INTERNATIONAL JOURNAL OF LEPROSY Volume 70, Number 2Printed in the U.S.A.

(ISSN 0148-9I6X)

INTERNATIONALJOURNAL OF LEPROSY

and Other Mycobacterial Diseases

VoLumE 70, NUMBER 2^ JUNE 2002

MR Imaging of Neuropathic Feet in Leprosy PatientsWith Suspected Osteomyelitis'

Mario Maas, Erik J. Slim, Agnes F. Heoksma, Ad J. van der Kleij,Erik M. Akkerman, Gerard J. den Heeten, and William R. Faber 2

The invasion by Mycobacterium lepmeof Schwalm cells with the resulting periph-eral nerve damage can lead to a so-calledneuropathic foot. Ulceration and infection(cell ulitis or osteomyelitis) are importantcomplications. Repeated injury secondaryto the neuropathy may lead to tarsal disinte-gration with osteolysis, fragmentation andprogressive bone resorption. In extremecases, dissolution of the mid-foot results inseparation of the forefoot and the hindfoot,changing all biomechanics and weight bear-ing areas ( 1,11,12, 22‘ .) The neuro-osteoarthro-pathy in the foot is a cause of considerablemorbidity in leprosy ( o. 12, 22, 26 ,) Therefore,when a patient with a neuropathic foot pre-sents himself with a warm foot, it is a clini-

' Received for publication on 8 March 2002. Ac-cepted for publication on 13 May 2002.

=Mario Maas, M.D.; Erik J. Slim, M.D.; Erik. M.Akkerman, Ph.D., and Gerard J. den Heeten, M.D.,Department of Radiology, Suite G1-231: William R.Faber, M.D.. Department of Dermatology: and Ad J.van der Kleij, M.D., Department of Surgery, AcademicMedical Center, Meibergdreef 9. 1 105 AZ AmsterdamZuidoost, The Netherlands. Erik J. Slim, M.D. andAgnes F. Hoeksma, M.D., Department of Rehabilita-tion, Jan yen Breemen Institute, Amsterdam, TheNetherlands.

Reprint requests to Dr. M. Maas, at above address.Telephone: 31-20-5668698; FAX: 31-20-5669119; ore-mail: m.maas@amc.uva.n1

cal challenge to discriminate betweenneuro-osteoarthropathy and an ongoing os-teomyelitis. Especially, this is difficult in thepresence of an ulcer, because an ulcer itselfleads to increased local temperature (10, 22).

Various diagnostic modalities have beeninvestigated in the analysis of osteomyelitisin neuropathic feet (5, 13, 24, 26‘ .) MagneticResonance Imaging (MRI) has been de-scribed as an important modality to assessosteomyelitis in the neuropathic foot of dia-betic patients (16, 18, 19, 20, 2_7) . Tissue charac-terization and spatial resolution facilitateidentification of associated soft tissuepathology ( 2 .'. 4 ' 16' 3"). To detect subtle bonemarrow pathology, such as a low-gradechronic infection, it is mandatory to use fat-suppression sequences with the use ofcontrast administration ( 1 ". 2ft 2 '). A homoge-neous fat-suppression in the entire field ofview, both before and after intravenous con-trast material (Gadolinium-chelate [GO, isrequired to avoid artifacts and misreading(23). This can adequately be achieved by theuse of Two Point Dixon Chemical ShiftImaging (TPDCS1) ( 14 . ' 9).

The radiological literature available onMRI and osteomyelitis in neuropathic feetnearly exclusively concerns diabetic footpathology, being the most frequent cause ofneuropathic feet in the western world.

97

98^ International Journal of Leprosy^ 2002

However, leprosy is an important cause ofneuropathic feet worldwide. According tothe latest World Health Organization( WHO) information at the end of 2000,597,232 cases were on treatment, and719,330 new cases were reported ( 2 ").

Literature concerning MRI and leprosy isscarce. Recently, an MRI study of neuro-pathic leprosy feet without clinical signs ofinflammation was published (''). As far aswe know, no papers concerning, the use ofMRI in neuropathic leprosy feet, clinicallysuspected of osteomyelitis, exist. In this pa-per we present our results with MRI in lep-rosy patients with neuropathic feet clini-cally suspected of having osteomyelitis.The purpose of this study was to analyze thevalue of MRI in diagnosing osteomyelitis asa single diagnostic procedure. The MRIfindings are compared to the signs describedin literature for evaluating osteomyelitis.These MRI results were compared to thegold standard (bone biopsy or bone culture)or, when no gold standard was available, theMRI results were compared to the clinicaloutcome after 6 months.

MATERIALS AND METHODSPatients. We retrospectively evaluated

all consecutive MRI studies, following theDixon protocol (see later) of the foot in lep-rosy patients performed in the period1994-2000. All patients had long-standingneuropathic foot pathology and were clini-cally suspected of having inflammation;they had a neuropathic warm, swollen footthat did not respond to conservative weightreduction therapy. A neuropathic foot wasdefined as a foot in which one or more ofthe neuronal functions, i.e., sensory, motorfunction or autonomic functions, was dis-turbed (consensus of the Dutch NeuropathicFoot Society) ( 7 ). Furthermore, the clinicalfollow up had to cover a period of 6 months.

Clinical criteria. Patient charts were re-viewed for clinical information concerning,leprosy classification ( 25 ), presence and loca-tion of an ulcer and clinical signs of inflam-mation. Twelve patients with neuropathicfeet clinically suspected of having os-teomyelitis were investigated, and 19 MRIstudies were performed. The patients wereclassified as borderline lepromatous (n = 3),borderline tuberculoid (n = 1), and at thelepromatous side of the spectrum (n = 8).

TABU. i . Results' of clinical JO1low-updiagoilo.s . ing asleomyclitis.

Eve n t Gold standard Clinical outcome

1 PusPos

3 Pos4 Pos5 Pos6 Pus7 Pus8 Pus9 PosI() Pus11 Pos12 Pus13 Neg14 Pus15 Neg16 Pus17 Pus18 Pus

The gold standard for the diagnosis ofosteomyelitis was a positive culture and/orhistopathology taken from bone material.Clinical outcome after a 6-month follow-upwas retrospectively evaluated in caseswhere histopathology or culture was notavailable or not conclusive. A combinationof clinical criteria was evaluated in a con-sensus reading by a dermatologist (WRF), aphysiatrist (AFH) and a surgeon (AjvdK).The clinical criteria evaluated were the re-sponse on antibiotic treatment, the nature ofthe surgical treatment when performed, thepersistent signs of inflammation, the statusof the ulcer, and the change in deformity.

Diagnostic criteria (MRI). A total num-ber of 24 MRI studies in 12 adult leprosypatients (9 male, 3 female; mean age 63years, age range 45 years-81 years) wereincluded for evaluation. Of these 24 MRIstudies, 18 were performed because of clin-ical suspicion of osteomyelitis. Follow-upMRIs were performed in 6 patients.

MRI. MRI examination was performedusing a 1.5 Tesla Vision (Siemens, Erlangen,Germany). All MRI studies were performedfollowing the Dixon protocol (('' 14. 1' ). Thisprotocol consisted of: Sagittal Turbo-STIR(short tau inversion recovery) (3 mm), T1-weighted Dixon sequence with in- and op-posed-phase images, sagittal dual echo T2-Weighted FSE (Fast Spin Echo) (3 mm); af-ter the intravenous administration of

69, 2^ M(I(I.S, et al.: MR Imaging^ 99

TABLE 2. Primary MRI^numbergif posltire .findings on various MRI se-quence,s'.

Positive primary sign Number (%. ) of MR Is

1 . 1 16 (88.9(4)T2 13 (72.2%)STIR 13 (72.2%)Contrast 17 (94.4%)

Gadolinium chelate (0.1 mmol/kg Of bodyweight) TI-weighted Dixon sequence within- and opposed-phase images (o). ' 5 ).

To evaluate the MRI studies, signs wereused as described in literature concerningdiabetic neuropathic feet (►'). Typi-cal, primary MRI signs are decreased mar-row signal intensity on T 1 -weighted im-ages. increased signal intensity on fat sup-pressed T2-weighted and/or fast STIRimages, and focal marrow enhancement al-ter gadolinium-enhanced fat-suppressedT 1 -weighted images 17- 2(1. "). Sec-ondary MRI signs are: the presence of a cu-taneous ulcer, cellulitis, a soft tissue mass, asoft tissue abscess, a sinus tract, and corti-cal interruption ('''"). One musculoskeletalradiologist (MM) retrospectively evaluatedthe images blinded to all clinical informa-tion except the knowledge of clinical suspi-cion for osteomyelitis. The signal intensityof the hone marrow on Tl-weighted in andout of phase Dixon images, fast STIR im-ages and gadolinium enhanced Tl-weightedin and out of phase Dixon images (ptiii -larysigns) was classified as normal or abnormalon a data collecting form. The secondarysigns were classified as present or absent.Furthermore, the site of involvement wasnoted (medial arch. central compartment orlateral arch) ' 2 ).

RESULTSClinical findings. In 8 patients there was

one event of suspected osteomyelitis. Infour patients there were multiple events ofsuspected osteomyelitis -, in three patientsthere were two events of suspected os-teomyelitis, and in one patient there werefour events of suspected osteomyelitis. Thefoot of involvement was 6 times for theright and 12 times for the left. The locationof the ulcer was at the lateral side 14 times,at the medial side two times. and an ulcer

TABLE 3. Presence of positive secon-dary MRI signs.

Positive secondary sign Number ((%) of MRIs

Cellulitis 18 (1()()%)Ulcer 18 (100%)Cortical interruption 17 (88.9% )Sinus tract 5(27.7)Solt tissue abscess 3 (16.6%)Soil tissue mass 2(11.1%)

was present at the medial and lateral sidetwo times.

The results of the gold standard are listedin Table 1. When evaluating, results from ahone biopsy or bone culture and/or presetclinical criteria, without detailed knowledgeof the MRI results, the diagnosis of os-teomyelitis was made in 16 of 18 events(88.9%).

Diagnostic findings (MRI). In 18 eventsof suspected osteomyelitis we encountered17 MR1 examinations which were positivefor priinary MRI signs of osteomyelitis(94.4%), decreased signal on Tl in and outof phase on 16 MRIs (88.9% ). increasedsignal oil T2 on 13 MRIs (72.2%), fast SESTIR on 13 MRIs (72.2%), and localizedmarrow enhancement after gadolinium-en-hanced, fat-suppresed Tl on 17 MRI(94.4%) (Table 2).

The secondary signs were positive in allMRI examinations (100%). Cellulitis waspresent in all cases (100%). A cutaneous ul-cer in the region of the suspected os-teomyelitis was also present in all cases(100%). Cortical interruption was found in16 investigations (88.9%). A sinus tract waspresent in 5 cases (27.7%). A soft tissue ab-scess was present in 3 cases (16.6%). A softtissue mass was found on two occasions(11.1%) (Table 3 ). An example of positiveprimary signs and secondary signs at the lat-eral side of the foot is shown in The Figure.

The sites of involvement (MRI). Themedial-central-lateral sites of involvementwere also analyzed. The areas of os-teomyelitis were located at the medial site(MTP 1 joint, Os metatarsal 1, cuneiform 1.navicular hone) in 3 events, the medial/cen-tral in 2 events, the central ( MTP 2-3, Osmetatarsal 2-4) in 3 events, and the lateral(MTP 4-5 .joint, os metatarsal 4-5, cuboid.calcaneus ) in 9 events. In one patient allthree areas were involved.

100 hitermilional .10111 -11(11 of Lepro.sy^ )002

THE Fic;t A = Two point Dixon Lit suppres-sion image of the right foot of a 79-year-old l'emale pa-tient. Note the degradation of the plantar fat with thepresence of soft tissue edema (interrupted arrow) andthe high signal intensity in the partly destroyed cuboidbone (non-interrupted arrow). B = Same patient afterintravenous gadolinium chelate administration. Notethe marked enhancement at the Literal side of the footboth in the soft tissue (cellulitis) (interrupted arrow)and in the cuboid bone (osteomyelitis) (non-inter-rupted arrow).

Follow up (MRI). Six follow-up MRIswere made after antibiotic treatment. Themean time of follow up was live months. Acomplete healing of the ulcer occurred intwo patients with a normal follow-up MR1.Two patients had an improved but still ab-normal MRI. The MRI changes that wereseen were a reduction, but still present zoneof enhancement of the hone marrow. Bothpatients eventually showed a complete clin-ical remission. The foot of the patient thatshowed an unchanged follow-up MRI de-spite continued antihiotics eventually wasamputated.

DISCUSSIONOsteomyelitis is a well-known complica-

tion in patients with neuropathic footpat h o l ogy ( 4.13. 1(,, 1'). 2(), 24. 26, 28, 30 ,) These pa-tients may develop ulcers that persist over along period of time. In this way spread ofinfection per con/lint/la/ern can cause an in-fection of the osseous structures in the foot.Clinical examination kicks specificity inthis patient group, since by clinical exami-nation alone it is difficult to differentiate be-tween cellulitis, osteomyelitis and neuro-osteoarthropathy ( 2 . 2"). MR imaging is apotentially powerful tool in the evaluationof the neuropathic foot. It is useful for theevaluation of the presence and the extent ofosteomyelitis, as well as for the identifica-tion of the presence and the extent of asso-ciated soft tissue abnormalities that mayhave clinical importance, such as cellulitis,abscess, and sinus tract ( 4-1 ' 1 ' I ' "-3()).Nearly all data available on MRI and neu-ropathic feet concern patients sufferingfrom diabetes. As far as we know, this is thefirst report on the use of MRI as a diagnos-tic procedure in neuropathic leprosy feetsuspected Of having osteomyelitis.

When analyzing the primary MRI signsfor osteomyelitis, we found that in ourpopulation that in 17 out of 18 events(94.4%) primary MRI signs were positive.A decreased signal intensity on in and outof phase Tl-weighted images and the mar-row enhancement after gadolinium admin-istration on fat-suppressed T1 were themost frequently encountered abnormalities.In our retrospective analysis (gold standardand/or clinical outcome), 16 out of 18events were diagnosed as positive for os-teomyelitis. Comparing, this evaluation with

69, 2 Maas, et al.: MR Imaging^ 101

the primary MRI signs, there was agree-ment in 17 out Of 18 events. The disagree-ment found in one patient was caused bythe primary MRI sign Of focal marrow en-hancement after contrast administration.Therefore, we conclude that these pri narysigns, used in evaluating MRI examinationsin diabetics, can adequately be used to ana-lyze MRI examinations in leprosy patientswith long-standing complicated neuro-pathic feet.

of the secondary MRI signs, ulcer andcellulitis were present in all cases. The ar-eas on each MR1 suspected of osteomyelitiswere in continuity with the ulcer. The rela-tion between ulcer and osteomyelitis hasalso been described in diabetes (s). In con-trast to diabetic feet only a minority of ex-aminations revealed a sinus tract or soft tis-sue abscess in our population ( 2 '). It seemsthat these latter secondary signs are infre-quently found in leprosy. However. thepresence of an ulcer and cellulitis is com-mon in leprosy patients with long-standingneuropathic feet suspected of having os-teomyelitis. Contrary to diabetic foot litera-ture, the secondary MRI signs seem to haveno additional value in diagnosing osteo-myelitis in a population of leprosy patientswith long-standing neuropathic foot disease.However, the value of these findings in a pa-tient population of leprosy patients withneuropathy and clinical suspicion of inflam-mation, without long-standing disease, wasnot evaluated in this study. For this purposea study is currently being conducted.

The present study demonstrates in 9events MRI changes suspected of havingosteomyelitis were seen on the lateral sideonly (50%). In a minority of events thesechanges were found on the medial side only(16.7%). This is in contrast to the resultsfound in a recent study of asymptomaticneuropathic feet in leprosy patients inwhich 90 percent of the MRI changes werelocated on the medial side of the foot W).Most likely the biomechanics in the two pa-tient groups (clinically-unsuspected versusclinically-suspected in long-standing neuro-pathic foot disease) are different. Biome-chanical analysis in early tarsal disintegra-tion shows the highest stress to occur dur-ing the push-off phase in the hones of thelateral foot arch ('). Perhaps this is causedby inversion due to ixtralysis of the lateral

musculature. An analysis of the walking cy-cle in two groups of leprosy patients withneuropathic feet, with and without clinicalabnormalities, may he of additional value inorder to analyze the stress distribution.

When a leprosy patient With long-stand-ing neuropathic foot disease is suspected ofosteomyelitis, clinical examination lacksspecificity. Contrast-enhanced MRI with theuse of Two Point Dixon Chemical Shift Imag-ing. as a fat-suppression technique, is a valu-able technique to detect osteomyelitis. Theprimary MR1 signs known from literatureconcerning the diabetic neuropathic footcan adequately he assessed. MRI can serveas a one-step diagnostic strategy to diag-nose osteomyelitis in leprosy patients witha long-standing neuropathic toot problem.

SUMMARYThis study was undertaken to analyze

MRI findings in leprosy patients with neu-ropathic feet, which are suspected of havingosteomyelitis. As far as we know, there isno literature concerning osteomyelitis andMR1 in neuropathic leprosy feet at present.Therefore, we have included MRI examina-tion of 18 events of suspected osteomyelitisin 12 leprosy patients. All patients withlong-standing neuropathic foot problemswere clinically suspected of having os-teomyelitis. All patients underwent the MRIprotocol with the inclusion of Two PointDixon Chemical Shift Imaging as a fat-sup-pression sequence. For the MRI evaluation,we used signs that are described in litera-ture for detecting osteomyelitis in diabeticfeet. The primary MRI signs were positivein 17 of 18 patients. The secondary MRIsigns were positive in 1 0O%% of the patients.

Our results show that MRI with the useof Two Point Dixon Chemical Shift Imag-ing is a promising diagnostic modality to de-tect osteomyelitis ill the presence of neuro-steoarthropathic changes in patients withleprosy. Whenever available, MRI couldplay an important role in detecting osteo-myelitis in leprosy patients with long-stand-ing neuropathic feet.

RESU MENEste estudio se realizO con el lin de amtlizar los hal-

lazgos poi - NiR I en los pacientes con lepra y pie neu-ritico, sospechosos de teller osteomielit is. Hasty dondesahemos, actualmente no hay &aos la literatura

In

102^ hiternotiona/ .1011/71(1/ efLepras'y^ 2002

relacionados con la osteomiclitis y MRI Cn el pie neu-ropatico de la lepra. Por to tanto, incluimos el examenpot MRI de 18 eventos sospechosos (IC osteomiclitisen 12 pacientes con lepra. Thdos los pacientes conprohlemas neuropaticos (lel pie de durackin seconsideraron conk) candidatos de teller osteomiclitis.Todos los pacientes se sometieron al protocol° MRIcon la incluskin del :inOlisis de Dixon de dos puntos( -Two Point Dixon ('hk.mlical Shift Imaging - ) comouna secuencia de supresiOn de grasa. Part evalltal losresult:tdos del estudio por MRI usamos Is signos de-scritos en la literatura para detector la osteomiclitisel pie diabetico. I.os signos MRI priniarios lucron pos-iliVOS ell 17 de 18 pacientes. Los signos Ni RI secun -darios fueron positives en el 1()()(; de los pacientes.

Nuestros resultados muestran que el MRI :timadouse del analisis de Dixon de dos puntos es unaidad diagikistica promisoria para detect:tr ostcomicl it iscuando hay cambios neuro-osteoartropaticos en los pa-cientes con lepra. La aplicaciOn de esta metodologia,siempre que sea posihle. puede jugar tin impel i mpor-tante en la deteeckin de osteomiclitis en los pacientescon lepra y pie neuropatico de largo durackin.

RESUMECelle etude tut entreprise dans le but d'analyser les

donnees d' IRM obtenues chez les patients lepreux at-teints de neuropathies des picds et suspectes de souffrird'osteomyelite. A noire connaissance, it n'existe pasactuellement de litterature rapportant des donneesd'IRM sur les osteomyelites, comme complication deneuropathies des pieds dans la lepre. C'est pourquoinous avons inclus on examen IRM lors de la caracteri-sation de 18 suspicion d'osteomyelite concernant 12patients hanséniens. Tons les patients souffrant deproblemes de neuropathic podale de longue dureefirent r ohjet cr une suspicion d'osteomyelite. Thus ICspatients furent soinnis a till protocole 1RM, 'nekton(tine imagerie de type &placement chimique en deuxpoints selon Dixon ( -Two Point Dixon Chemical ShiftImaging- ), comme sequence de suppression du tissuadipeux. Pour evaluation IRM, nous avons utilise lessignes decrits dans la litterature pour &teeter les os-teomyelites des pieds diabetiques. Les signes IRMprincipaux etaient detectes chez 17 des 18 patientsetudies. Les signes IRM secondaires etaient presentschez 100 (les patients.

Nos resultats demontrent que L'1RM, avec [utilisa-tion de 1' itnagerie de type &placement chimique deDixon en deux points, est till outils diagnostic promet-teur pour &teeter Line osteomyelite en presence designes neuro-arthrosiques chez les patients lepreux. L'ap-plication de la technologie IRM. Iorsque disponible,pourrait jouer tin rule important pour détecter une os-teomyelite chez les patients atteint de la lepre, qui soul-frent depuis longtemps de neuropathies des pieds.

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