Efficacy of magnetic resonance imaging in deciding the

Miki Fujii, MD, PhD1
David G. Armstrong, DPM,
MD, PhD2,
Efficacy of magnetic resonance
imaging in deciding the
appropriate surgical margin
in diabetic foot osteomyelitis
ABSTRACT
The best therapy for diabetic foot osteomyelitis (DFO) is controversial. However, identification of the precise localization of DFO is
essential for appropriate treatment.
AIM
To ascertain the efficacy of magnetic resonance imaging (MRI) in the diagnosis of
DFO, and to select the appropriate surgical
margin.
Hiroto Terashi, MD, PhD3
1Department
of Plastic and
Reconstructive
Surgery, Kitaharima
Medical Center, Ono,
Japan
2Southern Arizona Limb
Salvage Alliance, University
of Arizona College of Medicine, Tucson, AZ, USA
3Department
of Plastic and
Reconstructive Surgery,
Kobe University Hospital,
Kobe, Japan
Correspondence to:
[email protected]
Conflicts of interest: None
METHODS
Preoperative MRI findings were compared
with the results of histopathological examinations of resected bones, and the margins
of the resected bones were analysed by histopathology. A total 149 bones from 28 foot
ulcers in 26 patients were examined. All ulcers were classified into 4 types according to
the main etiological factors.
RESULTS
In 14 neuropathic ulcers, all 55 bones, even
those with severe infection, were fully and
accurately diagnosed with the use of MRI. In
14 ischemic ulcers, only 9 of 94 bones evaluated by MRI after revascularization were diagnosed accurately. Of 32 bone margins that
showed bone marrow oedema, 28 healed,
and 4 did not heal, displaying severe infection or ischemia.
CONCLUSIONS
MRI is effective in the diagnosis of neuropathic ulcers, but not as effective in the diagnosis of ischemic ulcers. This study suggested
that the appropriate surgical margin should
be defined in the area of the bone marrow
oedema, but diligence should be exercised
in cases with severe infection or ischemia.
8
INTRODUCTION
The best therapy for diabetic foot osteomyelitis (DFO),
whether primarily medical or primarily surgical, is a subject of contention. Each has its potential advantages and
disadvantages1. Recent guidelines2 have recommended
that the presence and amount of residual dead or infected
bone and soft tissue should determine the duration of
antibiotic therapy. Besides the choice of primary therapy,
identification of the precise localization of DFO is essential
for appropriate treatment.
Guidelines2,3 recommend the use of plain radiographs
as a first-line investigative tool for diagnosing DFO, and
further note that although magnetic resonance imaging
(MRI) has been recognized as the most accurate imaging
modality for detecting DFO, it is not always necessary for
diagnosing or managing DFO. Plain radiographs, however,
show only destruction of bone, and not actual bone infection or inflammation.
We have previously demonstrated the efficacy of MRI
in the diagnosis of DFO in ulcers with different aetiologies 4,5. In the present report, we describe our study of
additional cases, and propose a means of defining the appropriate surgical margin for remission based on MRI and
histopathological findings.
METHODS
First, preoperative MRI findings were compared with the
results of histopathological examination of the resected
bones. Second, bone margins of the resected bones were
analysed by histopathology.
The records of 26 patients with diabetic foot ulcers (20
men and 6 women; mean age, 66.8 years; range, 42−85
years of age) who were suspected of having osteomyelitis
and had undergone surgery from 2008−2014 were examined. All patients had been diagnosed with type 2 diabetes, according to the classification of the World Health
Organization.
The ulcers were classified into 4 types according to the
main aetiological factors: type I, neuropathic ulcers; type
II, ischemic ulcers (critical limb ischemia [CLI]); type III,
neuropathic ulcers with infection; and type IV, ischemic
EWMA Journal 2015 vol 15 no 1
Science, Practice and Education
ulcers with infection4-6. Peripheral neuropathy (PN) was
assessed by touch sensation using the Ipswich touch test7.
Peripheral arterial disease (PAD) was suspected by the absence of pulsation and/or sound from the dorsalis pedis
artery and the posterior tibial artery assessed by Doppler
stethoscope, an ankle-brachial index < 0.9, and skin perfusion pressure < 40 mmHg. Patients with suspected PAD
were evaluated with the use of computed tomographic
angiography, duplex ultrasonography, and angiography.
Infection was assessed by the following: general conditions
such as high fever, chills, or malaise; clinical findings such
as redness, warmth, swelling, or purulent secretions; the
results of laboratory tests. DFO was suspected in patients
with a positive probe-to-bone test, swollen foot, sausage
toe, unexplained high leukocyte count or inflammatory
markers, and plain foot radiographic findings3.
Preoperative MRI was carried out with 1.5 T MR
scanners (3 mm slice thickness, T1-weighted images,
conventional spin echo, repetition time/echo time of 460
ms/13 ms, fat-suppressed T2-weighted images, short-tau
inversion-recovery images, short T1 inversion recovery,
and repetition time/echo time/inversion time of 3,401
ms/80 ms/150 ms). All MRI findings were checked by
M.F and H.T with consensus interpretation. The affected
bone marrow was compared with the adjacent normal fatty
marrow, and low intensity signals on T1-weighted images
and high intensity signals on fat-suppressed T2-weighted
images were attributed to osteomyelitis. Incomplete or
hazy signals or reticulated patterns were attributed to reactive bone marrow oedema. Normal bone marrow signals
were considered indicative of areas clear of disease (8). All
bones were marked according to the presence of osteomyelitis (OM), bone marrow oedema (BME), or normal
bone (N) (Fig. 1).
Surgery after the MRI diagnosis included resection of
Figure 1: MRI diagnosis of case 1, left 2nd toe
b)
b)
C)
a)
a)
b)
c)
c)
b)
c)
a) Osteomyelitis (OM) (T1WI: low intensity, fat-suppressed;
T2WI: high intensity)
b) Bone marrow edema (BME)
(incomplete or hazy signals or reticulated patterns)
c) Normal bone marrow signal (N)
MRI diagnosis:
Distal phalanges (c): Normal bone (N)
Middle phalanges (b, a): bone marrow edema/ osteomyelitis (BME/
OM)
Proximal phalanges (a, b, c): osteomyelitis/bone marrow edema/
normal bone (OM/BME/N)
EWMA Journal 2015 vol 15 no 1
the infected bones and gangrenous tissue, amputation, or
disarticulation. The area of resection was estimated preoperatively (from the MRI findings, blood flow, and area
of soft tissue infection) and confirmed intraoperatively.
A definitive diagnosis was then made from the histopathological examination of 5 mm thick sections of formalinfixed and paraffin-embedded bones stained with haematoxylin and eosin. Only bone marrow oedema or infiltration of inflammatory cells, or both was considered indicative of reactive bone marrow oedema. However, these 2
conditions, together with the presence of osteonecrosis,
granulation tissue, and/or fibrosis, were considered indicative of osteomyelitis (Fig. 2). The diagnosis from the
preoperative MRI findings was compared with the definitive diagnosis from the histopathological findings (Fig. 3).
Bone margins of the resected bones were examined by
histopathology.
Figure 2: Histopathological diagnosis (haematoxylin & eosin
staining, 40×)
Osteomyelitis (OM) Bone marrow edema (BME)
(H&E; 40 )
Bone marrow edema
Inflammatory cells Osteonecrosis
Granulation
Fibrosis
(H&E; 40 )
Bone marrow edema
Inflammatory cells
Informed consent was obtained from each patient, and
the study protocol conformed to the ethical guidelines of
the Declaration of Helsinki as reflected in the approval by
the institution’s human research review committee.
RESULTS
A total of 28 ulcers from 26 patients, including 2 patients
with 2 different types of ulcers each, were classified into
4 types according to the main aetiological factors as follows: type I, neuropathic ulcers (n=3); type II, ischemic
ulcers (n=3); type III, neuropathic ulcers with infection
(n=11); and type IV, ischemic ulcers with infection (n=11)
(Table 1).
The 26 patients underwent a total of 30 MRI examinations before surgery (Table 2). The average interval between the MRI examinations and surgery was 16.7 (range
2−48) days. All ischemic ulcers (type II and type IV) were
revascularised by bypass or endovascular treatment before
surgery. MRI was carried out as follows: 3 examinations
for 3 type I ulcers; 3 before revascularisation for 3 type II
ulcers; 1 after revascularisation for 1 type II ulcers; 11 for
9

Figure 3: Histopathological diagnosis of
case 1, left 2nd toe.
OM
N
BME)
OM)
BME
BME)
N)
N)
BME
Histopathological features of bone marrow
in the resected bones correspond to the
MRI findings.
Table 1. Classification of ulcers OM
Main aetiologic factors Classification* Ulcers (n) Neuropathic ulcers Type I 3** Ischemic ulcers ( CLI ) Type II 3** Neuropathic ulcers Type III 11** ½ (H&E; 40
)
with infection CLI with infection Type IV 11** Total 28** *Terashi H. et al Keio Osteomyelitis
J Med 2011; 6
0:17-­‐21, *
*Two (OM), bone marrow edema
(BME), normal
marrow
(N)
patients, had two types obone
f ulcers each. N different OM
Table Table 1
1. . C
Classification lassification o
of f u
ulcers lcers Table 2. Details of MRI examinations Main aaetiologic etiologic ffactors actors Classification* Classification* Ulcers Ulcers ((n) n) Main Neuropathic u
lcers Type I
3** Neuropathic ulcers Type I 3** Ischemic u
lcers (
C
LI )
Type I
I 3** Ischemic ulcers ( CLI ) Type II 3** Neuropathic u
lcers Type I
II 11** ½ Neuropathic ulcers Type III 11** ½ with i
nfection with infection CLI 11** CLI w
with ith iinfection nfection Type Type IIV V 11** Total 28** Total 28** *Terashi H
. e
t a
l K
eio J
M
ed 2
011; 6
0:17-­‐21, *
*Two *Terashi H. et al Keio J Med 2011; 60:17-­‐21, **Two patients, h
had ad ttwo wo d
different ifferent ttypes ypes o
of f u
ulcers lcers eeach. ach. patients, Type I Type II MRI 3* 4* Pre-­‐revascularization: 3 Post-­‐revascularization: 1 Type III 11 11* Type IV 11 12* Pre-­‐revascularization: 6 Post-­‐revascularization: 6 Total 28 30* Average interval between MRI and surgery: 16.7 days. *One ulcer of Type II (Case 5) underwent both pre-­‐ and post-­‐
revascularization MRI. Table Table 2
2. . D
Details etails o
of f M
MRI RI e
examinations xaminations 11 type III ulcers; and 6 before and 6 after revascularisation
Ulcers MRI MRI post-revascularisation
for
type IV Ulcers ulcers. Pre- and
MRI
Type I
3 3* Type I for 23 patients who
3* underwent
was
done
2
surgeries,
1 for
Type 3 4* Type III I 3 4* Pre-­‐revascularization: Pre-­‐revascularization: 3
3 type II ulcer and 1 for type IV ulcer.
Post-­‐revascularization: Post-­‐revascularization: 1
1 A
total
of
149
bone
specimens
(39
distal
phalanx,
29
Type I
II 11 11* Type III 11 11* Type 11 12* Pre-­‐revascularization: 6
middle
34 metatarsal bone,
Type IIV V phalanx,
11 46 proximal
12* phalanx,
Pre-­‐revascularization: 6 Post-­‐revascularization: 6
and
from 57 toes as follows:
1 cuboid bone were obtained Post-­‐revascularization: 6 Total 28 30* Total 28 from 3 ulcers),
30* type
II (40 bones from 3
type
I (11 bones
Average iinterval b
etween M
RI a
nd ssurgery: 1
d
Average nterval b
etween M
RI a
nd urgery: 16.7 6.7 and
days. ays. ulcers),
typeof III
(44II (bones
from
11
ulcers),
typeost-­‐
IV
*One u
lcer T
ype Case 5
) u
nderwent b
oth p
re-­‐ *One ulcer of Type II (Case 5) underwent both pre-­‐ aand nd p
post-­‐
(54
bones
from
11
ulcers)
(Table
3).
revascularization revascularization M
MRI. RI. Histologic analysis of all bone specimens revealed the
Table Table 3
3: : SSpecification pecification o
of f b
bone one sspecimens pecimens iin n e
each ach u
ulcer lcer ttype ype Ulcers Ulcers (n) Toes ((n) n) (n) Toes Type I
3 4* Type I 3 4* Type I
I 3 12* Type II 3 12* Type I
II 11 19* Type III 11 19* Type I
V 11 22* Type IV 11 22* Total 28 57* Total 28 57* *Four t
oes a
nd a
c
uboid bone one *Four toes and a cuboid b
10
Bones Bones ((n) n) 11 11 40 40 44 44 54 54 149 149 Distal Distal phalanx phalanx ((n) n) 3 3 12 12 13 13 11 11 39 39 Ulcers 3 3 presence
of osteomyelitis, bone marrow oedema, normal
bone, or gangrene. The histopathological features of bone
Table 3: in
Specification of bbones
one specimens in each ype marrow
the resected
corresponded
toulcer the tMRI
findings for ulcers of types I and III in every localisationMiddle (Table 4). Osteomyelitis
was detected in 41 bones,
Ulcers Distal withphalanx (n) specificity
Toes (n) of Bones phalanx (n) (n) a sensitivity
and
100%.(n) In type
II ulcers,
Type I
3 4* 11 3 however, none of the 40 bones was accurately diagnosed 3 Type II because
3 of
unclear
12* or equivocal
40 12 (Table 9 by
MRI
images
Type III 11 19* 44 13 5). Of 40 bones from type II ulcers, 27 showed
dry gan- 7 Type IV 11 22* 54 11 10 grene.
Only28 9 bones
from
type149 IV ulcers
examined
by 29 Total 57* 39 post-revascularisation
*Four toes and a cuboid MRI
bone were accurately diagnosed.
Middle Middle phalanx phalanx (n) (n) 3 3 9 9 7 7 10 10 29 29 Proximal Proximal phalanx phalanx Metatarsal Metatarsal (n) (n) (n) (n) 3 1 3 1 11 8 11 8 14 10 14 10 18 15 18 15 46 34 46 34 Cuboid Cuboid (n) (n) 1 1 1 1 EWMA Journal 2015 vol 15 no 1
Science, Practice and Education
Table 4. MRI and histopathological diagnosis of neuropathic ulcers (Type I; Neuropathic ulcers, Type III; neuropathic ulcers with infection) MRI diagnosis (n) Histopathological diagnosis (n) Type Ulcers(n) Bones(n) Correct Incorrect OM OM/BME OM/BME/N BME I 3 11 11 0 6 4 0 1 III 11 44 44 0 17 12 2 10 Total 14 55 55 0 Osteomyelitis (OM), bone marrow edema (BME), normal bone (N) N 0 3 The other 45 bones still could not be diagnosed because
clinical outcomes of nonsurgical treatments have been
of unclear or equivocal images.
demonstrated with long-term courses of antibiotics2. If
conservative surgery is chosen, the surgeon needs to know
Histopathological analysis revealed osteomyelitis in 27
bones of type IV ulcers, but only 9 bones were correctly
the precise area of osteomyelitis. If medical therapy were
Table 5. MRI nd histopathological diagnosis ischemic ulcers (CLI) chosen, the duration of antibiotic therapy would depend
diagnosed
byapost-revascularisation
MRI,of with
a sensitiv(Type II; CLI, Type IV; CLI with infection) ity
of 29.6%.
on the presence and amount of residual dead or infected
Margins of 49 bones wereGroup examined
by
histopathology
bone2. Besides choosing primary therapy, identification of
A; Pre-­‐revascularization MRI diagnosis (Table
6). Of 37 bone margins of healed ulcers, 9 were
the precise localization of DFO is therefore essential for
MRI d
iagnosis Histopathological diagnosis normal and 28 displayed bone marrow oedema. Of 12
appropriate
treatment.
OM/
OM/ bone margins of unhealed ulcers, 4 showed bone marrow
MRI is a valuable tool for diagnosing osteomyelitis,
Type Ulcers Bones Correct Incorrect* OM BME BME/N OM/G BME BME/N G N oedema
and
II 3** 8 were
33 gangrenous.
0 Of the
33 32
bone
4 margins
0 0 as well as
0 for defining
1 the
1 presence
27 and
0 anatomy of deep
3
with
marrow
the 4 0 soft
displaying
IV bone
5** 14 oedema,
0 28
healed
14 (87.5%)
3 and 5 tissue
1 infections
2 . Its2 efficacy
1 in accurately
0 that
did not heal were from 2 patients with type III ulcers
the extent of DFO of different aetiological types of ulcers
Table 4. MTable Table RI and 44. . hM
M
istopathological RI RI aand nd hhistopathological istopathological diagnosis dodiagnosis oof f nneuropathic europathic ulcers uulcers lcers involving
severe
soft
tissue
infection
and f iagnosis 2neuropathic patients
with
is not
definitively known. Our previous studies4,5 have
Group Post-­‐revascularization MRI iagnosis (Type I; Neuropathic (Type (Type II; ; NNeuropathic europathic ulcers, Type uulcers, lcers, III; nBeuropathic TT; ype ype IIII; II; nneuropathic europathic ulcers with uulcers ilcers nfection) w
wdith ith iinfection) nfection) type
IV ulcers involving severe soft tissue infection and
demonstrated the efficacy of MRI in diagnosing DFO
ischemia.
8 gangrenous
bone
margins
from
of different
aetiological
types
of
ulcers,
showing that for
dMRI diagnosis MRI MRI d(dn) iagnosis iagnosis (Histopathological (n) n) Histopathological Histopathological diagnosis iagnosis iagnosis n) The
MRI iagnosis 2 patients
dHistopathological iagnosis d(dn) ((n) Type type Type Ulcers(n) Type Ulcers(n) Ulcers(n) Bones(n) Bones(n) Bones(n) Correct Correct Correct Incorrect Incorrect OM OM/ OM/BME OM OM OM/BME OM/BME OM/BME/N OM/BME/N OM/BME/N BME I, III),
BME BME N DFO
N N was reliably disOM/
with
II
ulcers could
not be
diagnosed
by MRIIncorrect because
neuropathic
ulcers
(type
I Ulcers I I 3 Bones 3 3 11 11 11 11 11 11 0 OM BME 0 0 6 BME/N tinguishable
6 6 4 OM/G 4 4 0 from
0 0 BME/N 1 bone
0 1 1 oedema
N 0 0 at any location,
Correct Incorrect* BME G ofType severe
ischemia.
reactive
11 III III 7 11 11 44 44 44 7 44 44 0 0 0 0 17 0 17 17 12 12 2 4 2 2 10 2 3 10 10 0 1 3 3 II III 1** 44 0 0 12 in the presence of severe infection.
Total 6** Total Total 14 40 14 14 55 55 55 -­‐ 55 55 0 1 0 0 1 even
0 However, MRI
IV 55 9 6 0 1 0 0 useful in1 diagnosing
Osteomyelitis Osteomyelitis Osteomyelitis b one OM), marrow b-­‐ bone one m
marrow arrow (BME), eedema dema (12 (BME), BME), bone n4 normal ormal ( N) bbone one ( (N) N) not 3 (OM), ((OM), edema 31 normal 1 was
1 ischemic
9 0 ulcers (type II, IV)
DISCUSSION
because
Osteomyelitis (OM), Bone marrow edema (BME), Normal bone (N), Gangrene (G) of insufficient interstitial fluid. Taken together, our
*Because of unclear equivocal MRI findings, **One ulcer of Type II uprevious
nderwent bconclusions
oth pre-­‐ and phave
ost-­‐ been confirmed by additional
Positive
results
haveor been
shown
with
conservative
surgery
vascularization MRI. combined with antibiotics9,10, and additional satisfactory
cases in the present study. 
Table 5. M
RI and istopathological diagnosis dodiagnosis f iagnosis ischemic lcers (CLI) Table Table 55. . h M
M
RI RI aand nd hhistopathological istopathological oof f uiischemic schemic uulcers lcers ((CLI) CLI) (Type II; CLI, Type with infection) (Type (Type III; I; CICV; LI, LI, C TLI Type ype IIV; V; CCLI LI w
with ith iinfection) nfection) Group A; PGroup Group re-­‐revascularization AA; ; PPre-­‐revascularization re-­‐revascularization MRI diagnosis M
MRI RI ddiagnosis iagnosis Histopathological Histopathological iagnosis Histopathological diagnosis ddiagnosis OM/
OM/
OM/ OM/ OM/
OM/ Type Ulcers Incorrect* Incorrect* OM BME OM/G OM/G BME G N G Type Type Bones Ulcers Ulcers Correct Bones Bones Correct Correct Incorrect* OM OM BME/N BME BME BME/N BME/N OM/G BME/N BME BME BME/N BME/N G N N II 3** II II 33 3** 3** 33 33 0 0 0 33 33 4 33 0 4 4 0 0 0 0 0 0 1 0 0 1 1 1 27 1 1 0 27 27 0 0 IV 5** IV IV 14 5** 5** 14 14 0 0 0 14 14 3 14 5 3 3 0 5 5 0 0 1 2 1 1 2 2 2 1 2 2 0 1 1 0 0 MRI MRI MRI ddiagnosis iagnosis diagnosis Group B; PGroup Group ost-­‐revascularization BB; ; PPost-­‐revascularization ost-­‐revascularization MRI diagnosis M
MRI RI ddiagnosis iagnosis Histopathological diagnosis ddiagnosis Histopathological Histopathological iagnosis OM/
OM/ OM/
OM/
OM/ OM/ Type Ulcers Incorrect* Incorrect* OM BME OM/G OM/G BME G N G Type Type Bones Ulcers Ulcers Correct Bones Bones Correct Correct Incorrect* OM OM BME/N BME BME BME/N BME/N OM/G BME/N BME BME BME/N BME/N G N N II 1** II II 1** 1** 7 7 7 0 0 0 7 7 0 7 0 0 0 0 0 0 0 0 0 4 0 0 2 4 4 0 2 2 1 0 0 1 1 IV 6** IV IV 40 6** 6** 40 40 9 9 9 -­‐ 1 -­‐ -­‐ 6 1 1 1 6 6 1 1 0 1 0 0 0 1 1 0 0 0 0 0 0 0 0 -­‐ -­‐ -­‐ 31 31 12 31 4 12 12 1 4 4 1 1 3 1 3 3 1 1 1 9 1 1 0 9 9 0 0 Osteomyelitis Osteomyelitis Osteomyelitis (OM), Bone ((OM), OM), marrow BBone one edema m
marrow arrow (BME), eedema dema Normal ((BME), BME), bone NNormal ormal (N), G
bbone angrene one ((N), N), GG
(G) angrene angrene ((G) G) *Because *Because o*Because f unclear ooof f r uuenclear quivocal RI findings, *f*One ulcer of Type II uoonderwent b
oth pre-­‐ babnd ppp
ost-­‐
nclear oor r eM
equivocal quivocal M
MRI RI findings, indings, ***One *One uulcer lcer f f TType ype III I uunderwent nderwent oth oth re-­‐ re-­‐ aand nd ppost-­‐
ost-­‐
vascularization MRI. vascularization vascularization M
MRI. RI. EWMA Journal diagnosis MRI MRI MRI ddiagnosis iagnosis 2015 vol 15 no 1
11
Table 6. Histopathological examinations of the bone margin Bone margins (n) Healed ulcers 37 Unhealed ulcers 12 Total 49 Histopathological diagnosis Normal Bone marrow edema Bone marrow edema Gangrene Currently, the appropriate surgical margin for full remission of DFO is not known. In the present study, we examined 49 bone margins by histopathology and demonstrated
that when the bone margin was set in the area of bone
marrow oedema, the chances of cure were high, and that
diligence was essential with cases of severe soft tissue infection or ischemia.
We propose an appropriate surgical strategy based on
MRI and histopathology. In neuropathic ulcers (type I and
III), the localisation of osteomyelitis is identified by MRI
and the surgical margins are determined on the MR images of the bone (in the area of bone marrow oedema), and
the range of soft tissue infection. Because no methods are
currently available for diagnosing the range of soft tissue
infections, it has to be defined, in part, empirically. Type
II ulcers, CLI, are of dry gangrene caused by ischemia, and
preoperative MRI is not effective for diagnosis, therefore
the site of resection has to be determined based on the
sufficiency of blood supply after revascularisation. Type
IV ulcers, CLI with infection, are the most difficult to
treat because of the decision regarding which to carry out
first, revascularisation for ischemia or debridement for
infection.
Except for cases requiring emergency debridement for
infection, we advocate evaluation of osteomyelitis using
MRI after revascularisation and setting of the bone margin
in the area of bone marrow oedema. Thus, the appropriate
surgical margin should be based on not only the range of
osteomyelitis, but also on the range of soft tissue infection
or the sufficiency of blood supply.
Toes in each type(n) I 0 4 0 0 4 II 2 2 0 8 12 III 2 8 2 0 12 IV 5 14 2 0 21 Total 9 28 4 8 49 Our study has several limitations. First, the definitive
diagnosis of DFO requires both histopathological findings
and isolation of bacteria from bone samples2. To show the
localisation of osteomyelitis, we used histopathological
findings in the diagnosis. Second, our bone samples were
from toes, metatarsals, and a cuboid bone. Although the
forefoot is not the only site of diabetic foot ulcers, it is
the most common11. Third, the classification6 chosen for
categorizing ulcers is not universal. Our Kobe classification7, a hybrid of the University of Texas11 and the Wagner classification12, have recently been used in Japan. In
Asia, type 2 diabetes is becoming epidemic, characterized
by rapid rates of increase within a short period, onset at
a relatively young age, and a low body mass index13. A
distinct discipline of podiatric medicine such as that in
United States or Europe is not available in Asia; therefore,
the establishment of a classification system that is more
relevant to Asian populations is necessary.
In conclusion, although the present study comprised a
limited number of patients, we were able to recommend
an appropriate surgical margin and strategy based on MRI
and histopathology. These continuing studies are therefore
aimed at salvaging as much of the diabetic foot as possible.
REFERENCES
1 Lipsky BA. Treating diabetic foot osteomyelitis
primarily with surgery or antibiotics: have we
answered the question? Diabetes Care
2014;37(3):593-5.
5 Fujii M, Armstrong DG, Terashi H. Efficacy of
Magnetic Resonance Imaging in Diagnosing Diabetic
Foot Osteomyelitis in the Presence of Ischemia. J Foot
Ankle Surg 2013;52: 717-23.
2 Lipsky BA, Berendt AR, Cornia PB, Pile JC, Peters EJ,
Armstrong DG et al. Infectious Diseases Society of
America. 2012 Infectious Diseases Society of America
clinical practice guideline for the diagnosis and
treatment of diabetic foot infections. Clin Infect Dis
2012:54:e132-73.
6 Terashi H, Kitano I, Tsuji Y. Total management of
diabetic foot ulcerations-Kobe classification as a new
classification of diabetic foot wounds. Keio J Med
2011;60:17-21.
3 Lipsky BA, Peters EJG, Senneville E, Berendt AR,
Embil JM, Lavery LA et al. Expert opinion on the
management of infections in the diabetic foot.
Diabetes Metab Res Rev 2012;28(1):163–78.
4 Fujii M, Terashi H, Tahara H. Efficacy of Magnetic
Resonance Imaging in Diagnosing Osteomyelitis in
Dabetic Foot Ulcers. J Am Podiatr Med Assoc
2014;104(1):24-9.
12
7 Rayman G, Vas PR, Baker N, Taylor CG Jr, Gooday
C, Alder AI et al. The Ipswich Touch Test: A simple
and novel method to identify inpatients with diabetes
at risk of foot ulceration. Diabetes Care
2011;34:1517-8.
8 Morrison WB, Schweitzer ME, Batte WG, Radack DP,
Russel KM. Osteomyelitis of the foot: relative
importance of primary and secondary MR imaging
signs. Radiology 1998;207:625-32.
9 Aragón-Sánchez J. Treatment of diabetic foot
osteomyelitis: A surgical critique. Int J Low Extrem
Wounds 2010;9:37-59.
10 Ha Van G, Siney H, Danan JP, Sachon C, Grimaldi A.
Treatment of osteomyelitis in the diabetic foot.
Contribution of conservative surgery. Diabetes Care
1996;19:1257-60.
11 Armstrong DG, Lavery LA, Harkless LB. Validation of
a diabetic wound classification system: the contribution of depth, infection, and ischemia to risk of
amputation. Diabetes Care 1998;21:855–9.
12 Wagner FW. The dysvascular foot: a system for
diagnosis and treatment. Foot Ankle 1981;2:64–122.
13 Chan JC, Malik V, Jia W, Kadowaki T, Yajnik CS,
Yoon KH, Hu FB. Diabetes in Asia: epidemiology, risk
factors, and pathophysiology. JAMA 2009;301:2129–
40.
EWMA Journal 2015 vol 15 no 1