ABSTRACT
Almost all diabetic foot infections originate from a foot ulcer. Decreased pain perception
and structural deformities such as previous partial foot amputation, Charcot joints,
and toe deformity in combination with chronic ischemia lead to a propensity for skin
breakdown and subsequent infection. Magnetic resonance (MR) imaging is increasingly
performed to evaluate for potential bone infection, but diagnosis of osteomyelitis
can be complicated because signal changes from acute Charcot arthropathy, fractures,
and postoperative residues may be mistaken for infection. Signal alterations of bone
infection may be atypical in sclerosing osteomyelitis and gangrene. Differentiation
between osteomyelitis and acute or subacute neuroarthropathy requires careful analysis
of the location of bone signal alterations, their distribution, and pattern because
qualitative changes are often identical. Presence of secondary signs such as adjacent
ulcer, cellulitis, and sinus tract is indicative of osteomyelitis. Differentiation
of noninfected neuroarthropathy from infected neuroarthropathy based on MR examinations
is difficult. Presence of a sinus tract, disappearance of subchondral cysts, diffuse
bone marrow abnormality, and bone erosions are in favor of infection.
KEYWORDS
Diabetic foot - osteomyelitis - neuroarthropathy - magnetic resonance imaging
REFERENCES
- 1
Boulton A J.
The diabetic foot: a global view.
Diabetes Metab Res Rev.
2000;
16(suppl 1)
S2-S5
- 2
Reiber G E, Vileikyte L, Boyko E J et al..
Causal pathways for incident lower-extremity ulcers in patients with diabetes from
two settings.
Diabetes Care.
1999;
22
157-162
- 3
Centers for Disease Control and Prevention (CDC) .
History of foot ulcer among persons with diabetes-United States, 2000-2002.
MMWR Morb Mortal Wkly Rep.
2003;
52
1098-1102
- 4
Gordois A, Scuffham P, Shearer A, Oglesby A, Tobian J A.
The health care costs of diabetic peripheral neuropathy in the US.
Diabetes Care.
2003;
26
1790-1795
- 5
Jeffcoate W J, Harding K G.
Diabetic foot ulcers.
Lancet.
2003;
361
1545-1551
- 6
Ledermann H P, Morrison W B, Schweitzer M E.
MR image analysis of pedal osteomyelitis: distribution, patterns of spread, and frequency
of associated ulceration and septic arthritis.
Radiology.
2002;
223
747-755
- 7
Morrison W B, Schweitzer M E, Wapner K L, Hecht P J, Gannon F H, Behm W R.
Osteomyelitis in feet of diabetics: clinical accuracy, surgical utility, and cost-effectiveness
of MR imaging.
Radiology.
1995;
196
557-564
- 8
Morrison W B, Schweitzer M E, Batte W G, Radack D P, Russel K M.
Osteomyelitis of the foot: relative importance of primary and secondary MR imaging
signs.
Radiology.
1998;
207
625-632
- 9
Ledermann H P, Schweitzer M E, Morrison W B.
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.
2002;
178
215-222
- 10
Ledermann H P, Schweitzer M E, Morrison W B.
Pelvic heterotopic ossification: MR imaging characteristics.
Radiology.
2002;
222
189-195
- 11
Ledermann H P, Morrison W B, Schweitzer M E.
Is soft-tissue inflammation in pedal infection contained by fascial planes? MR analysis
of compartmental involvement in 115 feet.
AJR Am J Roentgenol.
2002;
178
605-612
- 12
Morrison W B, Ledermann H P.
Work-up of the diabetic foot.
Radiol Clin North Am.
2002;
40
1171-1192
- 13
Ledermann H P, Morrison W B, Schweitzer M E.
Pedal abscesses in patients suspected of having pedal osteomyelitis: analysis with
MR imaging.
Radiology.
2002;
224
649-655
- 14
Ledermann H P, Morrison W B, Schweitzer M E, Raikin S M.
Tendon involvement in pedal infection: MR analysis of frequency, distribution, and
spread of infection.
AJR Am J Roentgenol.
2002;
179
939-947
- 15
Croll S D, Nicholas G G, Osborne M A, Wasser T E, Jones S.
Role of magnetic resonance imaging in the diagnosis of osteomyelitis in diabetic foot
infections.
J Vasc Surg.
1996;
24
266-270
- 16
Nigro N D, Bartynski W S, Grossman S J, Kruljac S.
Clinical impact of magnetic resonance imaging in foot osteomyelitis.
J Am Podiatr Med Assoc.
1992;
82
603-615
- 17
Rajbhandari S M, Jenkins R C, Davies C, Tesfaye S.
Charcot neuroarthropathy in diabetes mellitus.
Diabetologia.
2002;
45
1085-1096
- 18
Lipman B T, Collier B D, Carrera G F et al..
Detection of osteomyelitis in the neuropathic foot: nuclear medicine, MRI and conventional
radiography.
Clin Nucl Med.
1998;
23
77-82
- 19
Wrobel J S, Connolly J E.
Making the diagnosis of osteomyelitis. The role of prevalence.
J Am Podiatr Med Assoc.
1998;
88
337-343
- 20
Craig J G, Amin M B, Wu K et al..
Osteomyelitis of the diabetic foot: MR imaging-pathologic correlation.
Radiology.
1997;
203
849-855
- 21
Cook T A, Rahim N, Simpson H C, Galland R B.
Magnetic resonance imaging in the management of diabetic foot infection.
Br J Surg.
1996;
83
245-248
- 22
Levine S E, Neagle C E, Esterhai J L, Wright D G, Dalinka M K.
Magnetic resonance imaging for the diagnosis of osteomyelitis in the diabetic patient
with a foot ulcer.
Foot Ankle Int.
1994;
15
151-156
- 23
Weinstein D, Wang A, Chambers R, Stewart C A, Motz H A.
Evaluation of magnetic resonance imaging in the diagnosis of osteomyelitis in diabetic
foot infections.
Foot Ankle.
1993;
14
18-22
- 24
Newman L G, Waller J, Palestro C J et al..
Leukocyte scanning with 111In is superior to magnetic resonance imaging in diagnosis of clinically unsuspected
osteomyelitis in diabetic foot ulcers.
Diabetes Care.
1992;
15
1527-1530
- 25
Seabold J E, Flickinger F W, Kao S C et al..
Indium-111-leukocyte/technetium-99m-MDP bone and magnetic resonance imaging: difficulty
of diagnosing osteomyelitis in patients with neuropathic osteoarthropathy.
J Nucl Med.
1990;
31
549-556
- 26
Wang A, Weinstein D, Greenfield L et al..
MRI and diabetic foot infections.
Magn Reson Imaging.
1990;
8
805-809
- 27
Yuh W T, Corson J D, Baraniewski H M et al..
Osteomyelitis of the foot in diabetic patients: evaluation with plain film, 99mTc-MDP bone scintigraphy, and MR imaging.
AJR Am J Roentgenol.
1989;
152
795-800
- 28
Horowitz J D, Durham J R, Nease D B, Lukens M L, Wright J G, Smead W L.
Prospective evaluation of magnetic resonance imaging in the management of acute diabetic
foot infections.
Ann Vasc Surg.
1993;
7
44-50
- 29
Durham J R, Lukens M L, Campanini D S, Wright J G, Smead W L.
Impact of magnetic resonance imaging on the management of diabetic foot infections.
Am J Surg.
1991;
162
150-153
- 30
Beltran J, Campanini D S, Knight C, McCalla M.
The diabetic foot: magnetic resonance imaging evaluation.
Skeletal Radiol.
1990;
19
37-41
- 31
Morrison W B, Schweitzer M E, Bock G W et al..
Diagnosis of osteomyelitis: utility of fat-suppressed contrast-enhanced MR imaging.
Radiology.
1993;
189
251-257
- 32
Moore T E, Yuh W T, Kathol M H, el Khoury G Y, Corson J D.
Abnormalities of the foot in patients with diabetes mellitus: findings on MR imaging.
AJR Am J Roentgenol.
1991;
157
813-816
- 33
Gold R H, Tong D J, Crim J R, Seeger L L.
Imaging the diabetic foot.
Skeletal Radiol.
1995;
24
563-571
- 34
Daffner R H, Lupetin A R, Dash N, Deeb Z L, Sefczek R J, Schapiro R L.
MRI in the detection of malignant infiltration of bone marrow.
AJR Am J Roentgenol.
1986;
146
353-358
- 35
Jelinek J, Pearl A B, Kominsky S J, Schultz P M.
Magnetic resonance imaging of the foot. Rheumatologic disorders mimicking osteomyelitis.
J Am Podiatr Med Assoc.
1996;
86
228-231
- 36
Bamberger D M, Daus G P, Gerding D N.
Osteomyelitis in the feet of diabetic patients. Long-term results, prognostic factors,
and the role of antimicrobial and surgical therapy.
Am J Med.
1987;
83
653-660
- 37
Erdman W A, Tamburro F, Jayson H T, Weatherall P T, Ferry K B, Peshock R M.
Osteomyelitis: characteristics and pitfalls of diagnosis with MR imaging.
Radiology.
1991;
180
533-539
- 38
Tang J S, Gold R H, Bassett L W, Seeger L L.
Musculoskeletal infection of the extremities: evaluation with MR imaging.
Radiology.
1988;
166
205-209
- 39
Dangman B C, Hoffer F A, Rand F F, O'Rourke E J.
Osteomyelitis in children: gadolinium-enhanced MR imaging.
Radiology.
1992;
182
743-747
- 40
Edmonds M E.
Progress in care of the diabetic foot.
Lancet.
1999;
354
270-272
- 41
Frykberg R G, Kozak G P.
Neuropathic arthropathy in the diabetic foot.
Am Fam Physician.
1978;
17
105-113
- 42
Fabrin J, Larsen K, Holstein P E.
Long-term follow-up in diabetic Charcot feet with spontaneous onset.
Diabetes Care.
2000;
23
796-800
- 43
Klenerman L.
The Charcot joint in diabetes.
Diabet Med.
1996;
13(suppl 1)
S52-S54
- 44
Cofield R H, Morrison M J, Beabout J W.
Diabetic neuroarthropathy in the foot: patient characteristics and patterns of radiographic
change.
Foot Ankle.
1983;
4
15-22
- 45
Armstrong D G, Todd W F, Lavery L A, Harkless L B, Bushman T R.
The natural history of acute Charcot's arthropathy in a diabetic foot specialty clinic.
J Am Podiatr Med Assoc.
1997;
87
272-282
- 46
Edelman S V, Kosofsky E M, Paul R A, Kozak G P.
Neuro-osteoarthropathy (Charcot's joint) in diabetes mellitus following revascularization
surgery. Three case reports and a review of the literature.
Arch Intern Med.
1987;
147
1504-1508
- 47
Edmonds M E.
The neuropathic foot in diabetes. Part I: Blood flow.
Diabet Med.
1986;
3
111-115
- 48
Archer A G, Roberts V C, Watkins P J.
Blood flow patterns in painful diabetic neuropathy.
Diabetologia.
1984;
27
563-567
- 49
Eymontt M J, Alavi A, Dalinka M K, Kyle G C.
Bone scintigraphy in diabetic osteoarthropathy.
Radiology.
1981;
140
475-477
- 50
Edmonds M E, Clarke M B, Newton S, Barrett J, Watkins P J.
Increased uptake of bone radiopharmaceutical in diabetic neuropathy.
Q J Med.
1985;
57
843-855
- 51
Zlatkin M B, Pathria M, Sartoris D J, Resnick D.
The diabetic foot.
Radiol Clin North Am.
1987;
25
1095-1105
- 52
Cundy T F, Edmonds M E, Watkins P J.
Osteopenia and metatarsal fractures in diabetic neuropathy.
Diabet Med.
1985;
2
461-464
- 53
Young M J, Marshall A, Adams J E, Selby P L, Boulton A J.
Osteopenia, neurological dysfunction, and the development of Charcot neuroarthropathy.
Diabetes Care.
1995;
18
34-38
- 54 Resnick D.
Neuropathic osteoarthropathy. In: Resnick D Diagnosis of Bone and Joint Disorders. 4th ed. Philadelphia; W.B.
Saunders Company 2002: 3564-3595
- 55 Myerson M S.
Diabetic neuroarthropathy. In: Myerson MS Foot and Ankle Disorders. Philadelphia; W.B. Saunders Company 1999:
439-465
- 56
Sella E J, Barrette C.
Staging of Charcot neuroarthropathy along the medial column of the foot in the diabetic
patient.
J Foot Ankle Surg.
1999;
38
34-40
- 57
Clouse M E, Gramm H F, Legg M, Flood T.
Diabetic osteoarthropathy. Clinical and roentgenographic observations in 90 cases.
Am J Roentgenol Radium Ther Nucl Med.
1974;
121
22-34
- 58
Schon L C, Easley M E, Weinfeld S B.
Charcot neuroarthropathy of the foot and ankle.
Clin Orthop.
1998;
349
116-131
- 59
Marcus C D, Ladam-Marcus V J, Leone J, Malgrange D, Bonnet-Gausserand F M, Menanteau B P.
MR imaging of osteomyelitis and neuropathic osteoarthropathy in the feet of diabetics.
Radiographics.
1996;
16
1337-1348
- 60
Yu J S.
Diabetic foot and neuroarthropathy: magnetic resonance imaging evaluation.
Top Magn Reson Imaging.
1998;
9
295-310
- 61
Katz I, Rabinovitz J G, Dziadiw R.
Early changes in Charcot's joints.
Am J Roentgenol Radium Ther Nucl Med.
1961;
86
965-974
- 62
Thomasson J L, Sundaram M.
The diabetic foot-radiographic appearances.
Orthopedics.
1985;
8
668-677
- 63
Allman R M, Brower A C, Kotlyarov E B.
Neuropathic bone and joint disease.
Radiol Clin North Am.
1988;
26
1373-1381
- 64
Nguyen V D.
The radiologic spectrum of abnormalities of the foot in diabetic patients.
Can Assoc Radiol J.
1992;
43
333-339
- 65
Nguyen V D, Keh R A, Daehler R W.
Freiberg's disease in diabetes mellitus.
Skeletal Radiol.
1991;
20
425-428
- 66
Schwarz G S, Berenyi M R, Siegel M W.
Atrophic arthropathy and diabetic neuritis.
Am J Roentgenol Radium Ther Nucl Med.
1969;
106
523-529
- 67
Cavanagh P R, Young M J, Adams J E, Vickers K L, Boulton A J.
Radiographic abnormalities in the feet of patients with diabetic neuropathy.
Diabetes Care.
1994;
17
201-209
- 68
Kathol M H, el Khoury G Y, Moore T E, Marsh J L.
Calcaneal insufficiency avulsion fractures in patients with diabetes mellitus.
Radiology.
1991;
180
725-729
- 69
El Khoury G Y, Kathol M H.
Neuropathic fractures in patients with diabetes mellitus.
Radiology.
1980;
134
313-316
- 70
Ahmadi M E, Morrison W B, Schweitzer M E, Carrino J A, Raikin S M, Ledermann H P.
Neuropathic arthropathy of the foot with and without superimposed osteomyelitis: MR
imaging characteristics.
Radiology.
2005;
, In press
Hans Peter LedermannM.D.
Universitätsspital Basel, Dep. diagn. Radiologie, Petersgraben 4
4031 Basel, Switzerland