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Semin Musculoskelet Radiol 2004; 08(4): 355-368
DOI: 10.1055/s-2004-861764
Copyright © 2004 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001 USA.

Cartilage MRI T2 Relaxation Time Mapping: Overview and Applications

Timothy J. Mosher1 , Bernard J. Dardzinski2 , 3 , 4
  • 1Department of Radiology, The Penn State Milton S. Hershey Medical Center, Hershey Pennsylvania
  • 2Imaging Research Center, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio
  • 3Department of Radiology, University of Cincinnati College of Medicine, Cincinnati, Ohio
  • 4Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio
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Publication History

Publication Date:
10 January 2005 (online)

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ABSTRACT

The sensitivity of magnetic resonance imaging to biochemical and biophysical changes in the extracellular matrix of articular cartilage give it the potential to noninvasively detect the earliest changes of cartilage damage. The transverse relaxation time (T2) of cartilage has been shown to be a sensitive parameter for evaluation of early degeneration in articular cartilage, particularly changes in water and collagen content and tissue anisotropy. Although initial application has been in microimaging of small cartilage explants, in vivo techniques have been developed for cartilage T2 mapping of human joints. In addition to potential application in development of new pharmaceuticals and surgical techniques for preserving cartilage, in vivo cartilage T2 mapping can improve understanding of arthritis, cartilage aging, and response of cartilage to exercise.

KEYWORDS

Articular cartilage - cartilage collagen - arthritis - osteoarthritis - magnetic resonance imaging - cartilage T2

REFERENCES

  • 1 McCauley T R, Recht M P, Disler D G. Clinical imaging of articular cartilage in the knee.  Semin Musculoskelet Radiol. 2001;  5 293-304
    Thieme ConnectPubMedSearch in Google Scholar
  • 2 Gray M L, Burstein D, Xia Y. Biochemical (and functional) imaging of articular cartilage.  Semin Musculoskelet Radiol. 2001;  5 329-343
    PubMedSearch in Google Scholar
  • 3 Moskowitz R W. Osteoarthritis: Diagnosis and Medical/Surgical Management. 3rd ed. Philadelphia; Saunders 2001
    Search in Google Scholar
  • 4 Brandt K D, Doherty M, Lohmander L S. Osteoarthritis. Oxford Medical P. Oxford New York; Oxford University Press 1998
    Search in Google Scholar
  • 5 Mow V C, Hayes W C. Basic Orthopaedic Biomechanics. 2nd ed. Philadelphia: Lippincott-Raven; 1997
    Search in Google Scholar
  • 6 Mow V C, Holmes M H, Lai W M. Fluid transport and mechanical properties of articular cartilage: a review.  J Biomech. 1984;  17 377-394
    CrossrefPubMedSearch in Google Scholar
  • 7 Mankin H J, Thrasher A Z. Water content and binding in normal and osteoarthritic human cartilage.  J Bone Joint Surg Am. 1975;  57 76-80
    PubMedSearch in Google Scholar
  • 8 Venn M, Maroudas A. Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. I. Chemical composition.  Ann Rheum Dis. 1977;  36 121-129
    CrossrefPubMedSearch in Google Scholar
  • 9 Mankin H J, Brandt K D. Biochemistry and metabolism of articular cartilage in osteoarthritis. In: Moskowitz RW, Goldberg VM, Mankin HJ Osteoarthritis: Diagnosis and Medical/Surgical Management Philadelghia; W.B. Saunders 1992: 109-154
    Search in Google Scholar
  • 10 Lipshitz H. Etheredge RD, Glimcher MJ. Changes in the hexosamine content and swelling ratio of articular cartilage as functions of depth from the surface.  J Bone Joint Surg Am. 1976;  58 1149-1153
    PubMedSearch in Google Scholar
  • 11 Lai W M, Hou J S, Mow V C. A triphasic theory for the swelling and deformation behaviors of articular cartilage.  J Biomech Eng. 1991;  113 245-258
    CrossrefPubMedSearch in Google Scholar
  • 12 Guilak F, Ratcliffe A, Lane N, Rosenwasser M P, Mow V C. Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis.  J Orthop Res. 1994;  12 474-484
    CrossrefPubMedSearch in Google Scholar
  • 13 Hultkrantz W. Uber die spaltrichtungen der gelenkknorpel. Verhandlungen der anatomischen gesellschaft. 1898 12: 248
    Search in Google Scholar
  • 14 Maroudas A. Balance between swelling pressure and collagen tension in normal and degenerate cartilage.  Nature. 1976;  260 808-809
    CrossrefPubMedSearch in Google Scholar
  • 15 Mow V C, Kuei S C, Lai W M, Armstrong C G. Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments.  J Biomech Eng. 1980;  102 73-84
    CrossrefPubMedSearch in Google Scholar
  • 16 Harrison R, Bronskill M J, Henkelman R M. Magnetization transfer and T2 relaxation components in tissue.  Magn Reson Med. 1995;  33 490-496
    PubMedSearch in Google Scholar
  • 17 Packer K J. The dynamics of water in heterogeneous systems.  Philos Trans R Soc Lond B Biol Sci. 1977;  278 59-87
    PubMedSearch in Google Scholar
  • 18 Henkelman R M, Stanisz G J, Kim J K, Bronskill M J. Anisotropy of NMR properties of tissues.  Magn Reson Med. 1994;  32 592-601
    PubMedSearch in Google Scholar
  • 19 Duewell S H, Ceckler T L, Ong K, Wen H, Jaffer F A, Chesnick S A et al.. Musculoskeletal MR imaging at 4 T and at 1.5 T: comparison of relaxation times and image contrast.  Radiology. 1995;  196 551-555
    PubMedSearch in Google Scholar
  • 20 Kaufman J, Cecil K M, Kneeland J, Bolinger L. Structure in Images of articular cartilage at 4T. In: International Society for Magnetic Resonance in Medicine New York; ISMRM 1996
    Search in Google Scholar
  • 21 Mlynarik V, Degrassi A, Toffanin R, Vittur F, Cova M, Pozzi-Mucelli R S. Investigation of laminar appearance of articular cartilage by means of magnetic resonance microscopy.  Magn Reson Imaging. 1996;  14 435-442
    CrossrefPubMedSearch in Google Scholar
  • 22 Lusse S, Knauss R, Werner A, Grunder W, Arnold K. Action of compression and cations on the proton and deuterium relaxation in cartilage.  Magn Reson Med. 1995;  33 483-489
    PubMedSearch in Google Scholar
  • 23 Mosher T, Dardzinski B, Smith M. Characterization of Multiple T2 Components in Articular Cartilage. In: Proceedings of the International Society for Magnetic Resonance in Medicine; 1997 Vancouver, B.C., Canada; 1997: p. 1331
    Search in Google Scholar
  • 24 Dardzinski B J, Mosher T J, Li S, Van Slyke M A, Smith M B. Spatial variation of T2 in human articular cartilage.  Radiology. 1997;  205 546-550
    CrossrefPubMedSearch in Google Scholar
  • 25 Lusse S, Claassen H, Gehrke T, Hassenpflug J, Schunke M, Heller M et al.. Evaluation of water content by spatially resolved transverse relaxation times of human articular cartilage.  Magn Reson Imaging. 2000;  18 423-430
    PubMedSearch in Google Scholar
  • 26 Xia Y, Farquhar T, Burton-Wurster N, Ray E, Jelinski L W. Diffusion and relaxation mapping of cartilage-bone plugs and excised disks using microscopic magnetic resonance imaging.  Magn Reson Med. 1994;  31 273-282
    PubMedSearch in Google Scholar
  • 27 Mlynarik V, Degrassi A, Toffanin R, Jarh O, Vittur F. A method for generating magnetic resonance microimaging T2 maps with low sensitivity to diffusion.  Magn Reson Med. 1996;  35 423-425
    PubMedSearch in Google Scholar
  • 28 Watrin A, Ruaud J P, Olivier P T, Guingamp N C, Gonord P D, Netter P A et al.. T2 mapping of rat patellar cartilage.  Radiology. 2001;  219 395-402
    CrossrefPubMedSearch in Google Scholar
  • 29 Freeman D M, Bergman G, Glover G. Short TE MR microscopy: accurate measurement and zonal differentiation of normal hyaline cartilage.  Magn Reson Med. 1997;  38 72-81
    PubMedSearch in Google Scholar
  • 30 Frank L R, Wong E C, Luh W M, Ahn J M, Resnick D. Articular cartilage in the knee: mapping of the physiologic parameters at MR imaging with a local gradient coil-preliminary results.  Radiology. 1999;  210 241-246
    PubMedSearch in Google Scholar
  • 31 Smith H E, Mosher T J, Dardzinski B J, Collins B G, Collins C M, Yang Q X et al.. Spatial variation in cartilage T2 of the knee.  J Magn Reson Imaging. 2001;  14 50-55
    CrossrefPubMedSearch in Google Scholar
  • 32 Goodwin D W, Zhu H, Dunn J F. In vitro MR imaging of hyaline cartilage: correlation with scanning electron microscopy.  AJR Am J Roentgenol. 2000;  174 405-409
    PubMedSearch in Google Scholar
  • 33 Nieminen M T, Rieppo J, Toyras J, Hakumaki J M, Silvennoinen J, Hyttinen M M et al.. T2 relaxation reveals spatial collagen architecture in articular cartilage: a comparative quantitative MRI and polarized light microscopic study.  Magn Reson Med. 2001;  46 487-493
    CrossrefPubMedSearch in Google Scholar
  • 34 Grunder W, Kanowski M, Wagner M, Werner A. Visualization of pressure distribution within loaded joint cartilage by application of angle-sensitive NMR microscopy.  Magn Reson Med. 2000;  43 884-891
    CrossrefPubMedSearch in Google Scholar
  • 35 Xia Y. Heterogeneity of cartilage laminae in MR imaging.  J Magn Reson Imaging. 2000;  11 686-693
    CrossrefPubMedSearch in Google Scholar
  • 36 Dardzinski B J, Laor T, Schmidthorst V J, Klosterman L, Graham T B. Mapping T2 relaxation time in the pediatric knee: feasibility with a clinical 1.5-T MR imaging system.  Radiology. 2002;  225 233-239
    PubMedSearch in Google Scholar
  • 37 Lazovic-Stojkovic J, Mosher T J, Smith H E, Yang Q X, Dardzinski B J, Smith M B. In vivo T2 mapping of the proximal interphalangeal (PIP) joint at 3T. In: International Society for Magnetic Resonance in Medicine Honolulu, HI; 2002
    Search in Google Scholar
  • 38 Shapiro E M, Borthakur A, Kaufman J H, Leigh J S, Reddy R. Water distribution patterns inside bovine articular cartilage as visualized by 1H magnetic resonance imaging.  Osteoarthritis Cartilage. 2001;  9 533-538
    CrossrefPubMedSearch in Google Scholar
  • 39 Liess C, Lusse S, Karger N, Heller M, Gluer C C. Detection of changes in cartilage water content using MRI T(2)-mapping in vivo.  Osteoarthritis Cartilage. 2002;  10 907-913
    CrossrefPubMedSearch in Google Scholar
  • 40 Borthakur A, Shapiro E M, Beers J, Kudchodkar S, Kneeland J B, Reddy R. Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI.  Osteoarthritis Cartilage. 2000;  8 288-293
    PubMedSearch in Google Scholar
  • 41 Regatte R R, Kaufman J H, Noyszewski E A, Reddy R. Sodium and proton MR properties of cartilage during compression.  J Magn Reson Imaging. 1999;  10 961-967
    CrossrefPubMedSearch in Google Scholar
  • 42 Toffanin R, Mlynarik V, Russo S, Szomolanyi P, Piras A, Vittur F. Proteoglycan depletion and magnetic resonance parameters of articular cartilage.  Arch Biochem Biophys. 2001;  390 235-242
    CrossrefPubMedSearch in Google Scholar
  • 43 Fragonas E, Mlynarik V, Jellus V, Micali F, Piras A, Toffanin R et al.. Correlation between biochemical composition and magnetic resonance appearance of articular cartilage.  Osteoarthritis Cartilage. 1998;  6 24-32
    PubMedSearch in Google Scholar
  • 44 Mlynarik V, Trattnig S, Huber M, Zembsch A, Imhof H. The role of relaxation times in monitoring proteoglycan depletion in articular cartilage.  J Magn Reson Imaging. 1999;  10 497-502
    CrossrefPubMedSearch in Google Scholar
  • 45 Nieminen M T, Toyras J, Rieppo J, Hakumaki J M, Silvennoinen J, Helminen H J et al.. Quantitative MR microscopy of enzymatically degraded articular cartilage.  Magn Reson Med. 2000;  43 676-681
    CrossrefPubMedSearch in Google Scholar
  • 46 Rubenstein J D, Kim J K, Morova-Protzner I, Stanchev P L, Henkelman R M. Effects of collagen orientation on MR imaging characteristics of bovine articular cartilage.  Radiology. 1993;  188 219-226
    PubMedSearch in Google Scholar
  • 47 Goodwin D W, Wadghiri Y Z, Dunn J F. Micro-imaging of articular cartilage: T2, proton density, and the magic angle effect.  Acad Radiol. 1998;  5 790-798
    CrossrefPubMedSearch in Google Scholar
  • 48 Xia Y, Farquhar T, Burton-Wurster N, Lust G. Origin of cartilage laminae in MRI.  J Magn Reson Imaging. 1997;  7 887-894
    CrossrefPubMedSearch in Google Scholar
  • 49 Kim D J, Suh J S, Jeong E K, Shin K H, Yang W I. Correlation of laminated MR appearance of articular cartilage with histology, ascertained by artificial landmarks on the cartilage.  J Magn Reson Imaging. 1999;  10 57-64
    CrossrefPubMedSearch in Google Scholar
  • 50 Fullerton G D, Cameron I L, Ord V A. Orientation of tendons in the magnetic field and its effect on T2 relaxation times.  Radiology. 1985;  155 433-435
    CrossrefPubMedSearch in Google Scholar
  • 51 Hayes C W, Parellada J A. The magic angle effect in musculoskeletal MR imaging.  Top Magn Reson Imaging. 1996;  8 51-56
    PubMedSearch in Google Scholar
  • 52 Wacker F K, Bolze X, Felsenberg D, Wolf K J. Orientation-dependent changes in MR signal intensity of articular cartilage: a manifestation of the “magic angle” effect.  Skeletal Radiol. 1998;  27 306-310
    CrossrefPubMedSearch in Google Scholar
  • 53 Erickson S J, Prost R W, Timins M E. The “magic angle” effect: background physics and clinical relevance [editorial].  Radiology. 1993;  188 23-25
    CrossrefPubMedSearch in Google Scholar
  • 54 Xia Y. Relaxation anisotropy in cartilage by NMR microscopy (muMRI) at 14- microm resolution.  Magn Reson Med. 1998;  39 941-949
    PubMedSearch in Google Scholar
  • 55 Xia Y, Moody J B, Burton-Wurster N, Lust G. Quantitative in situ correlation between microscopic MRI and polarized light microscopy studies of articular cartilage.  Osteoarthritis Cartilage. 2001;  9 393-406
    PubMedSearch in Google Scholar
  • 56 Mosher T J, Smith H, Dardzinski B J, Schmithorst V J, Smith M B. MR imaging and T2 mapping of femoral cartilage: in vivo determination of the magic angle effect.  AJR Am J Roentgenol. 2001;  177 665-669
    CrossrefPubMedSearch in Google Scholar
  • 57 Gomez S, Toffanin R, Bernstorff S, Romanello M, Amenitsch H, Rappolt M et al.. Collagen fibrils are differently organized in weight-bearing and not-weight-bearing regions of pig articular cartilage.  J Exp Zool. 2000;  287 346-352
    CrossrefPubMedSearch in Google Scholar
  • 58 Xia Y, Moody J B, Alhadlaq H, Hu J. Imaging the physical and morphological properties of a multi-zone young articular cartilage at microscopic resolution.  J Magn Reson Imaging. 2003;  17 365-374
    CrossrefPubMedSearch in Google Scholar
  • 59 Goodwin D W. Visualization of the macroscopic structure of hyaline cartilage with MR imaging.  Semin Musculoskelet Radiol. 2001;  5 305-312
    Thieme ConnectPubMedSearch in Google Scholar
  • 60 Maroudas A I. Balance between swelling pressure and collagen tension in normal and degenerate cartilage.  Nature. 1976;  260 808-809
    CrossrefPubMedSearch in Google Scholar
  • 61 Maroudas A, Venn M. Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. II. Swelling.  Ann Rheum Dis. 1977;  36 399-406
    CrossrefPubMedSearch in Google Scholar
  • 62 Venn M. M.A., Chemical composition and swelling of normal and osteoarthritic femoral head cartilage.  Ann Rheum Dis. 1977;  36 121-129
    CrossrefPubMedSearch in Google Scholar
  • 63 Armstrong C G, Mow V C. Variations in the intrinsic mechanical properties of human articular cartilage with age, degeneration, and water content.  J Bone Joint Surg Am. 1982;  64 88-94
    PubMedSearch in Google Scholar
  • 64 Mow V C, Zhu W, Ratcliffe A. Structure and function of articular cartilage and meniscus. In: Mow VC, Hayes HC Basic Orthopedic Biomechanics New York; Raven Press 1991: 143-189
    Search in Google Scholar
  • 65 Dunham J, Chambers M G, Jasani M K, Bitensky L, Chayen J. Changes in the orientation of proteoglycans during the early development of natural murine osteoarthritis.  J Orthop Res. 1990;  8 101-104
    CrossrefPubMedSearch in Google Scholar
  • 66 Dunham J, Shackleton D R, Nahir A M, Billingham M E, Bitensky L, Chayen J et al.. Altered orientation of glycosaminoglycans and cellular changes in the tibial cartilage in the first two weeks of experimental canine osteoarthritis.  J Orthop Res. 1985;  3 258-268
    CrossrefPubMedSearch in Google Scholar
  • 67 Mori Y, Kubo M, Okumo H, Kuroki Y. A scanning electron microscopic study of the degenerative cartilage in patellar chondropathy.  Arthroscopy. 1993;  9 247-264
    PubMedSearch in Google Scholar
  • 68 Muir H, Bullough P, Maroudas A. The distribution of collagen in human articular cartilage with some of its physiological implications.  J Bone Joint Surg Br. 1970;  52 554-563
    CrossrefPubMedSearch in Google Scholar
  • 69 Mosher T J, Dardzinski B J, Smith M B. Human articular cartilage: influence of aging and early symptomatic degeneration on the spatial variation of T2-preliminary findings at 3 T.  Radiology. 2000;  214 259-266
    CrossrefPubMedSearch in Google Scholar
  • 70 Hoch D H, Grodzinsky A J, Koob T J, Albert M L, Eyre D R. Early changes in material properties of rabbit articular cartilage after meniscectomy.  J Orthop Res. 1983;  1 4-12
    CrossrefPubMedSearch in Google Scholar
  • 71 Burstein D, Velyvis J, Scott K T, Stock K W, Kim Y J, Jaramillo D et al.. Protocol issues for delayed Gd(DTPA)(2-)-enhanced MRI (dGEMRIC) for clinical evaluation of articular cartilage.  Magn Reson Med. 2001;  45 36-41
    CrossrefPubMedSearch in Google Scholar
  • 72 Akella S V, Regatte R R, Gougoutas A J, Borthakur A, Shapiro E M, Kneeland J B et al.. Proteoglycan-induced changes in T1rho-relaxation of articular cartilage at 4T.  Magn Reson Med. 2001;  46 419-423
    CrossrefPubMedSearch in Google Scholar
  • 73 Grunder W, Wagner M, Werner A. MR-microscopic visualization of anisotropic internal cartilage structures using the magic angle technique.  Magn Reson Med. 1998;  39 376-382
    PubMedSearch in Google Scholar
  • 74 Goodwin D W, Dunn J F. High-resolution magnetic resonance imaging of articular cartilage: correlation with histology and pathology.  Top Magn Reson Imaging. 1998;  9 337-347
    PubMedSearch in Google Scholar
  • 75 Maier C F, Tan S G, Hariharan H, Potter H G. T2 quantitation of articular cartilage at 1.5 T.  J Magn Reson Imaging. 2003;  17 358-364
    CrossrefPubMedSearch in Google Scholar
  • 76 Vinitski S, Mitchell D G, Einstein S G, Rao V M, Flanders A E, Schweitzer M E et al.. Conventional and fast spin-echo MR imaging: minimizing echo time.  J Magn Reson Imaging. 1993;  3 501-507
    PubMedSearch in Google Scholar
  • 77 Poon C S, Henkelman R M. Practical T2 quantitation for clinical applications.  J Magn Reson Imaging. 1992;  2 541-553
    PubMedSearch in Google Scholar
  • 78 Xia Y, Moody J B, Alhadlaq H. Orientational dependence of T2 relaxation in articular cartilage: a microscopic MRI (microMRI) study.  Magn Reson Med. 2002;  48 460-469
    CrossrefPubMedSearch in Google Scholar
  • 79 Watson P J, Carpenter T A, Hall L D, Tyler J A. Cartilage swelling and loss in a spontaneous model of osteoarthritis visualized by magnetic resonance imaging.  Osteoarthritis Cartilage. 1996;  4 197-207
    PubMedSearch in Google Scholar
  • 80 Gahunia H K, Lemaire C, Babyn P S, Cross A R, Kessler M J, Pritzker K P. Osteoarthritis in rhesus macaque knee joint: quantitative magnetic resonance imaging tissue characterization of articular cartilage.  J Rheumatol. 1995;  22 1747-1756
    PubMedSearch in Google Scholar
  • 81 Jelicks L A, Paul P K, O'Byrne E, Gupta R K. Hydrogen-1, sodium-23, and carbon-13 MR spectroscopy of cartilage degradation in vitro.  J Magn Reson Imaging. 1993;  3 565-568
    PubMedSearch in Google Scholar
  • 82 McCauley T R, Kier R, Lynch K J, Jokl P. Chondromalacia patellae: diagnosis with MR imaging [see comments].  AJR Am J Roentgenol. 1992;  158 101-105
    PubMedSearch in Google Scholar
  • 83 Brown T R, Quinn S F. Evaluation of chondromalacia of the patellofemoral compartment with axial magnetic resonance imaging.  Skeletal Radiol. 1993;  22 325-328
    PubMedSearch in Google Scholar
  • 84 De Smet A A, Monu J U, Fisher D R, Keene J S, Graf B K. Signs of patellar chondromalacia on sagittal T2-weighted magnetic resonance imaging.  Skeletal Radiol. 1992;  21 103-105
    PubMedSearch in Google Scholar
  • 85 Bredella M A, Tirman P F, Peterfy C G, Zarlingo M, Feller J F, Bost F W. Accuracy of T2-weighted fast spin-echo MR imaging with fat saturation in detecting cartilage defects in the knee: comparison with arthroscopy in 130 patients.  AJR Am J Roentgenol. 1999;  172 1073-1080
    CrossrefPubMedSearch in Google Scholar
  • 86 Gagliardi J A, Chung E M, Chandnani V P, Kesling K L, Christensen K P, Null R N et al.. Detection and staging of chondromalacia patellae: relative efficacies of conventional MR imaging, MR arthrography, and CT arthrography.  AJR Am J Roentgenol. 1994;  163 629-636
    PubMedSearch in Google Scholar
  • 87 Olivier P, Loeuille D, Watrin A, Walter F, Etienne S, Netter P et al.. Structural evaluation of articular cartilage: potential contribution of magnetic resonance techniques used in clinical practice.  Arthritis Rheum. 2001;  44 2285-2295
    CrossrefPubMedSearch in Google Scholar
  • 88 Hollander A P, Pidoux I, Reiner A, Rorabeck C, Bourne R, Poole A R. Damage to type II collagen in aging and osteoarthritis starts at the articular surface, originates around chondrocytes, and extends into the cartilage with progressive degeneration.  J Clin Invest. 1995;  96 2859-2869
    PubMedSearch in Google Scholar

Timothy J MosherM.D. 

Department of Radiology/NMR Building M108

Milton S. Hershey Medical Center, 500 University Drive, Hershey, PA 17033