PICTORIAL REVIEW

Pelvic heterotopic ossification: when CT comes to the aidof MR imaging

Andrea Zagarella & Elisabetta Impellizzeri & Roberta Maiolino &

Raffaele Attolini & Maria Chiara Castoldi

Received: 18 April 2013 /Accepted: 4 June 2013 /Published online: 5 July 2013# The Author(s) 2013. This article is published with open access at Springerlink.com

AbstractObjective This article compares various imaging aspects ofmagnetic resonance (MR) and computed tomography (CT)of heterotopic ossification (HO) in the pelvic soft tissues inparaplegic patients. Our aim is to highlight the benefits ofintegratingMR and CT imaging in the diagnosis of immatureHO, which may be challenging with MR images alone.Methods Paraplegic patients examined on the same day bycontrast-enhanced 0.4-T pelvic MR and unenhanced CT forpressure-sore-related infections were selected. MR imagingwas performed on a Hitachi-Aperto 0.4 T; the Open Magnetserved as a more favourable configuration for the requiredlimb positioning of these patients. CT images were attainedon a six-slice Siemens-Somaton-Emotion.Results MR images of HO differ according to the degree ofbone maturity. The more immature the HO process, the moreheterogeneous is the signal, characterised mostly by focaliso-hypointensity on T1-weighted images and hyperintensityon T2-weighted/short TI inversion recovery (STIR). Thesecharacteristics correlate to different CT patterns.Conclusions MR and CT features of pelvic HO in paralysedpatients were reviewed with a focus on the different aspectsassociated with the degree of ossification. Based solely onthe MR findings, immature heterotopic ossification may bedifficult to differentiate from other soft tissue pelvic lesions.Teaching points• The pelvis and hip are common locations of heterotopicossifications (HO), often occurring in paraplegic patients.

• With respect to HO, MR imaging allows for a confidentdiagnosis in mature ossified lesions only. The MR aspect ofimmature ossification may be confused with otherpathologies.

• Plain radiographs and CT may show various phases ofossification: amorphous calcification, immature and ma-ture ossification.

• Integrating MR with CT can help recognise HO foci anddifferentiate them from infections and other soft tissuelesions.

Keywords Musculoskeletal . Neuro . CT .MR

Introduction

Heterotopic ossification is the development of bone in ab-normal sites. It may originate at any extraskeletal locationwhere undifferentiated mesenchymal cells are found.

While its etiopathogenesis is unknown, it is likely thatmore than one factor (vascular stasis, low tissue oxygena-tion, microtraumas) contributes to activation of osteoblastand chondroblast progenitor cells with a consequent precip-itation of calcium salts within the connective tissue [1–3].Clinically, heterotopic ossification (HO) occurs in rare con-genital disorders and, more commonly, in acquired condi-tions such as after surgery or related to spinal cord or headlesions. This latter condition, called neurogenic heterotopicossification, is the topic of this article.

Ossifying lesions run along an ossification continuum:amorphous calcification, to immature ossification, to matureossification.

MR imaging alone allows easy recognition of matureossifications; however, amorphous calcification or immatureossification shows non-specific signal and contrast enhance-ment features. Thus, since enhanced MR imaging is routine-ly performed on paraplegic patients with infection of the

A. Zagarella (*) : E. Impellizzeri : R. Maiolino :M. C. CastoldiRadiology Department, Istituti Clinici di Perfezionamento diMilano, C.T.O., Via Bignami 1, 20162 Milan, Italye-mail: andrea.zagarella@icp.mi.it

R. AttoliniParaplegic Unit - Orthopedic Surgery Department, Istituti Clinici diPerfezionamento di Milano, C.T.O., Via Bignami 1, 20162 Milan,Italy

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pelvis, the differential diagnosis between HO and other softtissue diseases can be problematic. Plain radiographs and CTcan help in identifying the ossifying process showing pecu-liar morphological characteristics related to the degree ofmaturity.

In this review article, we describe our experience withpelvic imaging in paraplegic patients. We focus on differentHO features through a simultaneous comparison of MR andCT findings.

All examined patients underwent both a contrast-enhancedMR scan and an unenhanced CT scan on the same day.All patients were scanned on a 0.4-T open magnet toaccommodate required patient positioning. Our goal inthis review is to underscore the importance of integrat-ing MR imaging with CT to differentiate HO from otherprocesses in the clinical management of paraplegic pa-tients. More generally, integrated imaging can be helpfulwhenever an ossifying process may be expected in thepelvis and/or around hip joints.

HO in paraplegia

HO is frequently observed in paraplegic patients with spinalcord lesions of traumatic or atraumatic origin. Its incidencevaries from 15 % to 35 % [1–3]. This phenomenon is mostlyobserved about larger joints, hips being the more affectedsite.

The cause of HO in paraplegia is unknown. Tissue dener-vation, oedema, and vascular stasis are all considered relatedto the formation of HO that usually occurs without precipi-tating trauma. Nevertheless, some authors have hypothesisedthat microtrauma may play a role in the etiopathogenesis ofneurogenic HO stemming from passive physiotherapy jointmanipulation [4].

Initial clinical findings of HO relate to the inflammatoryprocess, and are characterised by local swelling, redness,muscle spasms and pain. Early in the clinical setting HOmay be confused with infection, fracture or neoplasia [3].The inflammatory process then evolves to the formation of a

Fig. 1 A 58-year-oldparaplegic man, post trauma.a On axial STIR a diffuseincreased signal intensityinvolving the right obturatorexternus-adductor musclessuggests an inflammatoryreaction as observed in the earlyphase of ossification. b On CTaxial scan a circumscribedamorphous calcificationshowing ill-defined margins andno trabecular structure isevident within the periphery ofthe adductor brevis muscle belly

Fig. 2 A 55-year-oldtetraplegic male patientfollowing vertebral trauma.aAxial CTscan shows a bilateralossifying process about thefemural metaphyseal region withsome amorphous calcificationsin the ileopsoas muscle area. Aleft throcanteric calcific bursitisis also observed. b–d MRimaging: (b) axial STIR and (c)T1-weighted axial images showbilateral ileopsoas bursitis (smallarrows) on the right merging to amature ossification. d T1-weighted fat-suppressed imagesafter contrast administrationshow, on the right side,peripheral enhancement of thebursal walls (large arrow)

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connective mass with progressive deposition of bone tissue.In this phase, HO can cause motion restriction, joint anky-losis and decubiti. In fact, as many as 5–10 % of patientsdevelop complete hip ankylosis [1, 2, 4, 5]. Typically, HOdevelops between 1 and 5 months after spinal injury, and cancontinue to be active even 5 years after the onset of paraple-gia [6]; in some cases, it never reaches complete maturity [7].On radiographic imaging, HO foci vary in size and shape,and can range from a thin, 1-mm-long strip to a mass ofmany centimetres in diameter.

HO distribution and sites of origin

The most common sites of neurogenic pelvis ossification arethe iliac, ileopsoas or vastus muscle areas [7].

According to the literature, the initial HO process canoriginate inside a muscle or extend into a bursa [2]. Incases of primary muscle involvement, initial ossificationstarts in the peripheral tissue due to oedema and capil-lary stasis following muscle denervation [3]. The path-ogenesis of HO is similar to that of circumscribedmyositis ossificans [8–10]; therefore, it manifests many

of the same imaging features, including T2/short TI inversionrecovery (STIR) hyperintensity and some peripheral enhance-ment. Muscles initially involved in the ossification processshow diffuse hyperintensity on T2/STIR images with or with-out some heterogeneity within them. The corresponding CTappearance consists of a certain degree of swelling of themuscle, which can contain some peripheral calcification orimmature ossification (Fig. 1).

Bursae are other sites where HO can take place initiallyand progress to compression of the adjacent muscles [11].Some areas of elevated signal intensity on T2-weightedimages with rim contrast enhancement may represent fluid-filled merged bursae or inclusion within the ossification itself(Fig. 2). In cases of primary bursal involvement, it is notalways possible to differentiate HO from pressure-relatedcalcified bursitis that can evolve in ossification [2] (Fig. 3).

Our patient population showed immature HO either in themuscle and fascia or in the bursae; however, we never foundmature HO limited to the bursae. We assume that with in-creased maturity, HO formations tend to coalesce and adhereto the contiguous bone, which fades anatomic landmarks. CTimaging can easily identify calcium deposits inside a muscleor calcification/ossification at the anatomical site of a bursa, asis usually observed in initial soft tissue ossification.

Imaging findings

Imaging can assist in the identification of three degrees ofHO: amorphous calcifications, immature calcifications andmature calcifications [7].

Both plain radiographs and CT imaging are the stan-dard references to assess HO maturity, since CT moreaccurately defines the different stages of ossification than doplain radiographs.

Amorphous calcification is poorly defined with norecognisable trabecular structure (Fig. 4a); immature ossification

Fig. 3 A 62-year-old male patient with traumatic paraplegia. CT im-aging shows soft-tissue thickening adjacent to the great trochanter dueto bursitis. An immature ossification with an initial trabecular structureand faint margins is evident within the paratrochanteric bursa

Fig. 4 Different patterns of HO maturity shown on CT. a Amorphouscalcification located within the right quadratus femoris muscle,characterised by ill-defined margins and no recognisable trabecularstructure. b Immature ossification located within the right medius

gluteus muscle. Lesion shows poorly-defined margins and an initialtrabecular formation is recognisable. c Mature ossification locatedwithin the left ileopsoas muscle, outlined by cortex with well-definedcancellous bone inside

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shows poorly defined margins and initial trabecular formation(Fig. 4b); mature ossification is characterised by a corticaloutline with a well-defined cancellous bone centre (Fig. 4c).The morphological difference between amorphous calcifica-tion and immature ossification is not always sharp, and differ-ent degrees of maturity often coexist (Fig. 5).

At MR imaging, mature HO presents as typical cancellousfat bone that is hyperintense on T1- and T2-weighted images,outlined by a rim of hypointense cortical bone. At CT, thisfinding corresponds to bone formation characterised by corti-cal and trabecular structure. Amorphous calcification and

immature HO can present non-specific signal intensity andcontrast enhancement characteristics [2]. In cases of boneprocess immaturity, the formation can show hetereogeneoussignal, characterised mostly by focal iso-hypointensity on T1-weighted images and hyperintensity on T2-weighted/ STIRimages, with occasional fluid contents. A certain amount ofenhancement after contrast administration can occur bothinside and peripheral to the lesion (Figs. 6, 7).

While these findings may present in various combinations(Figs. 8, 9), several conclusions can be formulated. The moreimmature the HO process, the more these non-specific signs

Fig. 5 A 72-year-oldtetraplegic male patient withspinal injury. Different grades ofmaturity may coexist in thesame clinical setting. a AxialCTscan shows an HO formationlocated within the gluteusminimus muscle with the typicalfeatures of maturity: well-structured cancellous boneoutlined by cortex and adherentto cortical bone. Immatureossification and amorphouscalcifications coexist in variousregional muscles. b–d Axialcorresponding MR imagingshows the mature ossificationwith a high-fat bone marrowsignal outlined by low signalcortical bone (c) (small arrow).The amorphous calcificationscontiguous to the posterior iliacbone (large arrow) arecharacterised by elevated signalintensity on STIR images(b) and intense contrast-enhancement on T1-weightedfat-saturated (d) compared withunenhanced T1-weightedimages (c). The small immatureossification in the gluteusmedius muscle (asterisks) isclearly demonstrated by CT(a), while it is not easilyrecognisable on MR imaging

Fig. 6 A 35-year-old maleparaplegic patient after spinalinjury. a First CT axial scanshows swelling andhypodensity of the rightileopsoas muscle. b One-yearfollow-up examination showsthe appearance of an immatureossification within the ileopsoasmuscle

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Fig. 7 The same patient as inFig. 6: the corresponding MRexamination (a, b) performedon the same day as CTexamination shown in Fig. 6b.Muscle swelling andheterogeneity (large arrow) isclearly noticeable on STIRimages (a) and T2-weightedimages (b) associated withinflammatory changes ofcontiguous retroperitoneumtissue (asterisks). A markedintra-articular fluid collection isalso evident to the right of thecoxofemural joint (smallarrows). T1-enhanced (d)compared with T1-weightedunenhanced images (c): after i.v.gadolinium administration, aheterogeneous and prominentcontrast-enhancement is evidentinside the right ileopsoas muscleencircling a “dark spot”corresponding to theossification

Fig. 8 A 41-year-old maleparaplegic following spinaltrauma. a CT axial scan definesa bulky calcific mass locatedwithin the anterior compartmentof the right thigh and the gluteusminimus muscle. On MRimages (b–d), the mass ischaracterised by heterogeneityon STIR (b) and T1-weighted(c) images. d Focal contrast-enhancement appears on T1-weighted imaging following i.v.gadolinium administration(arrows)

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are observed [2]. Similar MR intensity characteristics canalso be found in tumours, local infections and, if fluid ispresent, in abscesses.

When MR imaging reveals a lesion with an indeterminateaspect, CT can aid the diagnosis of HO by detecting amor-phous calcification or immature ossification inside the lesion.

Differential diagnosis and pitfalls

Pelvic imaging of paraplegic patients may reveal masses ofdifferent natures, infection being the main pathology to bedifferentiated from HO. Soft tissue infections and abscessesoften develop in paraplegic patients beneath deep pressuresores [12]. Their evaluation is performed primarily with MRimaging. AsMR imaging can show lesions of different natures,the possibility of misleading features in immature HO shouldbe considered during evaluation of a pelvic MR examinationperformed for an infection process. In these cases, CT imagingis helpful as it reliably detects the initial formation of trabeculeswithin calcific lesions [13]. Nevertheless, the diagnosis of the

nature of a lesion containing amorphous calcifications is notalways obvious because dystrophic calcification may some-times be present in soft tissue infectious processes or in septicbursitis [14] (Fig. 10).

Whenever a certain degree of uncertainty is present indefining the nature of the calcifying lesion, and the clinicalsetting allows a “wait and see” behaviour, carefully timed CTimaging can be helpful. In cases of sterile HO, follow-up CTcan show the initial formation of a trabecular structure,which is a typical aspect of HO in evolution to maturity(Fig. 11). In cases of infection, CT imaging may show somechanges in the ossified mass, such as a more pronouncedfragmentation or even a burst ossification, which defines thediagnosis (Fig. 12).

Furthermore, as shown in Figs. 9 and 10, soft tissueinfection and ossification formation may show peculiar be-havioural patterns with respect to the superficial tissue. Inparalysed patients, deep infection of the soft tissues is usu-ally contiguous to skin ulcers and is always associated withinflammation of subcutaneous tissue since infection spreadsthrough the skin [12]. Conversely, HO originates from deep

Fig. 9 A 61-year-old maleparaplegic patient followingspinal injury. a CT axial scanreveals an elongated ossifyinglesion within the right pectineusmuscle. b On STIR images thelesion (small arrow) isessentially isointense to muscle,while on (d) T1-weightedimages it shows a considerablelow signal intensity). c Nocontrast-enhancement isnoticeable at this site. On the leftischiatic region, a deep infectedsoft tissue ulcer with boneinvolvement is shown (largearrow)

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in soft tissues; involvement of superficial subcutaneouslayers is secondary to fibrotic retractive changes.

Contrary to immatureHO,mature HO is easily recognisableby MR imaging since its signal intensity is similar to that ofnormal cancellous bone outlined by cortex. When thesefeatures of HO appear on MR images, CT is not required, asit offers no additional information.

Treatment

HO may lead to a series of complications, including nerveentrapment, pressure ulcers and joint ankylosis. Consequent-ly, early disease detection is extremely important.

Diphosphonates and non-steroidal anti-inflammatory drugs(NSAIDs) are used for prohylaxis or HO treatment [15].

After diagnosis, passive range-of-motion exercises tomaintain joint mobility are prescribed [16].

When the ossification formation restricts mobility, surgicalresection may be performed to increase joint function. Duringsurgery planning, assessment of the degree of ossification is

crucial, as resection must be performed only when HO ismature. Resection of an ossification process that has reachedmaturity implies less intra-operative complications, such ashaemorrhage or a minor risk of post-operative recurrence [7].On the other hand, excessive surgical delay may expose thepatient to development of joint ankylosis. Imaging plays animportant role in optimising the timing of surgery, and plainradiographs and CT imaging are the most reliable ways toevaluate advanced ossification foci.

Conclusion

Pelvic MRI of paraplegic patients is a diagnostic challenge.Based on MR findings, immature HO may be difficult todifferentiate from other pathologies, such as soft tissue pel-vic infection, abscess and septic bursitis. The radiologistshould be aware of the different aspects of HO at MRimaging. Correlation between MR and CT features is criticalto accurate diagnosis. When dubious findings are present,

Fig. 10 A 35-year-old malepatient with leg contractures,affected by posterior elementincomplete fusion (spina bifidaocculta). a MR T1-weightedaxial images evidence a softtissue abscess (small arrow) ofthe perineal region related topressure sores. Lesion isdetermining a certain retractionover the superficial layers of thedermis. b STIR images show thefocal inflammatory lesionpartially filled with fluid and alarge bursitis of the right glutealregion (large arrow). c Oncoronal T1-weighted fat-satimages after gadoliniumadministration, the abscess wallsappear highly vascularised. Thegluteal bursitis seems to becommunicating with theinfectious process, suggesting aseptic bursitis. A prominentcontrast enhancement is alsoseen to the sacrum, suggesting abony involvement by the septicprocess. d Axial CT imagingperformed with patient in adifferent leg positioning . Theexam validates the connectionbetween the perineal abscess andthe gluteal bursitis. Amorphouscalcifications (asterisks) areenclosed within the septicbursitis at the right gluteal region

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Fig. 11 A 34-year-oldparaplegic male followingspinal cord injury. Examinationswere performed to evaluateabscess and osteomyelitis of theleft ischial tuberosity (largearrow). The MR study reveals alesion in the area of the rightpsoas muscle (small arrow): (a)central hypo-intense area onaxial T1-weighted non-enhanced image (small arrow),(b) enhanced tissue and somefluid after contrastadministration (small arrow).Note that the sterile HO issimilar to the abscess of the leftischial region. c Thecorresponding CT shows themass as non-homogeneous withsome subtle calcifications on themedial side. d The CT studyrepeated 10 months later showstransformation of the immaturebone into a mature, heterotopicossification that adheres to thefemur

Fig. 12 A 30-year-old male patient affected by posterior elementincomplete fusion (spina bifida occulta). a On first CT axial scan abulky immature ossification is revealed adjacent to the left iliac wing.This HO was not comprised into the MR acquisition volume thatwas lower centred because of the clinical relevancy of a posterior

ischiofemural abscess. b A 10-month follow-up CT scan showsthe lesion appears to be fragmented and partially resorbed. Amarked soft tissue swelling is now visible caused by an underly-ing infectious process

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CT scan follow-up is advisable. In advanced ossification,imaging is key to correctly time surgical resection.

Open Access This article is distributed under the terms of the CreativeCommons Attribution License which permits any use, distribution, andreproduction in any medium, provided the original author(s) and thesource are credited.

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