Osteomyelitis of the lower extremity: pathophysiology, imaging, and classification, with an emphasis on diabetic foot infection

Jacob Mandell1, Bharti Khurana2, Jeremy T. Smith3, Gregory J. Czuczman1, Varand Ghazikhanian1, Stacy E. Smith1
1Division of Musculoskeletal Imaging and Intervention, Department of Radiology, Brigham and Women’s Hospital, Harvard Medical School, Boston, USA
2Division of Emergency Radiology, Department of Radiology, Brigham and Women’s Hospital, Harvard Medical School, Boston, USA
3Department of Orthopedic Surgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, USA

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Dabov GD (2016) Chapter 21: Osteomyelitis. In: Campbell’s Oper. Orthop. 4-Volume Set, Thirteenth. Elsevier Inc., p 764–787.e6

Walter G, Kemmerer M, Kappler C, Hoffmann R (2012) Treatment algorithms for chronic osteomyelitis. Dtsch Arztebl Int 109:257–264. https://doi.org/10.3238/arztebl.2012.0257

Kremers HM, Nwojo ME, Ransom JE et al (2015) Trends in the epidemiology of osteomyelitis. J Bone Joint Surg Am 97:837–845. https://doi.org/10.2106/JBJS.N.01350

Walenkamp GH (1997) Chronic osteomyelitis., Fifth Edit. Acta Orthop Scand. https://doi.org/10.1016/B978-1-4557-7628-3.00024-7

Lew DP, Waldvogel FA (2004) Osteomyelitis. Lancet (London, England) 364:369–379. https://doi.org/10.1016/S0140-6736(04)16727-5

Peltola H, Pääkkönen M (2014) Acute osteomyelitis in children. N Engl J Med 370:352–360. https://doi.org/10.1056/NEJMra1213956

Herman Kan J, Azouz EM (2013) Chapter 138: overview of musculoskeletal infections. In: Coley BD (ed) Caffey’s pediatric diagnostic imaging, 12th edn. Saunders, Philadelphia, pp 1471–1487

Offiah AC (2006) Acute osteomyelitis, septic arthritis and discitis: differences between neonates and older children. Eur J Radiol 60:221–232. https://doi.org/10.1016/j.ejrad.2006.07.016

Thein R, Tenenbaum S, Chechick O et al (2013) Delay in diagnosis of femoral hematogenous osteomyelitis in adults: an elusive disease with poor outcome. Isr Med Assoc J 15:85–88

Roberts JM, Drummond DS, Breed AL, Chesney J (1982) Subacute hematogenous osteomyelitis in children: a retrospective study. J Pediatr Orthop 2:249–254

Grey AC, Davies AM, Mangham DC et al (1998) The “penumbra sign” on T1-weighted MR imaging in subacute osteomyelitis: frequency, cause and significance. Clin Radiol 53:587–592

Jennin F, Bousson V, Parlier C et al (2011) Bony sequestrum: a radiologic review. Skelet Radiol 40:963–975. https://doi.org/10.1007/s00256-010-0975-4

Chai JW, Hong SH, Choi J-Y et al (2010) Radiologic diagnosis of osteoid osteoma: from simple to challenging findings. Radiographics 30:737–749. https://doi.org/10.1148/rg.303095120

Ware JK, Browner BD, Pesanti EL, et al (2014) Chapter 24: chronic osteomyelitis. In: Browner B, Jupiter J, Krettek C, Anderson P (eds) Skeletal trauma: basic science, management, and reconstruction, 5th edn. Saunders, Philadelphia, pp 609–635

Simpfendorfer CS (2017) Radiologic approach to musculoskeletal infections. Infect Dis Clin N Am 31:299–324. https://doi.org/10.1016/j.idc.2017.01.004

Khan SHM, Bloem HL (2008) Chapter 65—appendicular infection, Second Edi. Musculoskelet Imaging Second Ed. https://doi.org/10.1016/B978-1-4557-0813-0.00065-1

Lee YJ, Sadigh S, Mankad K et al (2016) The imaging of osteomyelitis. Quant Imaging Med Surg 6:184–198. 10.21037/qims.2016.04.01

Beaman FD, von Herrmann PF, Kransdorf MJ et al (2017) ACR appropriateness criteria {®} suspected osteomyelitis, septic arthritis, or soft tissue infection (excluding spine and diabetic foot). J Am Coll Radiol 14:S326–S337. https://doi.org/10.1016/j.jacr.2017.02.008

Capitanio MA, Kirkpatrick JA (1970) Early roentgen observations in acute osteomyelitis. Am J Roentgenol Radium Therapy, Nucl Med 108:488–496

Jaramillo D, Treves ST, Kasser JR et al (1995) Osteomyelitis and septic arthritis in children: appropriate use of imaging to guide treatment. AJR Am J Roentgenol 165:399–403. https://doi.org/10.2214/ajr.165.2.7618566

Anwer U, Yablon CM (2017) Imaging of osteomyelitis of the extremities. Semin Roentgenol 52:49–54. https://doi.org/10.1053/j.ro.2016.05.011

Gold RH, Tong DJF, Crim JR, Seeger LL (1995) Imaging the diabetic foot. Skelet Radiol 24:563–571. https://doi.org/10.1007/BF00204853

Fayad LM, Carrino JA, Fishman EK (2007) Musculoskeletal infection: role of CT in the emergency department. Radiographics 27:1723–1736. https://doi.org/10.1148/rg.276075033

Neha A, James S, Kothari NA et al (2001) Imaging of musculoskeletal infections. Radiol Clin N Am 21:653–671

Leone A, Cassar-Pullicino VN, Semprini A et al (2016) Neuropathic osteoarthropathy with and without superimposed osteomyelitis in patients with a diabetic foot. Skelet Radiol 45:735–754. https://doi.org/10.1007/s00256-016-2339-1

Love C, Palestro CJ (2016) Nuclear medicine imaging of bone infections. Clin Radiol 71:632–646. https://doi.org/10.1016/j.crad.2016.01.003

Lauri C, Tamminga M, Glaudemans AWJM et al (2017) Detection of osteomyelitis in the diabetic foot by imaging techniques: a systematic review and meta-analysis comparing MRI, white blood cell scintigraphy, and FDG-PET. Diabetes Care 40:1111–1120. https://doi.org/10.2337/dc17-0532

Dinh MT, Abad CL, Safdar N (2008) Diagnostic accuracy of the physical examination and imaging tests for osteomyelitis underlying diabetic foot ulcers: meta-analysis. Clin Infect Dis 47:519–527. https://doi.org/10.1086/590011

Towers JD (1997) The use of intravenous contrast in MRI of extremity infection. Semin Ultrasound CT MR 18:269–275

Ledermann HP, Schweitzer ME, Morrison WB (2002) Nonenhancing tissue on MR imaging of pedal infection: characterization of necrotic tissue and associated limitations for diagnosis of osteomyelitis and abscess. AJR Am J Roentgenol 178:215–222. https://doi.org/10.2214/ajr.178.1.1780215

Lipsky BA (1997) Osteomyelitis of the foot in diabetic patients. Clin Infect Dis 25:1318–1326. https://doi.org/10.1086/516148

Collins MS, Schaar MM, Wenger DE, Mandrekar JN (2005) T1-weighted MRI characteristics of pedal osteomyelitis. Am J Roentgenol 185:386–393. https://doi.org/10.2214/ajr.185.2.01850386

Johnson PW, Collins MS, Wenger DE (2009) Diagnostic utility of T1-weighted MRI characteristics in evaluation of osteomyelitis of the foot. AJR Am J Roentgenol 192:96–100. https://doi.org/10.2214/AJR.08.1376

Howe BM, Wenger DE, Mandrekar J, Collins MS (2013) T1-weighted MRI imaging features of pathologically proven non-pedal osteomyelitis. Acad Radiol 20:108–114. https://doi.org/10.1016/j.acra.2012.07.015

Craig JG, Amin MB, Wu K et al (1997) Osteomyelitis of the diabetic foot: MR imaging-pathologic correlation. Radiology 203:849–855. https://doi.org/10.1148/radiology.203.3.9169715

Duryea D, Bernard S, Flemming D et al (2017) Outcomes in diabetic foot ulcer patients with isolated T2 marrow signal abnormality in the underlying bone: should the diagnosis of “osteitis” be changed to “early osteomyelitis”? Skelet Radiol. https://doi.org/10.1007/s00256-017-2666-x

Waldvogel FA, Medoff G, Swartz MN (1970) Osteomyelitis: a review of clinical features, therapeutic considerations and unusual aspects (second of three parts). N Engl J Med 282:260–266. https://doi.org/10.1056/NEJM197001292820507

Waldvogel FA, Medoff G, Swartz MN (1970) Osteomyelitis: a review of clinical features, therapeutic considerations and unusual aspects. 3. Osteomyelitis associated with vascular insufficiency. N Engl J Med 282:316–322. https://doi.org/10.1056/NEJM197002052820606

Waldvogel FA, Medoff G, Swartz MN (1970) Osteomyelitis: a review of clinical features, therapeutic considerations and unusual aspects. N Engl J Med 282:198–206. https://doi.org/10.1056/NEJM197001222820406

Cierny G, Mader JT, Penninck JJ (1985) A clinical staging system for adult osteomyelitis. Contemp Orthop 10:17–37. https://doi.org/10.1097/01.blo.0000088564.81746.62

Wu H, Shen J, Yu X et al (2017) Two stage management of Cierny-Mader type IV chronic osteomyelitis of the long bones. Injury 48:511–518. https://doi.org/10.1016/j.injury.2017.01.007

Eggli KD, Quiogue T, Moser RP (1993) Ewing’s sarcoma. Radiol Clin N Am 31:325–337

Henninger B, Glodny B, Rudisch A et al (2013) Ewing sarcoma versus osteomyelitis: differential diagnosis with magnetic resonance imaging. Skelet Radiol 42:1097–1104. https://doi.org/10.1007/s00256-013-1632-5

McCarville MB, Chen JY, Coleman JL et al (2015) Journal club: distinguishing osteomyelitis from ewing sarcoma on radiography and mri. Am J Roentgenol 205:640–651. https://doi.org/10.2214/AJR.15.14341

Park J, Lee S, Bin JK, Park C (2014) Primary bone lymphoma of the distal tibia mimicking Brodie’s abscess. J Korean Soc Radiol 70:59–63

Skrepnek GH, Mills JL, Armstrong DG (2015) A diabetic emergency one million feet long: disparities and burdens of illness among diabetic foot ulcer cases within emergency departments in the United States, 2006-2010. PLoS One 10:1–15. https://doi.org/10.1371/journal.pone.0134914

Ramsey SD, Newton K, Blough D et al (1999) Incidence, outcomes, and cost of foot ulcers in patients with diabetes. Diabetes Care 22:382–387. https://doi.org/10.2337/diacare.22.3.382

Roug IK, Pierre-Jerome C (2012) MRI spectrum of bone changes in the diabetic foot. Eur J Radiol 81:1625–1629. https://doi.org/10.1016/j.ejrad.2011.04.048

Armstrong DG, Stacpoole-Shea S, Nguyen H, Harkless LB (1999) Lengthening of the Achilles tendon in diabetic patients who are at high risk for ulceration of the foot. J Bone Joint Surg Am 81:535–538

Lavery LA, Armstrong DG, AJM B, Diabetex Research Group (2002) Ankle equinus deformity and its relationship to high plantar pressure in a large population with diabetes mellitus. J Am Podiatr Med Assoc 92:479–482

Fry DE, Marek JM, Langsfeld M (1998) Infection in the ischemic lower extremity. Surg Clin North Am 78:465–479. https://doi.org/10.1016/S0039-6109(05)70326-1

Ledermann HP, Morrison WB, Schweitzer ME (2002) MR image analysis of pedal osteomyelitis: distribution, patterns of spread, and frequency of associated ulceration and septic arthritis. Radiology 223:747–755. https://doi.org/10.1148/radiol.2233011279

Morrison WB, Schweitzer ME, Batte WG et al (1998) Osteomyelitis of the foot: relative importance of primary and secondary MR imaging signs. Radiology 207:625–632. https://doi.org/10.1148/radiology.207.3.9609883

Marcus CD, Ladam-Marcus VJ, Leone J et al (1996) MR imaging of osteomyelitis and neuropathic osteoarthropathy in the feet of diabetics. Radiographics 16:1337–1348. https://doi.org/10.1148/radiographics.16.6.8946539

Charcot JM (1993) On arthropathies of cerebral or spinal origin. Clin Orthop Relat Res 296:4–7

Gupta R (1993) A short history of neuropathic arthropathy. Clin Orthop Relat Res 49:43–49

Ahmadi ME, Morrison WB, Carrino JA et al (2006) Neuropathic arthropathy of the foot with and without superimposed osteomyelitis: MR imaging characteristics. Radiology 238:622–631. https://doi.org/10.1148/radiol.2382041393

Berendt AR, Lipsky B (2004) Is this bone infected or not? Differentiating neuro-osteoarthropathy from osteomyelitis in the diabetic foot. Curr Diab Rep 4:424–429

Rubinow A, Spark EC, Canoso JJ (1980) Septic arthritis in a Charcot joint. Clin Orthop Relat Res 147:203–206

Schweitzer M, Morrison W (2004) MR imaging of the diabetic foot. Radiol Clin N Am 42:61–71. https://doi.org/10.1016/S0033-8389(03)00163-5

Abdel Razek AAK, Samir S (2017) Diagnostic performance of diffusion-weighted MR imaging in differentiation of diabetic osteoarthropathy and osteomyelitis in diabetic foot. Eur J Radiol 89:221–225. https://doi.org/10.1016/j.ejrad.2017.02.015

Martín Noguerol T, Luna Alcalá A, Beltrán LS et al (2017) Advanced MR imaging techniques for differentiation of neuropathic arthropathy and osteomyelitis in the diabetic foot. Radiographics 37:1161–1180. https://doi.org/10.1148/rg.2017160101

Peters EJ, Lipsky BA, Aragón-Sánchez J et al (2016) Interventions in the management of infection in the foot in diabetes: a systematic review. Diabetes Metab Res Rev 32(Suppl 1):145–153. https://doi.org/10.1002/dmrr.2706

Lipsky BA, Aragón-Sánchez J, Diggle M et al (2016) IWGDF guidance on the diagnosis and management of foot infections in persons with diabetes. Diabetes Metab Res Rev 32(Suppl 1):45–74. https://doi.org/10.1002/dmrr.2699

Senneville E, Morant H, Descamps D et al (2009) Needle puncture and transcutaneous bone biopsy cultures are inconsistent in patients with diabetes and suspected osteomyelitis of the foot. Clin Infect Dis 48:888–893. https://doi.org/10.1086/597263

Lesens O, Desbiez F, Vidal M et al (2011) Culture of per-wound bone specimens: a simplified approach for the medical management of diabetic foot osteomyelitis. Clin Microbiol Infect 17:285–291. https://doi.org/10.1111/j.1469-0691.2010.03194.x

Senneville E, Lombart A, Beltrand E et al (2008) Outcome of diabetic foot osteomyelitis treated nonsurgically. Diabetes Care 31:637–642. https://doi.org/10.2337/dc07-1744