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File ID 85742Filename CHAPTER 4 MR Imaging of neuropathic feet in leprosy patients with

suspected osteomyelitis

SOURCE (OR PART OF THE FOLLOWING SOURCE):Type DissertationTitle Clinical applications of Dixon chemical shift MR imaging: Morbus Gaucher,

Morbus HansenAuthor M. MaasFaculty Faculty of MedicineYear 2002Pages 168 + 76ISBN 909015888X

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MRR Imaging of neuropath ic fee t inl e p ros yy pa t i e n t s w i th s u s pe c t e dos teo m yel i t i s sM a r i o o M a a s l, Er ik J . Sl im l*4, A g n e s F . H o e k s m a 4 ,Add J . v a n de r Kleij 3, E r i k M . A k k e r m a n \

G e ra rdd J . d e n H e e te n ' , Wi l li a m R . F a b e r 2

Dep a r t m en t t o f R ad i o l o g y ' , De rm a t o l o g y ' ' an d S u rg e ry 1 , Acad em i c Med i ca l C en t e ra n dd t h e d e p a r t m e n t of R e h a b i l i t a t i o n , J a n v a n B r e e m e n I n s t i t u t e 4 ,A m s t e r d a m , , t h e N e t h e r l a n d s

Submitted Submitted

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Chapterr 4INTRODUCTION NThee invasion by Mycobacterium leprae of Schwann cells with the resultingperipherall nerve damage can lead to a so-called neuropathic foot.Ulcerationn and infection (cellulitis or osteomyelitis) are importantcomplications.. Repeated injury secondary to the neuropathy may lead totarsall disintegration with osteolysis, fragmentation and progressive boneresorption.. In extreme cases dissolution of the mid-foot results inseparationn of the forefoot and the hindfoot, changing all biomechanicsandd weight bearing areas [1,11,12,22]. The neuro-osteoarthropathy in thefoott is a cause of considerable morbidity in leprosy [9,12,22,26].Therefore,, when a patient with a neuropathic foot presents himself with awarmm foot, it is a clinical challenge to discriminate betweenneuro-osteoarthropathyy and an ongoing osteomyelitis. Especially, this isdifficultt in the presence of an ulcer, because an ulcer itself leads toincreasedd local temperature [10,22].Variouss diagnostic modalities have been investigated in the analysis ofosteomyelitiss in neuropathic feet [5,13,24,28]. Magnetic ResonanceImagingg (MRI) has been described as an important modality to assessosteomyelitiss in the neuropathic foot of diabetic patients [16,18-20,27].Tissuee characterisation and spatial resolution facilitate identification ofassociatedd soft tissue pathology [2-4,16,30]. To detect subtle bonemarroww pathology, such as a low-grade chronic infection, it is mandatorytoo use fat-suppression sequences with the use of contrast administration[19-21]. . A homogeneous fat-suppression in the entire field of view bothbeforee and after intravenous contrast material (Gadolinium-chelate (Gd))iss required, to avoid artefacts and misreading [23]. This can adequately beachievedd by the use of two-point Dixon chemical shift imaging (TPDCSI)[14,19]. .Thee radiological literature available on MRI and osteomyelitis inneuropathicc feet nearly exclusively concerns diabetic foot pathology, beingthee 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 atthee end of the year 2000 597.232 cases are on treatment, and 719.330neww cases are reported [29].

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Chapterr 4Clinicall outco m e after 6 m on th s follow-up was retrospectively evalu atedinn cases where his topathology or cul ture was not avai lable or notconclu sive.. A com bina tion of cl inical criteria was ev aluate d in aconsensuss reading by a dermatologist (WRF), a physiatris t (AFH) and asur ge onn (AJvdK). The cl inical cri teria th at were evalu ated w ere res po ns eonn ant ibiot ic t rea tment , na ture of surgical t rea tment when performed,persis tent t s igns of inflammation, s tatus of the ulcer, change in deformity.DiagnosticDiagnostic criteria MRI)AA total n u m b er of 24 MR stu die s in 12 adu lt leprosy pa t ie nts (9 ma le, 3female; ; mean age 63 years; age range 45-81 years) were included forevalu at ion. . Of the se 2 4 MR studie s 18 were performed be ca us e of cl inicalsu sp icio nn of osteom yelitis. Follow-up MRI w as performed in 6 p at ie nt s (6MRII studies).MRI MRIMRII 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 inversionrecovery)) (3mm), Tl-weighted Dixon sequence with in- and opposed-phaseimages,, sagittal dual echo T2-weighted FSE (Fast Spin Echo) (3mm); after theintravenouss administration of Gadolinium chelate (0,1 millirnol per kilogram ofbodyy 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 literatureconcerningg diabetic neuropathic feet [16,19,20,27], Typical, primary MRI signsaree decreased marrow signal intensity on Tl-weighted images, increased signalintensityy on fat suppressed T2-weighted and/or fast STIR images, and focalmarroww enhancement after Gadolinium-enhanced fat-suppressed Tl-weightedimagess [14,17,20,21,28], Secondary MRI signs are: the presence of a cutaneousulcer,, cellulitis, a soft tissue mass, a soft tissue abscess, a sinus tract, andcorticall interruption [21,30]. One musculoskeletal radiologist (MM)retrospectivelyy evaluated the images blinded to all clinical information exceptthee knowledge of clinical suspicion for osteomyelitis. The signal intensity of thebonee marrow on Tl-weighted in and out of phase Dixon images, fast STIRimagess and Gadolinium enhanced Tl-weighted in and out of phase Dixonimagess (primary s igns) was classif ied as normal or abnormal on a data

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MRII and osteomyelitis in leprosy patientscollectingg form. The secondary signs were classified as present or absent.Furthermore,, the site of involvement was noted (medial arch, centralcompartmentt or lateral arch) [8,12].RESULTS S

linical linical findingsInn 8 patients there was one event of suspected osteomyelitis. In 4 patientstheree were multiple events of suspected osteomyelitis; in 3 patients thereweree 2 events of suspected osteomyelitis, and in 1 pat ient there were 4eventss of suspected osteomyelitis. The foot of involvement was 6 timesrightright and 12 times left. The location of the ulcer was 2 times at the medialside,, 14 times at the lateral side, and 2 times an ulcer was present at themediall and lateral side.Thee results of the gold standard are listed in table 1. When evaluatingresultss from bone biopsy or bone culture and/or preset clinical criteria,withoutt detailed knowledge of the MRI results, the diagnosis osteomyelitiswass made in 16 of 18 events (88.9 ).

Tablee 1 Results of clinical follow-up in diagnosing osteomyelitisEvent t

2 23 34 45 56 67 78 89 9

Gold ds tandard d

Pos sPos sPos s

Pos s

Clinical loutcome e

Pos s

Pos s

Pos sPos sPos s

Event t

10 0

11 112 213 314 415 516 617 718 8

Gold ds tandard d

Pos sPos s

Pos sPos s

Clinical loutcome e

Pos s

Neg gPos sNeg g

Pos s

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C h a p t e r r 4DiagnosticDiagnostic findings MRI)I nn a t o t a l n u m b e r of 1 8 e v e n t s of s u s p e c t e d o s t e o m y e l i t i s w e e n c o u n t e r e d1 7 7 MR I e x a min a t io n s p o s i t i v e fo r p r ima ry MR s ig n s fo r o s t e o my e l i t i s(9 4 . 4 %) .. D e c re a s e d s ig n a l o n T l i n a n d o u t o f p h a s e o n 1 6 MR I (8 8 . 9 %) ,increasedd s igna l on T2 on 13 MRI (72 .2%) , fas t SE STIR on 13 MRI( 7 2. 2% ) ,, a n d f oc al ly m a r r o w e n h a n c e m e n t af te r g a d o l i n i u m - e n h a n c e d fa tsu p p re s s e d d T l o n 1 7 MR I (9 4 .4 %) (T ab le 2 ) .

Tablee 2 Primary MRI signs: number of positive findings on various MRIsequ ences s

P o s i t i v ee p r i m ary s i g n

Numberr of MRI (%)

T l l

166 (88.9%)

T2 2

133 (72.2%)

STIR R

133 (72.2%)

C o n t r a s t t

177 (94.4%)

T h e e s e c o n d a r y s i g n s w e r e p o s i t i v e i n a l l M R I e x a m i n a t i o n s ( 1 0 0 % ) .C e l l u l it i ss w a s p r e s e n t i n a ll c a s e s ( 1 0 0 % ) . A c u t a n e o u s u l c e r i n t h e r e g i o no ff t h e s u s p e c t e d o s t e o m y e l i t i s w a s a l s o p r e s e n t i n a ll c a s e s ( 1 0 0 % ) .C o r t i c a ll i n t e r r u p t i o n w a s f o u n d i n 1 6 i n v e s t i g a t i o n s ( 8 8 . 9 % ) . A s i n u s t r a c tw a s s p r e s e n t in 5 c a s e s ( 2 7 . 7 % ) . A s oft t i s s u e a b s c e s s w a s p r e s e n t i n 3c a s e ss ( 1 6 . 6 % ) . A s of t t i s s u e m a s s w a s f o u n d o n t w o o c c a s i o n s ( 11 .1 % )(Tablee 3).

Tablee & Presence of positive secondary MRI signsPosi t ive es e c o n d a r y ys ign n

Nu m b er r o fMRII (%)

Ce l lu l i t i s s

18 8(100% ) )

Ulce r r

18 8(100% ) )

Co r t i ca l li n t e r r u p t i o n n

17 7(88.9% ) )

S i n u s st ra c t t

5 5(27 .7% ) )

Soft tt i s s u e ea b s c e s s s

3 3(16.6% ) )

Soft tt i s s u e em a s s s

2 2(11.1%) )

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MRII an d os t eom ye l i t i s in l ep r o s y pa t i e n t sAnn ex am pl e of pos i t i ve p r i m ar y s i gn s an d s ec on da r y s i gns a t t h e l a t e r a lsidee of the foot is shown in f igure 1.

Figuree la Two-point Dixon fatsuppressionn image of the right foot of a79-year-oldd female patient. Note thedegradationn of the plantar fat with thepresencee of soft t issue edema(interruptedd arrow) and the high signalintensityy in the partly destroyed cuboidbonee (non-interrupted arrow).

Figuree lb Same patient after intravenousgadoliniumm chelate administration. Note themark edd en ha nce m en t at the lateral side ofthee foot both in the soft tissue (cellulitis)(interruptedd arrow) and in the cuboid bone(osteomyelitis)) (non-interrupted arrow).

TheThe sites of involvement MR I)T h ee s i te s of i n v o l v e m e n t : m e d i a l - c e n t r a l - l a t e r a l , o n M RI w e r e a n a l y s e d .Th ee a r e a s of o s t eo m ye l i t i s wer e l oca t e d a t t he m ed i a l s i t e (MTP1 j o i n t , o sm e t a t a r s a ll 1, c u n e i f o r m 1, n a v i c u l a r b o n e ) i n 3 e v e n t s , m e d i a l / c e n t r a l i n22 ev en t s , ce n t r a l ( MTP 2 - 3 , o s m e t a t a r s a l 2 - 4 ) i n 3 ev en t s , la t e r a l ( MTP4 - 5 5 j o i n t , o s m e t a t a r s a l 4 - 5 , c u b o i d , c a l c a n e u s ) i n 9 e v e n t s . In 1 p a t i e n ta l l l t h ree areas were involved .

Follow-upFollow-up MRI)Si xx f o l l ow- up MRI wer e ma d e a f te r an t i b i o t i c t r ea t m en t . M ean t i me off o l l ow- upp w a s 5 m o n t h s . A co m pl e t e hea l i ng of t he u l ce r oc cu r r ed i n t wopa t i en t s s w i t h a no r ma l f o l l ow- up MRI .

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Chapterr 4TwoTwo patients had an improved but still abnormal MRI; the MRI changesthatt were seen were a reduction but still present zone of enhancement ofthee bone marrow. Both patients eventually showed a complete clinicalremission.. The foot of the pat ient that showed an unchanged follow-upMRII despite continued antibiotics eventually was amputated.

DISCUSSION NOsteomyelitiss is a well-known complication in patients with neuropathicfoott pathology [4,13,16,19,20,24,26,28,30]. These patients may developulcerss that persist over a long period of time. In this way spread ofinfectionn per continuitatem can cause an infection of the osseousstructuress in the foot. Clinical examination lacks specificity in this patientgroup,, since by clinical examination alone it is difficult to differentiatebetweenn cellulitis, osteomyelitis and neuro-osteoarthropathy [22,26]. MRimagingg is potential powerful in the evaluation of the neuropathic foot; itiss useful for the evaluation of presence and extent of osteomyelitis, as wellass for the identification of the presence and extent of associated softtissuee abnormalities that may have clinical importance, such as cellulitis,abscess,, and sinus tract [4,16,18-21,27,30], Nearly all data available onMRII and neuropathic feet concern patients suffering from diabetes. As farass we know this is the first report on the use of MRI as a diagnosticproceduree in neuropathic leprosy feet suspected for osteomyelitis.Whenn analyzing the primary MRI signs for osteomyelitis we found in ourpopulationn that in 17 out of 18 events (94.4 ) primary MRI signs werepositive.. Decreased signal intensity on in and out of phase Tl-weightedimagess and the marrow enhancement after gadolinium administration onfat-suppressedd Tl were the most frequent encountered abnormalities. Inourr retrospective analysis (gold standard and/or clinical outcome) 16 outoff 18 events were diagnosed as positive for osteomyelitis. Comparing thisevaluationn with the primary MRI signs there was agreement in 17 out of188 events. The disagreement found in one patient was caused by theprimaryy MRI sign focal marrow enhancement after contras tadministration.. Therefore, we conclude that these primary signs, used inevaluatingg MRI examinations in diabetics can adequately be used toanalyzee MRI examinations in leprosy patients with longstandingcomplicatedd neuropathic feet.

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MRII and osteomyeli t is in leprosy patientsOff the secondary MR signs ulcer and celluli t is were present in al l cases.Thee areas on MRI suspected of osteomyeli t is were in continuity with theulcer. . The relat ion between ulcer and osteomyeli t is has also beendes crib edd in dia be tes [5]. In con tr as t to diab etic feet only a mino rity ofexaminationss revealed a sinus tract or soft t issue abscess in ourpop ulatio nn [21]; it se em s that th ese lat ter seco nd ary sign s areinfrequentlyy found in leprosy. However, the presence of an ulcer andcelluli t iss is common in leprosy patients with longstanding neuropathicfeett suspected for osteomyeli t is . Contrary to diabetic foot l i terature thesecondaryy MRI signs seem of no addit ional value in diagnosingosteomyeli t iss in a population of leprosy patients with longstandingneuropathicc foot disease. However, the value of these findings in a patientpopu lationn of leprosy pa tie nts with neu ro pa thy a nd clinical susp icion ofinflammation,, without longstanding disease was not evaluated in thiss tudy. . For th is purpose a s tudy is current ly conducted.Thee present s tudy demonstrates in 9 events MRI changes suspected forosteomyelitiss at the lateral side only (50%). In a minority of events thesecha nge ss were found at th e m edial s ide only (16.7%). This is in con tra st tothee resul ts found in a rec en t study of asy m pto m atic ne ur op ath ic feet inleprosyy patients in which 90 percent of the MRI changes were located atthee medial site of the foot [15]. Most likely the biomechanics in the twopatientt groups (cl inically unsuspected versus cl inically suspected inlong stand ingg ne ur op at hic foot disease) are different. Biom echa nicalanalysiss in early tarsal disintegration shows the highest s tress to occurduringg the push off phase in the bones of the lateral foot arch [12].Perhapss this is caused by inversion due to paralysis of the lateralmusculature. . An analysis of the walking cycle in two groups of leprosypatientss with neuropathic feet with and without cl inical abnormalit iesmayy be of addit ional value in order to analyse the stress distribution.Whenn a leprosy patient with longstanding neuropathic foot disease issus pe cte dd of osteom yeli t is clinical exa min ation la ck s specifici ty. C on tra sten ha nc edd MRI with th e u s e of two -point Dixon che m ical shift im aging, a sfat- sup pre sss ion tec hn iqu e is a valua ble tech niq ue to dete ct o steomy eli t is .Thee primary MR signs known from li terature, concerning diabeticneuropathicc foot can adequately be assessed. MRI can serve as a one stepdiagnosticc strategy to diagnose osteomyeli t is in leprosy patients with alongstandingg neuropathic foot problem.

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Chap t e r r 4SUMMARY YT h i ss s t u d y w a s u n d e r t a k e n t o a n a l y z e t h e M RI f i n d i n g s in l e p r o s yp a t i e n t ss w i t h n e u r o p a t h i c f ee t, s u s p e c t e d fo r o s t e o m y e l i t i s . A s f ar a s w ek n o w ,, n o p a p e r s c o n c e r n i n g o s t e o m y e l i t is a n d M R I i n n e u r o p a t h i c l e p r o s yfee t t a re present .W e e i n c l u d e d M R I e x a m i n a t i o n of 18 e v e n t s of s u s p e c t e d o s t e o m y e l i t is i n1 22 l e p r o s y p a t i e n t s . A ll p a t i e n t s w i t h l o n g s t a n d i n g n e u r o p a t h i c fo otp r ob l ems s wer e c l i n i ca l l y s us pec t ed f o r o s t eomye l i t i s . A l l pa t i en t su n d e r w e n tt t h e M R I p r o t o c o l w i t h t h e i n c l u s i o n o f t w o - p o i n t D i x o nc h e m i c a l l s h if t i m a g i n g a s f a t - s u p p r e s s i o n s e q u e n c e .For r t h e MRI ev a l u a t i o n we u s e d s i gn s t h a t a r e de s c r i be d i n l i t e r a t u r e f o rde t ec t i ngg os t eomye l i t i s i n d i abe t i c f ee t . The p r i mar y MRI s i gns wer epos i t i vee i n 17 o f 18 pa t i e n t s . Th e s ec on da r y MRI s i g ns wer e pos i t i ve in1 0 0 % % o f p a t i e n t s .O u rr r e s u l t s s ho w t h a t MRI wi t h t he u s e o f t w o- p o i n t D i xo n ch em i ca l s h if ti m ag i n gg i s a p r om i s i ng d i ag no s t i c mod a l i t y to de t ec t o s t eo my e l i t i s in t h ep r e s e n c e e 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 i n p a t i e n t s w i t h l e p r o sy .W h e n e v e rr a v a i l a b l e M R I c o u l d p l a y a n i m p o r t a n t r o l e i n d e t e c t i n go s t e o m y e l i t i s s i n l e p r o s y p a t i e n t s w i t h l o n g s t a n d i n g n e u r o p a t h i c f e e t ,s u s p e c t e d d f o r o s t e o m y e l i t i s .REFEREN ES S1.. Br an ds m a JW, Macdonald MRC, Warren AG, Cross H, Sch wa rtz RJ, Solomon

S,, Kazen R, Gravem PE, Shrinivasan H. Assessment and examination of theneurologicallyy impaired foot. Leprosy Review 2001; 72:263-275.

2.. Br ash PD, Foster JE} Anthony P, Tooke JE. Magnetic resonance imagingtechniquess demonstrates soft t issue damage in the diabetic foot . Diabet Med1999;; 16:55-61.

3.. Bra sh PD, Foster JE , Ven nart W, Daw J, Tooke JE . Magnetic reso nan ceimagingg reveals Micro-haemorrhage in the feet of diabetic patients with ahistoryy of Ulce ration. Diabet Med 1996; 1 3:9 73- 978 .

4.. Craig JG , Am in MB, Wu K, Eyler WR, va n Holsb eeck MT, Bouffard JA, Shiraz iK.. Osteomyelitis of the diabetic foot: MR imaging-pathologic correlation.Radiologyy 1997; 203:849-855.

5.. Crim JR , Seeger LI. Ima ging ev alu atio n of oste om ye litis. Crit Rev DiagnImagingg 1994; 35:201.

6.. Dixon WT. Simple proton spectroscopic imaging. Radiology 1984;153:189-194. .

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M R II 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 s7 .. F a b e r W R , H o e k s m a AF , v a n d e r K le ij AJ , Ma as M, D i j k s t r a P F . D i ag n o s t i c

p r o c e d u r e s s f or s u s p e c t e d o s t e o m y e l i t i s i n n e u r o p a t h i c fe et of l e p r o s y p a t i e n t s .In t t J L epr 1 99 8 ; 66 :29A .

8 .. G o o d w i n D W , S a l o n e n D C , Y u J S , B r o s c h m a n n J , T r u d e l l D J , R e s n i c k D L .P l a n t a r r c o m p a r t m e n t s of t h e fo ot: M R a p p e a r a n c e i n c a d a v e r s a n d d i a b e t i cp a t i e n t s .. R a d i ol o gy 1 9 9 5 ; 1 9 6 : 6 2 3 - 6 3 0 .

9 .. G u o c h e n g Z , W e n z h o n g L, L i a n g b i n Y , Z h o n g m i n Y , X i a n g s h e n g C , T i s h e n g Z ,G a n y u n n Y . An ep i d em i o l o g i ca l s u rv ey of d e fo rm i t i e s an d d i s ab i l i t i e s a m o m g1 4 , 2 5 7 7 c a s e s of l e p r o s y i n 1 1 c o u n t r i e s . L e p r o s y re v ie w 1 9 9 3 ; 6 4 : 1 4 3 - 1 4 9 .

10. . H o e k s m a A F , F a b e r W R . A s s e s s m e n t of s k i n t e m p e r a t u r e v ia p a l p a t i o n of t h en e u r o p a t h i c c f o o t . 1 s tw o r l d c o n g r e s s of I S P R M 2 0 0 1 .11. . J a c o b S , P a t il M K. S t r e s s a n a l y s e s i n t h r e e - d i m e n s i o n a l fo ot m o d e l s of n o r m a la n dd d i a b e t i c n e u r o p a t h y . F r o n t i e r s o f M e d i c a l a n d B io lo g ic a l E n g i n e e r i n g1999; ; 1-17.

12. . J a c o b S , P a t il M K . T h r e e - d i m e n s i o n a l f oo t m o d e l l i n g a n d a n a l y s i s of s t r e s s e si nn n o r m a l a n d e a r ly s ta g e H a n s e n ' s d i s e a s e w i t h m u s c l e p a r a l y s i s . J o u r n a l o fR e h a b i l i t a t io nn R e s e a r c h a n d D e v e l o p m e n t 1 9 9 9 ; 3 6 : 2 5 2 - 2 6 3 .

13 . . L i p m an B T, C o l l ie r B D, C a r r e ra G F , e t a l . De t ec t i o n of o s t eo m y e l i t i s i n t h en e u r o p a t h i c c f oo t: n u c l e a r m e d i c i n e , M R I a n d c o n v e n t i o n a l r a d i o g r a p h y . C l i nN u c l e a r r M e d 1 9 9 8 ; 2 3 : 7 7 - 8 2 .

14. . M a a s M , D i j k s t r a P F , A k k e r m a n E M . U n i f o r m f at s u p p r e s s i o n i n h a n d s a n dfee tt t h r o u g h t h e u s e of t wo -p o i n t D i x o n ch em i ca l s hi f t MR i m a g i n g . R ad i o l o g y1 9 9 9 ; ; 2 1 0 : 1 8 9 - 1 9 3 .

15.. M a a s M , S l im F J , A k k e r m a n E M , F a b e r W R . M RI i n c l in i c al ly a s y m p t o m a t i cn e u r o p a t h i c c le p r o s y f ee t: a b a s e l i n e s t u d y . I n t J L e p r o s y a n d O t h e r M y c o b a c tD i s s 2 0 0 1 ; 6 9 : 2 1 9 - 2 2 4 .

16. . M a r c u s C D , L a d a m - M a r c u s V J , L e o n e J , M a l g r a n g e D , B o n n e t - G r a u s s e r a n dF M ,, M e n t a n e a u B P . M R i m a g i n g of o s t e o m y e l i t i s a n d n e u r o p a t h i co s t e o a r t h r o p a t h yy i n t h e f ee t of d i a b e t i c s . R a d i o g r a p h i c s 1 9 9 6 ; 1 6 : 1 3 3 7 - 1 3 4 8 .

17. . Mo o re TE , Yu h W TC , Ka t h o l MH , E l -K h o u ry GY, C o r s o n J D . A b n o rm a l i t i e s o ft h ee fo o t i n p a t i en t s w i t h d i ab e t e s m e l l i t u s : f i n d i n g s o n MR i m ag i n g . AJ R 1 9 9 1 ;1 5 7 : 8 1 3 - 8 1 6 . .

18.. M o r r i s o n W B , L ed e r m an n HP , S c h w e i t z e r ME. MR i m ag i n g of t h e d i ab e t i c fo ot .M R I I C l i n N o r t h A m 2 0 0 1 ; 9 : 6 0 3 - 6 1 3 .

19. . M o r r i s o n W B , L e d e r m a n n H P , S c h w e i t z e r M E . M R i m a g i n g o f i n f l a m m a t o r yco n d i t i o n s s o f t h e an k l e an d foo t. MR I C l i n No r t h Am 2 0 0 1 ; 9 : 6 1 5 -6 3 7 .

2 0 . . M o r r i s o n W B , S ch w e i t ze r ME, B o c k GW , Mi t ch e l l DG, H u m e EL , P a t h r i a MN,R e s n i c k k D . D i a g n o s i s of o s t e o m y e l i t i s : U ti li ty of f a t - s u p p r e s s e dc o n t r a s t - e n h a n c e d d M R i m a g i n g . R a d io l og y 1 9 9 3 ; 1 8 9 : 2 5 1 - 2 5 7 .

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Chapterr 42 1 . . Mo r r i s o n W B , S ch we i t ze r ME, Gran v i l l e B a t t e W , R ad ack DP , R u s s e l KM.

Os t eo m y e l i t i ss of t h e fo ot : r e l a t i v e i m p o r t an ce o f p r i m ary an d s e co n d a r y MRi m a g i n g g s i g n s . R a d i o l o g y 1 9 9 8 ; 2 0 7 : 6 2 5 - 6 3 2 .

2 2 . . On v l ee GJ . Th e C h a rco t F o o t ; a c r i t i c a l r ev i ew an d o b s e rv a t i o n a l s t u d y o f ag r o u pp o f 6 0 p a t i e n t s , Th es i s 1 9 9 8 .

2 3 . . P e te rf y C G , L i n a r e s R, S t e i n b a c h L S . R e c e n t a d v a n c e s i n m a g n e t i c r e s o n a n c ei m a g i n gg of t h e m u s c u l o s k e l e t a l s y s t e m . R a d C li n N o r t h A m e r i c a 1 9 9 4 ;3 2 : 2 9 1 - 3 1 1 . .

2 4 . . R es n i ck D , N i w ay a m a G . D i ag n o s i s of b o n e an d J o i n t d i s o rd e r s 3 rd ed i t io n v ol4 .. C h a p t e r 6 6 : Os t e o m y e l i t i s , s ep t i c a r t h r i t i s an d s of t t i s s u e i n f ec t i o n :O r g a n i s m s .. W B S a u n d e r s C o m p a n y P e n s y l v a n i a 1 9 9 5 ; 2 4 8 6 - 2 4 9 2 .25 . . R i d l ey DS , J o p l i n g W H. C l a s s i f i c a t i o n o f Lep ro s y acco rd i n g t o i m m u n i t y . Af i ve - g ro u pp s y s t e m . I n t e r n a t i o n a l J o u r n a l of L e p r o s y a n d O t h e r M y c o b a t e r i a lD i s e a s e s s 1 9 9 6 ; 3 4 ( 3 ) : 2 5 5 - 2 7 3 .

26 . . S c h o n LC , E a s l e y M E , W e i n fe ld S B . C h a r c o t n e u r o a r t h r o p a t h y of t h e fo ot a n da n k l e .. C l i n ic a l O r t h o p a e d i c s a n d R e l a te d R e s e a r c h 1 9 9 8 ; 3 4 9 : 1 1 6 - 1 3 1 .

27 . . T e h r a n z a d e h J , W o n g E , W a n g F , S a d i g h p o u r M . I m a g i n g o f o s t e o m y e l i t i s i nt h e e m a t u r e s k e l e t o n . M RI C l in N o r t h A m 2 0 0 1 ; 3 9 : 2 4 0 - 2 5 0 .

28 . . T o m as MB , P a t e l M, M arwi n S E , P a l e s t r o C J . Th e d i ab e t i c foo t. Th e B r i t i s hJ o u r n a ll o f R a d i o lo g y 2 0 0 0 ; 7 3 : 4 4 3 - 4 5 0 .

29 . . W o r l d Hea l t h Org an i za t i o n . W eek l y ep i d em i o l o g i ca l r e co rd , 2 0 0 2 ; 77(1}: 1-8.h t t p : / / w w w . w h o . i n t / w e r r

3 0 . . Y u J S . D i a b e t ic fo ot a n d n e u r o a r t h r o p a t h y m a g n e t i c r e s o n a n c e i m a g i n ge v a l u a t i o n . . T o p i c s i n M a g n e t i c R e s o n a n c e I m a g i n g 1 9 9 8 ; 9 : 2 9 5 - 2 3 0 .

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