600 m. Numerous hyperintense fat cells and the markedly hypointense connective tissue trabeculae separating them occupy major parts of the subcutis. The interphalangeal joint (is) is seen with its narrow articular cavity and fine hyperintense cartilage (c), covering the adjoining articular surfaces. The large structures of the cortical bone are seen in negative contrast (i.e., lack of signal in signal rich surroundings) and also the fine trabeculae of the hyperintense structure of the bone marrow (bm) are visible. Additionally, oblong objects of 500-1000 m in diameter, at increased signal intensity are recurring observations in all investigated subjects, mostly located close to joints, or in the immediate vicinity of vessels. In some cases they seem to form small clusters of 2– 4 per image. In selected slices a connecting hyperintense stem is visible between the identified bodies and a longitudinal structure of intermediate signal intensity (a nerve) running nearby. Based on the known morphology and local visualization these structures could represent Vater Pacini corpuscles.
J. Constantin Sze´ les et al. / Magnetic Resonance Imaging 19 (2001) 1235–1238
4. Discussion Despite recent progress in in-vivo MR microscopy, the term MR microscopy remains somewhat ambiguous as it is not clearly defined. Isotropic spatial resolution of below 100 m is limited mostly to in vitro, or special in vivo animal or plant investigations, but are not generally available for human studies. Thus any high-resolution studies not achieving such high in plane resolutions, should rather be termed MR micro-imaging. The feasibility of MR micro-imaging for small structures of the toe is demonstrated in this study. In order to minimize motion artifacts a special fixation device was constructed which allows exact positioning of rf coil and feet of different sizes and shapes. Such a supporting device not only has to provide proper fixation, but will also be required to prevent any ischemic injuries during the measurements, particularly in patients suffering from occlusive vascular disease. On all images acquired the standard macro-anatomy of the human toes is identifiable with certainty, such as skeletal structures and the different layers of the skin— epidermis, dermis, subcutis. The high proportion of keratinocytes in the epidermis in various stages of their development are responsible for the bright signal [4]. Within the subcutis the ample amount of fat cells gather in smaller or larger hyperintense groups, separated by hypointense connective tissue trabeculas. As water in connective tissue of the dermis and subcutis is tightly bound it has too short T2 values to be visible with conventional imaging protocols. Small vessels of the toes running in the subcutis are also well detectable and give an intermediate signal, as the strong signal intensity caused by the high proton density of blood is somewhat decreased due to flow related dephasing effects. These vessels can serve as important landmarks for orientation and detection of other, smaller structures. In comparison, peripheral nerves running mostly along larger vessels yield only a slightly higher signal intensity than their surroundings and so are difficult to identify. Different parts of the long bones in the toes are also observable. The cortical substance (stratum compactum, consisting of predominantly calcium-hydroxyapatite crystals) gives hardly any signal with the applied pulse-sequences, and thus appears dark in all images. In sharp contrast bone marrow appears bright, demonstrating an inner structure of high signal intensity stroma (bone marrow) and low intensity trabeculae. The articulating joint between two adjacent bones is also clearly presented, as the articular cartilage gives a hyperintense signal, whereas the intraarticular liquid provides only intermediate signal intensity. The MR presentation of the described structures corresponds well to that observed by high resolution studies of the upper extremity [7]. Vater-Pacini sensory bodies in the subcutis of distal human extremities are known to be terminal nerve endings responsible for sensation of vibration [15]. Their inner structure consists of a terminal nerve ending with its own capillary supply, surrounded by a capsule of gel-like material [16] of high water content, separated into two distinct
1237
compartments. The inner core is built up from up to 20 concentric Schwann cell membranes, while the outer core of similar arrangement is continuous with the perineurinum of the innervating axon, but with up to 70 layers. Their size ranges between 50 –100 m [17] and 1500 –2000 m [18] depending on their location. Their special morphology (compartments of high water content) results in hyperintense presentation of these small oblong structures in the typical location (i.e., close to vessels and joints) on applied MR micro-images, indicating the educible location of Vater-Pacini bodies. This applies in particular to structures that are apparent to be connecting with a narrow stem to an adjoining peripheral nerve. Since the largest diameter of the sensory bodies and the direction of their stem do not always fall into the same plane, their simultaneous presentation within an image can not always be expected. Alternatively several other structures have to be considered as possible candidates for differential diagnosis. These include Meissner bodies (⬃40 –100 m in diameter) and Golgi-Mazzoni bodies (similar to Vater-Pacini bodies but without outer core: 20 – 40 m in size). Differentiation is predominantly based on size, as all these structures are markedly smaller than Vater-Pacinian bodies. Despite the fact that the nominal resolution is better than the expected diameter of neural structures investigated, it is estimated that for the positive identification of any homogeneous structure on a MR image a minimal coverage of at least 1 pixel, for the identification of shape at least 6 – 8 pixels are needed. The identification of the latter, however, is accessible by the resolution of 117 ⫻ 313 ⫻ 375 m3 achieved in this study. In conclusion, MR micro-imaging offers the potential of in vivo visualization of small anatomic structures at a resolution and with contrast not achievable by other imaging modalities. To achieve this, special instrumentation high field strength and strong gradients are required. Visualization of fine structures of the human toe by MR microimaging may become a helpful tool for strengthening the diagnosis of some diseases including diabetic angio- and neuropathy, Raynaud’s phenomenon, alcoholic neuropathy as well as spondyloarthropathy and tophaceous gout, or other systemic diseases presenting in the lower extremities, in particular as 3 Tesla whole body systems are currently tested for routine clinical work.
Acknowledgments Grant sponsor: Fonds zur Fo¨ rderung der wissenschaftlichen Forschung (FWF), grant number P12041MED.
References [1] Lauterbur P. MR microscopy using projection reconstruction. In: Blu¨ mich B, Kuhn W, editors. Magnetic resonance microscopy. Weinheim: VCH, 1992. p. 3–25.
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J. Constantin Sze´ les et al. / Magnetic Resonance Imaging 19 (2001) 1235–1238
[2] Aguayo JB, Blackband SJ, Schoeniger J. Nuclear Magnetic Resonance imaging in a single cell. Nature 1986;322:190 –1. [3] Cho ZH, Ahn CB, Juh SC, Lee HK, Jacobs RE, Lee S, Yi JH, Jo JM. Nuclear magnetic resonance microscopy with 4-m resolution: theoretical study and experimental results. Med Phys 1989;15:815–24. [4] Song HK, Wehrli FW, Ma J. In vivo MR microscopy of the human skin. Magn Reson Med 1997;37:85–91. [5] Richard SB, Querleux BG, Bittoun J. Characterization of the skin in vivo by high resolution magnetic resonance imaging: water behavior and age-related effects. J Invest Dermatol 1993;100:705–9. [6] Ablett S, Burdett NG, Carpenter TA, Hall LD, Salter DC. Short echo time MRI enables visualisation of the natural state of human stratum corneum water in vivo. Magn Res Imaging 1996;14:357– 60. [7] Blackband SJ, Chakrabarti I, Gibbs P, Buckley DL, Horsman A. Fingers: three-dimensional MR imaging, and angiography with a local gradient coil. Radiology 1994;190:895–9. [8] Erickson SJ, Kneeland JB, Middleton WD, Jesmanowicz A, Hyde J, Lawson TL, Foley WD. MR imaging of the finger: correlation with normal anatomic sections. Am J Roentgenol 1989;152:1013–9. [9] Klarho¨ fer M, Csapo B, Balassy C, Szeles JC, Moser E. Blood flow velocities in the human finger. Magn Reson Med 2001;45:716 –19.
[10] Drape JL, Idy-Peretti I, Goettmann S, Guerin-Surville H, Bittoun J. Standard and high resolution magnetic resonance imaging of glomus tumors of toes and fingertips. J Am Acad Dermatol 1996;35:550 –5. [11] Zanetti M, Ledermann T, Zollinger H, Hodler J. Efficacy of MR imaging in patients suspected of having Morton’s neuroma. Am J Roentgenol 1997;168:529 –32. [12] D’Souza D, McDiarmid J, Tickle C. A polydactylous human foot with ‘double-dorsal’ toes. J Anat 1998;193:121–30. [13] Katz JB. Progressive macrodactyly. J Foot Ankle Surg 1999;38:143– 6. [14] Vater A. Dissertatio de consensu partium corporis humani. Haller. isputationum Anatomicarum selectarum. Gottingaeh, vol. 2, pp. 953– 72; 1741. [15] Iggo A. Is the physiology of cutaneous receptors determined by morphology? Prog Brain Res 1976;43:15–31. [16] Fawcett DW, Jensh RP. Bloom & Fawcett: concise histology. New York: Chapman and Hall, 1997. p. 179. [17] Bistevins R, Awad E. A structure and ultrastructure of mechanoreceptors at the human musculotendinous junction. Arch Phys Med Rehabil 1981;62:74 – 83. [18] Stark B Carlstedt T, Hallin RG. Distribution of human Pacinian corpuscules in the hand. A cadaver study. Br J Hand Surg 1998;23: 370 –2.