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85742 CHAPTER 4 MR Imaging of neuropathic feet in leprosy patients with suspected osteomyelitis

SOURCE (OR PART OF THE FOLLOWING SOURCE): Type Dissertation Title Clinical applications of Dixon chemical shift MR imaging: Morbus Gaucher, Morbus Hansen Author M. Maas Faculty Faculty of Medicine Year 2002 Pages 168 + 76 ISBN 909015888X


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MRR Imaging of neuropathic feet in leprosyy patients with suspected osteomyelitis s

Marioo Maas l , Erik J . Slim l*4, Agnes F. H o e k s m a 4 , Add J . van der Kleij 3 , Erik M. Akkerman \ Gerardd J . den Heeten ', William R. F a b e r 2

D e p a r t m e n tt of Radiology ', Dermatology'"' a n d Surgery 1 , Academic Medical Center a n dd the d e p a r t m e n t of Rehabilitation, J a n van Breemen I n s t i t u t e 4 , Amsterdam,, the Netherlands

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Chapterr 4 INTRODUCTION N Thee invasion by Mycobacterium leprae of Schwann cells with the resulting peripherall nerve damage can lead to a so-called neuropathic foot. Ulcerationn and infection (cellulitis or osteomyelitis) are important complications.. Repeated injury secondary to the neuropathy may lead to tarsall disintegration with osteolysis, fragmentation and progressive bone resorption.. In extreme cases dissolution of the mid-foot results in separationn of the forefoot and the hindfoot, changing all biomechanics andd weight bearing areas [1,11,12,22]. The neuro-osteoarthropathy in the foott is a cause of considerable morbidity in leprosy [9,12,22,26]. Therefore,, when a patient with a neuropathic foot presents himself with a warmm foot, it is a clinical challenge to discriminate between neuro-osteoarthropathyy and an ongoing osteomyelitis. Especially, this is difficultt in the presence of an ulcer, because an ulcer itself leads to increasedd local temperature [10,22]. Variouss diagnostic modalities have been investigated in the analysis of osteomyelitiss in neuropathic feet [5,13,24,28]. Magnetic Resonance Imagingg (MRI) has been described as an important modality to assess osteomyelitiss in the neuropathic foot of diabetic patients [16,18-20,27]. Tissuee characterisation and spatial resolution facilitate identification of associatedd soft tissue pathology [2-4,16,30]. To detect subtle bone marroww pathology, such as a low-grade chronic infection, it is mandatory too use fat-suppression sequences with the use of contrast administration [19-21].. A homogeneous fat-suppression in the entire field of view both beforee and after intravenous contrast material (Gadolinium-chelate (Gd)) iss required, to avoid artefacts and misreading [23]. This can adequately be achievedd by the use of two-point Dixon chemical shift imaging (TPDCSI) [14,19]. . Thee radiological literature available on MRI and osteomyelitis in neuropathicc feet nearly exclusively concerns diabetic foot pathology, being thee most frequent cause of neuropathic feet in the western world. However,, leprosy is an important cause of neuropathic feet worldwide. Accordingg to the latest World Health Organization (WHO) information at thee end of the year 2000 597.232 cases are on treatment, and 719.330 neww cases are reported [29].

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MRII and osteomyelitis in leprosy patients Literaturee concerning MRI and leprosy is scarce. Recently, an MRI study off neuropathic leprosy feet without clinical signs of inflammation was publishedd [15]. As far as we know, no papers concerning the use of MRI inn neuropathic leprosy feet, clinically suspected of osteomyelitis exist. In thiss paper we present our results with MRI in leprosy patients with neuropathicc feet clinically suspected for osteomyelitis. The purpose of this studyy was to analyze the value of MRI in diagnosing osteomyelitis as a singlee diagnostic procedure. The MRI findings are compared to the signs describedd in literature for evaluating osteomyelitis. These MRI results weree compared to the gold standard (bone biopsy or bone culture) or whenn no gold standard was available the MRI results were compared to thee clinical outcome after six months. MATERIALL & METHODS Patients Patients Wee retrospectively evaluated all consecutive MRI studies, following the Dixonn protocol (see later) of the foot in leprosy patients performed in the periodd 1994-2000. All patients had longstanding neuropathic foot pathologyy and were clinically suspected for inflammation; they had a neuropathicc warm swollen foot that did not respond to conservative weightt reduction therapy. A neuropathic foot was defined as a foot in whichh one or more of the neuronal functions i.e. sensory, motor function orr autonomic function was disturbed (consensus of the Dutch Neuropathicc Foot Society) [7]. Furthermore, the clinical follow-up had to coverr a period of six months. ClinicalClinical criteria Patientt charts were reviewed for clinical information concerning leprosy classificationn [25], presence and location of an ulcer and clinical signs of inflammation.. Twelve patients with neuropathic feet clinically suspected forr osteomyelitis were investigated, in which 18 MRI studies were performed.. The patients were classified as borderline lepromatous (n=3), borderlinee tuberculoid (n=l), and at the lepromatous side of the spectrum (n=8). . Thee gold standard for the diagnosis of osteomyelitis was a positive culture and/orr histopathology taken from bone material.

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Chapterr 4 Clinicall outcome after 6 months follow-up was retrospectively evaluated inn cases where histopathology or culture was not available or not conclusive.. A combination of clinical criteria was evaluated in a consensuss reading by a dermatologist (WRF), a physiatrist (AFH) and a surgeonn (AJvdK). The clinical criteria that were evaluated were response onn antibiotic treatment, nature of surgical treatment when performed, persistentt signs of inflammation, status of the ulcer, change in deformity. DiagnosticDiagnostic criteria (MRI) AA total number of 24 MR studies in 12 adult leprosy patients (9 male, 3 female;; mean age 63 years; age range 45-81 years) were included for evaluation.. Of these 24 MR studies 18 were performed because of clinical suspicionn of osteomyelitis. Follow-up MRI was performed in 6 patients (6 MRII studies). MRI MRI MRII examination was performed using a 1.5 Tesla Vision (Siemens, Erlangen, Germany).. All MRI studies were performed following the Dixon protocol [6,14,15].. This protocol consisted of: sagittal turbo-STIR (short tau inversion recovery)) (3mm), Tl-weighted Dixon sequence with in- and opposed-phase images,, sagittal dual echo T2-weighted FSE (Fast Spin Echo) (3mm); after the intravenouss administration of Gadolinium chelate (0,1 millirnol per kilogram of bodyy weight) Tl-weighted Dixon sequence with in- and opposed phase images [6,14,15]. . Too evaluate the MRI studies signs were used as described in literature concerningg diabetic neuropathic feet [16,19,20,27], Typical, primary MRI signs aree decreased marrow signal intensity on Tl-weighted images, increased signal intensityy on fat suppressed T2-weighted and/or fast STIR images, and focal marroww enhancement after Gadolinium-enhanced fat-suppressed Tl-weighted imagess [14,17,20,21,28], Secondary MRI signs are: the presence of a cutaneous ulcer,, cellulitis, a soft tissue mass, a soft tissue abscess, a sinus tract, and corticall interruption [21,30]. One musculoskeletal radiologist (MM) retrospectivelyy evaluated the images blinded to all clinical information except thee knowledge of clinical suspicion for osteomyelitis. The signal intensity of the bonee marrow on Tl-weighted in and out of phase Dixon images, fast STIR imagess and Gadolinium enhanced Tl-weighted in and out of phase Dixon imagess (primary signs) was classified as normal or abnormal on a data
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MRII and osteomyelitis in leprosy patients collectingg form. The secondary signs were classified as present or absent. Furthermore,, the site of involvement was noted (medial arch, central compartmentt or lateral arch) [8,12].

ClinicalClinical findings Inn 8 patients there was one event of suspected osteomyelitis. In 4 patients theree were multiple events of suspected osteomyelitis; in 3 patients there weree 2 events of suspected osteomyelitis, and in 1 patient there were 4 eventss of suspected osteomyelitis. The foot of involvement was 6 times rightright and 12 times left. The location of the ulcer was 2 times at the medial side,, 14 times at the lateral side, and 2 times an ulcer was present at the mediall and lateral side. Thee results of the gold standard are listed in table 1. When evaluating resultss from bone biopsy or bone culture and/or preset clinical criteria, withoutt detailed knowledge of the MRI results, the diagnosis osteomyelitis wass made in 16 of 18 events (88.9%). Tablee 1. Results of clinical follow-up in diagnosing osteomyelitis
Event t Gold d Clinical l Event t standard d outcome e
Pos s Pos s Pos s Pos s Pos s Pos s Pos s Pos s Pos s 10 0 11 1 12 2 13 3 14 4 15 5 16 6 17 7 18 8 Pos s Pos s Pos s Pos s Pos s Neg g Pos s Neg g

Gold d Clinical l standard d outcome e

Pos s

11 22 33 44 55 66 77 88 99

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C h a p t e rr 4 DiagnosticDiagnostic findings (MRI) Inn a total n u m b e r of 18 events of s u s p e c t e d osteomyelitis we encountered 177 MRI e x a m i n a t i o n s positive for primary MR signs for osteomyelitis (94.4%).. Decreased signal on T l in a n d o u t of p h a s e on 16 MRI (88.9%), increasedd signal on T2 on 13 MRI (72.2%), fast SE STIR on 13 MRI (72.2%),, a n d focally marrow e n h a n c e m e n t after g a d o l i n i u m - e n h a n c e d fat s u p p r e s s e dd T l on 17 MRI (94.4%) (Table 2).

Tablee 2.

Primary MRI signs: number of positive findings on various MRI sequences s

Tl l 166 (88.9%) T2 2 133 (72.2%) STIR R 133 (72.2%) Contrast t 177 (94.4%)

Positivee primary sign Numberr of MRI (%)

Thee secondary signs were positive in all MRI e x a m i n a t i o n s (100%). Cellulitiss w a s p r e s e n t in all c a s e s (100%). A c u t a n e o u s ulcer in t h e region off the s u s p e c t e d osteomyelitis w a s also p r e s e n t in all c a s e s (100%). Corticall i n t e r r u p t i o n w a s found in 16 investigations (88.9%). A s i n u s tract w a ss p r e s e n t in 5 c a s e s (27.7%). A soft t i s s u e a b s c e s s w a s p r e s e n t in 3 c a s e ss (16.6%). A soft t i s s u e m a s s was found on two occasions (11.1%) (Tablee 3).

Tablee & Presence of positive secondary MRI signs

Positive e secondary y sign n Numberr of MRII (%) Soft t tissue e abscess s 33 (16.6%) ) Soft t tissue e mass s 22 (11.1%) )

Cellulitis s Ulcer r 18 8 (100%) ) 18 8 (100%) )

Cortical l interruption n 17 7 (88.9%) )

Sinus s tract t 55 (27.7%) )

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MRII a n d osteomyelitis in leprosy p a t i e n t s Ann example of positive primary signs a n d s e c o n d a r y signs at the lateral sidee of the foot is shown in figure 1.

Figuree la. Two-point Dixon fat suppressionn image of the right foot of a 79-year-oldd female patient. Note the degradationn of the plantar fat with the presencee of soft tissue edema (interruptedd arrow) and the high signal intensityy in the partly destroyed cuboid bonee (non-interrupted arrow).

Figuree lb. Same patient after intravenous gadoliniumm chelate administration. Note the markedd enhancement at the lateral side of thee foot both in the soft tissue (cellulitis) (interruptedd arrow) and in the cuboid bone (osteomyelitis)) (non-interrupted arrow).

TheThe sites of involvement (MRI) Thee sites of involvement: medial-central-lateral, on MRI were analysed. Thee a r e a s of osteomyelitis were located at the medial site (MTP1 joint, os m e t a t a r s a ll 1, cuneiform 1, navicular bone) in 3 events, m e d i a l / c e n t r a l in 22 events, central (MTP 2-3, os m e t a t a r s a l 2-4) in 3 events, lateral (MTP 4-55 joint, os m e t a t a r s a l 4-5, cuboid, calcaneus) in 9 events. In 1 patient alll three a r e a s were involved. Follow-upFollow-up (MRI) Sixx follow-up MRI were m a d e after antibiotic t r e a t m e n t . Mean time of follow-upp w a s 5 m o n t h s . A complete healing of the ulcer occurred in two p a t i e n t ss with a normal follow-up MRI. -- 49 -

Chapterr 4 TwoTwo patients had an improved but still abnormal MRI; the MRI changes thatt were seen were a reduction but still present zone of enhancement of thee bone marrow. Both patients eventually showed a complete clinical remission.. The foot of the patient that showed an unchanged follow-up MRII despite continued antibiotics eventually was amputated. DISCUSSION N Osteomyelitiss is a well-known complication in patients with neuropathic foott pathology [4,13,16,19,20,24,26,28,30]. These patients may develop ulcerss that persist over a long period of time. In this way spread of infectionn per continuitatem can cause an infection of the osseous structuress in the foot. Clinical examination lacks specificity in this patient group,, since by clinical examination alone it is difficult to differentiate betweenn cellulitis, osteomyelitis and neuro-osteoarthropathy [22,26]. MR imagingg is potential powerful in the evaluation of the neuropathic foot; it iss useful for the evaluation of presence and extent of osteomyelitis, as well ass for the identification of the presence and extent of associated soft tissuee abnormalities that may have clinical importance, such as cellulitis, abscess,, and sinus tract [4,16,18-21,27,30], Nearly all data available on MRII and neuropathic feet concern patients suffering from diabetes. As far ass we know this is the first report on the use of MRI as a diagnostic proceduree in neuropathic leprosy feet suspected for osteomyelitis. Whenn analyzing the primary MRI signs for osteomyelitis we found in our populationn that in 17 out of 18 events (94.4%) primary MRI signs were positive.. Decreased signal intensity on in and out of phase Tl-weighted imagess and the marrow enhancement after gadolinium administration on fat-suppressedd Tl were the most frequent encountered abnormalities. In ourr retrospective analysis (gold standard and/or clinical outcome) 16 out off 18 events were diagnosed as positive for osteomyelitis. Comparing this evaluationn with the primary MRI signs there was agreement in 17 out of 188 events. The disagreement found in one patient was caused by the primaryy MRI sign focal marrow enhancement after contrast administration.. Therefore, we conclude that these primary signs, used in evaluatingg MRI examinations in diabetics can adequately be used to analyzee MRI examinations in leprosy patients with longstanding complicatedd neuropathic feet.

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MRII and osteomyelitis in leprosy patients Off the secondary MR signs ulcer and cellulitis were present in all cases. Thee areas on MRI suspected of osteomyelitis were in continuity with the ulcer.. The relation between ulcer and osteomyelitis has also been describedd in diabetes [5]. In contrast to diabetic feet only a minority of examinationss revealed a sinus tract or soft tissue abscess in our populationn [21]; it seems that these latter secondary signs are infrequentlyy found in leprosy. However, the presence of an ulcer and cellulitiss is common in leprosy patients with longstanding neuropathic feett suspected for osteomyelitis. Contrary to diabetic foot literature the secondaryy MRI signs seem of no additional value in diagnosing osteomyelitiss in a population of leprosy patients with longstanding neuropathicc foot disease. However, the value of these findings in a patient populationn of leprosy patients with neuropathy and clinical suspicion of inflammation,, without longstanding disease was not evaluated in this study.. For this purpose a study is currently conducted. Thee present study demonstrates in 9 events MRI changes suspected for osteomyelitiss at the lateral side only (50%). In a minority of events these changess were found at the medial side only (16.7%). This is in contrast to thee results found in a recent study of asymptomatic neuropathic feet in leprosyy patients in which 90 percent of the MRI changes were located at thee medial site of the foot [15]. Most likely the biomechanics in the two patientt groups (clinically unsuspected versus clinically suspected in longstandingg neuropathic foot disease) are different. Biomechanical analysiss in early tarsal disintegration shows the highest stress to occur duringg the push off phase in the bones of the lateral foot arch [12]. Perhapss this is caused by inversion due to paralysis of the lateral musculature.. An analysis of the walking cycle in two groups of leprosy patientss with neuropathic feet with and without clinical abnormalities mayy be of additional value in order to analyse the stress distribution. Whenn a leprosy patient with longstanding neuropathic foot disease is suspectedd of osteomyelitis clinical examination lacks specificity. Contrast enhancedd MRI with the use of two-point Dixon chemical shift imaging, as fat-suppresss ion technique is a valuable technique to detect osteomyelitis. Thee primary MR signs known from literature, concerning diabetic neuropathicc foot can adequately be assessed. MRI can serve as a one step diagnosticc strategy to diagnose osteomyelitis in leprosy patients with a longstandingg neuropathic foot problem. - 5 11 -

Chapterr 4 SUMMARY Y Thiss study w a s u n d e r t a k e n to analyze t h e MRI findings in leprosy p a t i e n t ss with n e u r o p a t h i c feet, s u s p e c t e d for osteomyelitis. As far a s we know,, no p a p e r s concerning osteomyelitis a n d MRI in n e u r o p a t h i c leprosy feett are present. Wee included MRI examination of 18 events of s u s p e c t e d osteomyelitis in 122 leprosy p a t i e n t s . All patients with longstanding n e u r o p a t h i c foot problemss were clinically s u s p e c t e d for osteomyelitis. All patients u n d e r w e n tt the MRI protocol with the inclusion of two-point Dixon chemicall shift imaging a s fat-suppression sequence. Forr t h e MRI evaluation we u s e d signs t h a t are described in literature for detectingg osteomyelitis in diabetic feet. The primary MRI signs were positivee in 17 of 18 p a t i e n t s . The secondary MRI signs were positive in 100%% of p a t i e n t s . O u rr results show t h a t MRI with the u s e of two-point Dixon chemical shift imagingg is a promising diagnostic modality to detect osteomyelitis in the p r e s e n c ee of n e u r o - o s t e o a r t h r o p a t h i c c h a n g e s in p a t i e n t s with leprosy. Wheneverr available MRI could play a n i m p o r t a n t role in detecting osteomyelitiss in leprosy patients with longstanding n e u r o p a t h i c feet, s u s p e c t e dd for osteomyelitis.

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MRII a n d o s t e o m y e l i t i s i n l e p r o s y p a t i e n t s 7.. F a b e r WR, Hoeksma AF, van der Kleij AJ, Maas M, Dijkstra PF. Diagnostic p r o c e d u r e ss for suspected osteomyelitis in n e u r o p a t h i c feet of leprosy p a t i e n t s . Intt J Lepr 1998; 66:29A. Goodwin DW, Salonen DC, Yu J S , B r o s c h m a n n J , Trudell DJ, Resnick DL. P l a n t a rr c o m p a r t m e n t s of the foot: MR a p p e a r a n c e in cadavers a n d diabetic p a t i e n t s .. Radiology 1995; 196:623-630. G u o c h e n g Z, Wenzhong L, Liangbin Y, Zhongmin Y, Xiangsheng C, Tisheng Z, G a n y u nn Y. An epidemiological survey of deformities a n d disabilities a m o m g 14,2577 cases of leprosy in 11 c o u n t r i e s . Leprosy review 1993; 6 4 : 1 4 3 - 1 4 9 . H o e k s m a AF, Faber WR. A s s e s s m e n t of skin t e m p e r a t u r e via palpation of t h e n e u r o p a t h i cc foot. 1 st world congress of ISPRM 2 0 0 1 . J a c o b S, Patil MK. Stress analyses in three-dimensional foot models of n o r m a l a n dd diabetic n e u r o p a t h y . Frontiers of Medical a n d Biological Engineering 1999;; 1-17. J a c o b S, Patil MK. Three-dimensional foot modelling a n d analysis of s t r e s s e s inn n o r m a l a n d early stage H a n s e n ' s disease with muscle paralysis. J o u r n a l of Rehabilitationn Research a n d Development 1999; 3 6 : 2 5 2 - 2 6 3 . Lipman BT, Collier BD, Carrera GF, et al. Detection of osteomyelitis in t h e n e u r o p a t h i cc foot: nuclear medicine, MRI a n d conventional radiography. Clin Nuclearr Med 1998; 23:77-82. M a a s M, Dijkstra PF, A k k e r m a n EM. Uniform fat s u p p r e s s i o n in h a n d s a n d feett t h r o u g h t h e u s e of two-point Dixon chemical shift MR imaging. Radiology 1999;; 2 1 0 : 1 8 9 - 1 9 3 . M a a s M, Slim FJ, Akkerman EM, Faber WR. MRI in clinically a s y m p t o m a t i c n e u r o p a t h i cc leprosy feet: a baseline s t u d y . Int J Leprosy a n d Other Mycobact Diss 2 0 0 1 ; 69:219-224. M a r c u s CD, Ladam-Marcus VJ, Leone J , Malgrange D, B o n n e t - G r a u s s e r a n d FM,, M e n t a n e a u BP. MR imaging of osteomyelitis a n d n e u r o p a t h i c o s t e o a r t h r o p a t h yy in the feet of diabetics. Radiographics 1996; 1 6 : 1 3 3 7 - 1 3 4 8 . Moore TE, Yuh WTC, Kathol MH, El-Khoury GY, Corson J D . Abnormalities of t h ee foot in patients with diabetes mellitus: findings on MR imaging. AJR 1 9 9 1 ; 157:813-816. . Morrison WB, Ledermann HP, Schweitzer ME. MR imaging of t h e diabetic foot. MRII Clin North Am 2 0 0 1 ; 9 : 6 0 3 - 6 1 3 . Morrison WB, Ledermann HP, Schweitzer ME. MR imaging of inflammatory conditionss of the ankle a n d foot. MRI Clin North Am 2 0 0 1 ; 9:615-637. Morrison WB, Schweitzer ME, Bock GW, Mitchell DG, H u m e EL, Pathria MN, Resnickk D. Diagnosis of osteomyelitis: Utility of fat-suppressed c o n t r a s t - e n h a n c e dd MR imaging. Radiology 1993; 189:251-257.



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