Diagnostic value of hybrid FDG-PET/MR imaging of chronic osteomyelitis

Dennis Jan Willem Hulsen1,2, Cristina Mitea3, Jacobus J. Arts1, Daan Loeffen3, Jan Geurts1
1Department of Orthopaedic Surgery, Research School Caphri, Maastricht University Medical Centre, Maastricht, The Netherlands
2Department of Medical Physics, Jeroen Bosch Ziekenhuis, ‘s-Hertogenbosch, The Netherlands
3Department of Radiology and Nuclear Medicine, Maastricht University Medical Centre, Maastricht, the Netherlands

Tóm tắt

Magnetic resonance imaging (MRI) and 2-[18F]-fluoro-2-deoxy-d-glucose (18F-FDG) Positron Emission Tomography, paired with Computed Tomography (PET/CT) are commonly used modalities in the complicated diagnostic work-up of osteomyelitis. PET/MRI is a relatively novel hybrid modality with suggested applications in bone infection imaging, based on expert opinion and previous qualitative research. 18F-FDG PET/MRI has the advantages of reduced radiation dose, more soft tissue information, and is deemed more valuable for surgical planning compared to 18F-FDG PET/CT. The goal of this study is to quantitatively assess the diagnostic value of hybrid 18F-FDG PET/MRI for chronic osteomyelitis. A retrospective analysis was performed by a nuclear medicine physician and radiologist on 36 patients with 18F-FDG PET/MRI scans for suspected osteomyelitis. Sensitivity, specificity, and accuracy were determined with the clinical assessment by the orthopaedic surgeon (based on subsequent intraoperative microbiology or long-term follow-up) as the ground truth. Standardized uptake values (SUV) were measured and analysed by means of receiver operating characteristics (ROC). This first study to quantitatively report the diagnostic value of 18F-FDG PET/MRI yielded a sensitivity, specificity, and accuracy of 78%, 100%, and 86% respectively. Area under the ROC curve was .736, .755, and .769 for the SUVmax, target to background ratio, and SUVmax_ratio respectively. These results are in the same range and not statistically different compared to diagnostic value for 18F-FDG PET/CT imaging of osteomyelitis in literature. Based on the aforementioned advantages of 18F-FDG PET/MRI and the diagnostic value reported here, the authors propose 18F-FDG PET/MRI as an alternative to 18F-FDG PET/CT in osteomyelitis diagnosis, if available.

Từ khóa


Tài liệu tham khảo

Averill LW, Hernandez A, Gonzalez L, Peña AH, Jaramillo D (2009) Diagnosis of osteomyelitis in children: utility of fat-suppressed contrast-enhanced MRI. Am J Roentgenol 192:1232–1238. https://doi.org/10.2214/AJR.07.3400 Beam E, Osmon D (2018) Prosthetic joint infection update. Infect Dis Clin N Am 32:843–859. https://doi.org/10.1016/j.idc.2018.06.005 Bose D, Kugan R, Stubbs D, McNally M (2015) Management of infected nonunion of the long bones by a multidisciplinary team. Bone Jt J 97-B:814–817. https://doi.org/10.1302/0301-620X.97B6.33276 Demirev A, Weijers R, Geurts J, Mottaghy F, Walenkamp G, Brans B (2014) Comparison of [18F]FDG PET/CT and MRI in the diagnosis of active osteomyelitis. Skelet Radiol 43:665–672. https://doi.org/10.1007/s00256-014-1844-3 Fahnert J, Purz S, Jarvers JS, Heyde CE, Barthel H, Stumpp P et al (2016) Use of simultaneous 18F-FDG PET/MRI for the detection of spondylodiskitis. J Nucl Med 57:1396–1401. https://doi.org/10.2967/jnumed.115.171561 Familiari D, Glaudemans AWJM, Vitale V, Prosperi D, Bagni O, Lenza A et al (2011) Can sequential 18F-FDG PET/CT replace WBC imaging in the diabetic foot? J Nucl Med 52:1012–1019. https://doi.org/10.2967/jnumed.110.082222 Florkow MC, Willemsen K, Zijlstra F, Foppen W, van der Wal BCH, van der Voort van Zyp JRN et al (2021) MRI-based synthetic CT shows equivalence to conventional CT for the morphological assessment of the hip joint. J Orthop Res Off Publ Orthop Res Soc. https://doi.org/10.1002/jor.25127 Floyed RL, Steele RW (2003) Culture-negative osteomyelitis. Pediatr Infect Dis J 22:731–735. https://doi.org/10.1097/01.inf.0000078901.26909.cf Glaudemans AWJM, Israel O, Slart RHJA (2015) Pitfalls and limitations of radionuclide and hybrid imaging in infection and inflammation. Semin Nucl Med 45:500–512. https://doi.org/10.1053/j.semnuclmed.2015.02.005 Glaudemans AWJM, Jutte PC, Cataldo MA, Cassar-Pullicino V, Gheysens O, Borens O et al (2019) Consensus document for the diagnosis of peripheral bone infection in adults: a joint paper by the EANM, EBJIS, and ESR (with ESCMID endorsement). Eur J Nucl Med Mol Imaging 46:957–970. https://doi.org/10.1007/s00259-019-4262-x Goebel M, Rosa F, Tatsch K, Grillhoesl A, Hofmann GO, Kirschner MH (2007) Diagnostik der chronischen osteitis des extremitätenskeletts: Stellenwert der F-18-FDG-PET. Unfallchirurg 110:859–866. https://doi.org/10.1007/s00113-007-1302-y Govaert GA, IJpma FF, McNally M, McNally E, Reininga IH, Glaudemans AW (2017) Accuracy of diagnostic imaging modalities for peripheral post-traumatic osteomyelitis: a systematic review of the recent literature. Eur J Nucl Med Mol Imaging. https://doi.org/10.1007/s00259-017-3683-7 Harris JC, Caesar DH, Davison C, Phibbs R, Than MP (2011) How useful are laboratory investigations in the Emergency Department evaluation of possible osteomyelitis? Emerg Med Australas 23:317–330. https://doi.org/10.1111/j.1742-6723.2011.01413.x Hartmann A, Eid K, Dora C, Trentz O, Von Schulthess GK, Stumpe KDM (2007) Diagnostic value of 18F-FDG PET/CT in trauma patients with suspected chronic osteomyelitis. Eur J Nucl Med Mol Imaging 34:704–714. https://doi.org/10.1007/s00259-006-0290-4 Hulsen DJW, Geurts J, Arts JJ, Loeffen D, Mitea C, Vöö SA (2019) Hybrid FDG-PET/MR imaging of chronic osteomyelitis: a prospective case series. Eur J Hybrid Imaging. https://doi.org/10.1186/s41824-019-0055-5 Husain T, Kim D (2002) C-reactive protein and erythrocyte sedimentation rate in orthopaedics. Univ Pa Orthop J 15:13–16 Jamar F, Buscombe J, Chiti A, Christian PE, Delbeke D, Donohoe KJ et al (2013) EANM/SNMMI guideline for 18F-FDG use in inflammation and infection. J Nucl Med 54:647–658. https://doi.org/10.2967/jnumed.112.112524 Jans LBO, Chen M, Elewaut D, Van den Bosch F, Carron P, Jacques P et al (2021) MRI-based synthetic CT in the detection of structural lesions in patients with suspected sacroiliitis: comparison with MRI. Radiology 298:343–349. https://doi.org/10.1148/RADIOL.2020201537 Johnstone E, Wyatt JJ, Henry AM, Short SC, Sebag-Montefiore D, Murray L et al (2018) Systematic review of synthetic computed tomography generation methodologies for use in magnetic resonance imaging-only radiation therapy. Int J Radiat Oncol Biol Phys. https://doi.org/10.1016/j.ijrobp.2017.08.043 Kaim AH, Gross T, von Schulthess GK (2002) Imaging of chronic posttraumatic osteomyelitis. Eur Radiol. https://doi.org/10.1007/s00330-001-1141-0 Kan JH, Young RS, Yu C, Hernanz-Schulman M (2010) Clinical impact of gadolinium in the MRI diagnosis of musculoskeletal infection in children. Pediatr Radiol 40:1197–1205. https://doi.org/10.1007/s00247-010-1557-2 Kapoor A, Page S, LaValley M, Gale DR, Felson DT (2007) Magnetic resonance imaging for diagnosing foot osteomyelitis: a meta-analysis. Arch Intern Med 167:125–132. https://doi.org/10.1001/archinte.167.2.125 Kershah S, Partovi S, Traughber BJ, Muzic RF, Schluchter MD, O’Donnell JK et al (2013) Comparison of standardized uptake values in normal structures between PET/CT and PET/MRI in an oncology patient population. Mol Imaging Biol 15:776–785. https://doi.org/10.1007/s11307-013-0629-8 Kouijzer IJE, Scheper H, de Rooy JWJ, Bloem JL, Janssen MJR, van den Hoven L et al (2018) The diagnostic value of 18F–FDG-PET/CT and MRI in suspected vertebral osteomyelitis: a prospective study. Eur J Nucl Med Mol Imaging 45:798–805. https://doi.org/10.1007/s00259-017-3912-0 Ladefoged CN, Hansen AE, Keller SH, Holm S, Law I, Beyer T et al (2014) Impact of incorrect tissue classification in Dixon-based MR-AC: fat-water tissue inversion. EJNMMI Phys 1:101. https://doi.org/10.1186/s40658-014-0101-0 Lankinen P, Lehtimäki K, Hakanen AJ, Roivainen A, Aro HT (2012) A comparative 18F-FDG PET/CT imaging of experimental Staphylococcus aureus osteomyelitis and Staphylococcus epidermidis foreign-body-associated infection in the rabbit tibia. EJNMMI Res 2:1–10. https://doi.org/10.1186/2191-219X-2-41 Lankinen P, Seppänen M, Mattila K, Kallajoki M, Knuuti J, Aro HT (2017) Intensity of 18F-FDG PET uptake in culture-negative and culture-positive cases of chronic osteomyelitis. Contrast Media Mol Imaging. https://doi.org/10.1155/2017/9754293 Lee YJ, Sadigh S, Mankad K, Kapse N, Rajeswaran G (2016) The imaging of osteomyelitis. Quant Imaging Med Surg 6:184–198. https://doi.org/10.21037/qims.2016.04.01 Lemans JVC, Hobbelink MGG, IJpma FFA, Plate JDJ, van den Kieboom J, Bosch P et al (2019) The diagnostic accuracy of 18 F-FDG PET/CT in diagnosing fracture-related infections. Eur J Nucl Med Mol Imaging 46:999–1008. https://doi.org/10.1007/s00259-018-4218-6 Lew DP, Waldvogel FA (2004) Osteomyelitis. Lancet 364:369–379. https://doi.org/10.1016/S0140-6736(04)16727-5 Lyons K, Seghers V, Sorensen JIL, Zhang W, Paldino MJ, Krishnamurthy R et al (2015) Comparison of standardized uptake values in normal structures between PET/CT and PET/MRI in a tertiary pediatric hospital: a prospective study. Am J Roentgenol 205:1094–1101. https://doi.org/10.2214/AJR.15.14304 Martinez-Möller A, Souvatzoglou M, Delso G, Bundschuh RA, Chefd’hotel C, Ziegler SI et al (2009) Tissue classification as a potential approach for attenuation correction in whole-body PET/MRI: evaluation with PET/CT data. J Nucl Med 50:520–526. https://doi.org/10.2967/jnumed.108.054726 Mcnally M, Sendi P (2015) Implant-associated osteomyelitis of long bones. Bone Jt Infect Microbiol Diagn Treat. https://doi.org/10.1002/9781118581742.ch20 Parsons B, Strauss E (2004) Surgical management of chronic osteomyelitis. Am J Surg 188:57–66. https://doi.org/10.1016/S0002-9610(03)00292-7 Sconfienza LM, Signore A, Cassar-Pullicino V, Cataldo MA, Gheysens O, Borens O et al (2019) Diagnosis of peripheral bone and prosthetic joint infections: overview on the consensus documents by the EANM, EBJIS, and ESR (with ESCMID endorsement). Eur Radiol Eur J Nucl Med Mol Imaging 29:6425–6438. https://doi.org/10.1007/s00330-019-06326-1 Sheehy SH, Atkins BA, Bejon P, Byren I, Wyllie D, Athanasou NA et al (2010) The microbiology of chronic osteomyelitis: Prevalence of resistance to common empirical anti-microbial regimens. J Infect 60:338–343. https://doi.org/10.1016/j.jinf.2010.03.006 Subramaniam RM, Jadvar H, Colletti PM, Guimaraes A, Gullapali R, Iagaru AH et al (2017) ACR and SNMMI joint credentialing statement for PET/MRI of the body. J Nucl Med 58:1174–1176. https://doi.org/10.2967/jnumed.117.193524 Termaat MF, Raijmakers PGHM, Scholten HJ, Bakker FC, Patka P, Haarman HJTM (2005) The accuracy of diagnostic imaging for the assessment of chronic osteomyelitis: a systematic review and meta-analysis. J Bone Jt Surg Am 87:2464–2471. https://doi.org/10.2106/JBJS.D.02691 van der Bruggen W, Bleeker-Rovers CP, Boerman OC, Gotthardt M, Oyen WJG (2010) PET and SPECT in osteomyelitis and prosthetic bone and joint infections: a systematic review. Semin Nucl Med. https://doi.org/10.1053/j.semnuclmed.2009.08.005 Wang GL, Zhao K, Liu ZF, Dong MJ, Yang SY (2011) A meta-analysis of fluorodeoxyglucose-positron emission tomography versus scintigraphy in the evaluation of suspected osteomyelitis. Nucl Med Commun 32:1134–1142. https://doi.org/10.1097/MNM.0b013e32834b455c Wenter V, Müller JP, Albert NL, Lehner S, Fendler WP, Bartenstein P et al (2016) The diagnostic value of [18F]FDG PET for the detection of chronic osteomyelitis and implant-associated infection. Eur J Nucl Med Mol Imaging 43:749–761. https://doi.org/10.1007/s00259-015-3221-4