Canadian Association of Radiologists Journal 67 (2016) 28e40www.carjonline.org

Musculoskeletal Radiology / Radiologies musculo-squelettique

Radiology of Osteoporosis

Thomas M. Link, MD, PhD*

Department of Radiology and Biomedical Imaging, University of California at San Francisco, San Francisco, California, USA

Abstract

The radiologist has a number of roles not only in diagnosing but also in treating osteoporosis. Radiologists diagnose fragility fractures with all

imaging modalities, which includes magnetic resonance imaging (MRI) demonstrating radiologically occult insufficiency fractures, but alsolateral chest radiographs showing asymptomatic vertebral fractures. In particular MRI fragility fractures may have a nonspecific appearance andthe radiologists needs to be familiar with the typical locations and findings, to differentiate these fractures from neoplastic lesions. It should benoted that radiologists do not simply need to diagnose fractures related to osteoporosis but also to diagnose those fractures which are compli-cations of osteoporosis related pharmacotherapy. In addition to using standard radiological techniques radiologists also use dual-energy x-rayabsorptiometry (DXA) and quantitative computed tomography (QCT) to quantitatively assess bone mineral density for diagnosing osteoporosisor osteopenia as well as to monitor therapy. DXAmeasurements of the femoral neck are also used to calculate osteoporotic fracture risk based onthe Fracture Risk Assessment Tool (FRAX) score, which is universally available. Some of the new technologies such as high-resolution pe-ripheral computed tomography (HR-pQCT) and MR spectroscopy allow assessment of bone architecture and bone marrow composition tocharacterize fracture risk. Finally radiologists are also involved in the therapy of osteoporotic fractures by using vertebroplasty, kyphoplasty, andsacroplasty. This review article will focus on standard techniques and new concepts in diagnosing and managing osteoporosis.

R�esum�e

Le role du radiologiste ne se limite pas au diagnostic de l’ost�eoporose; il intervient �egalement dans le traitement de cette maladie. Le

radiologiste �emet des diagnostics de fracture de fragilisation avec toutes les modalit�es d’imagerie, y compris par imagerie par r�esonancemagn�etique (IRM) qui r�ev�ele la pr�esence de fractures par insuffisance invisibles par radiographie, ainsi que sur l’incidence de profil lorsd’une radiographie du thorax qui r�ev�ele la pr�esence de fractures vert�ebrales asymptomatiques. Comme les fractures de fragilisations d�etect�eespar IRM ont parfois une pr�esentation non sp�ecifique, le radiologiste doit connaıtre leur emplacement et leurs r�esultats typiques afin de lesdiff�erencier des l�esions n�eoplastiques. Il importe de souligner que le radiologiste ne se limite pas au diagnostic des fractures li�ees �al’ost�eoporose. Il doit �egalement diagnostiquer les fractures qui d�ecoulent de complications li�ees �a la pharmacoth�erapie de l’ost�eoporose.Outre les techniques radiologiques normalis�ees, le radiologue a recours �a l’absorptiom�etrie bi�energ�etique �a rayons (DXA) et �a la tomo-densitom�etrie quantitative (QCT) pour �evaluer quantitativement l’ost�eodensitom�etrie aux fins de diagnostic de l’ost�eoporose ou del’ost�eop�enie ainsi que de suivi du traitement. La mesure par DXA du col du f�emur est �egalement utilis�ee pour calculer le risque de fractureost�eoporotique �a l’aide du syst�eme universel de cote FRAX. De nouvelles technologies, comme la tomodensitom�etrie quantitativep�eriph�erique haute r�esolution (HR-pQCT) et la spectroscopie par r�esonance magn�etique (SRM), permettent d’�evaluer l’architecture osseuseet la composition de la moelle osseuse afin de caract�eriser le risque de fracture. Enfin, le radiologiste participe �egalement au traitement desfractures ost�eoporotiques par vert�ebroplastie, spondyloplastie expansive et sacroplastie. Le pr�esent article de synth�ese porte sur les techniquesnormalis�ees et les nouvelles m�ethodes de diagnostic et de prise en charge de l’ost�eoporose.� 2016 Canadian Association of Radiologists. All rights reserved.

Key Words: Osteoporosis; Bone mineral density; Dual-energy x-ray absorptiometry; Insufficiency fractures; Vertebroplasty; Kyphoplasty; Sacroplasty

An important driver that motivates us to diagnose osteo-porosis at early stages and to evaluate the risk of fracture isthe availability of effective therapies that can prevent

* Address for correspondence: Thomas M. Link, MD, PhD, Department of

Radiology and Biomedical Imaging, University of California at San Fran-

cisco, 400 Parnassus Ave, A-367, San Francisco, California 94143, USA.

0846-5371/$ - see front matter � 2016 Canadian Association of Radiologists. A

http://dx.doi.org/10.1016/j.carj.2015.02.002

osteoporotic fractures. It is critical, however, that only thoseat risk or with prevalent osteoporotic fractures are treated astherapies are expensive and side effects have been associated

E-mail address: tmlink@radiology.ucsf.edu

ll rights reserved.

Figure 1. Lateral chest radiograph of a 71-year-old man with a grade 2

osteoporotic vertebral fracture at T11 with 35% height loss measured by

dividing the height of the posterior border of the vertebral body by the

anterior height (white lines). These fractures can be easily missed but are

clinically very significant as they may be an indication for medical treatment

of osteoporosis.

29Radiology of osteoporosis / Canadian Association of Radiologists Journal 67 (2016) 28e40

with these therapies, such as atypical subtrochantericfractures with bisphosphonates [1,2]. Patients who alreadyhave osteoporotic fractures are clearly candidates for therapybut not always are fractures symptomatic or correctly diag-nosed by the radiologist. Also, the referring physician maynot consider these incidentally noted fractures as an indica-tion for treatment. Radiologists therefore have an importantrole in guiding management, but not always are they awareof the significance of the findings and adequate training isessential [3].

Interpretation of standard imaging biomarkers such asdual energy x-ray absorptiometry (DXA) and quantitativecomputed tomography (QCT) is more straightforward buttraining is also critical to provide treatment recommenda-tions and interpret the impact of therapy. DXA measure-ments of the proximal femur should include Fracture RiskAssessment Tool (FRAX) fracture risk assessment toimprove identification of patients at risk for fracture withosteopenic bone mineral density (BMD) [4]. Limitations ofBMD measurements are well known and have driven thedevelopment of novel imaging biomarkers focusing on bonequality such as high-resolution peripheral QCT (HR-pQCT).

In addition to identifying and guiding management of pa-tients at risk for fractures as well as monitoring therapy radi-ologists are also directly involved in treatment by performingvertebroplasties, kyphoplasties, and sacroplasties. These are ateam approach and require concomitant treatment and radiol-ogists need to be an active part of the treatment team [5].

The scope of this article is: 1) to highlight the importanceof osteoporotic fractures and typical imaging findings using

different modalities; 2) to review standard and novel quan-titative imaging modalities to measure bone mineral densityand bone quality; and 3) to discuss therapeutic interventionsand their role in osteoporotic fractures.

Background and Epidemiology

The percentage of older patients is steadily increasing andthe yearly number of fragility fractures related to deficientbone mass and quality will increase substantially withcontinued ageing of the population [6]. Approximately 50%of women and 20% of men older than 50 years of age willhave a fragility fracture in their remaining lifetime inCaucasian populations [7] with potentially devastating re-sults. Of the individuals who suffer hip fractures 20% willdie within the next year and 20% will require permanentnursing home care [7].

Patients with vertebral fractures have less severe com-plications, but vertebral fractures are much more frequentand only 30% of the vertebral fractures come to clinicalattention [6]. Those that come to clinical attention areassociated with substantial disability from pain and increasedthoracic kyphosis. In addition the presence of 1 vertebralfracture leads to a 10-fold increase in risk of subsequentvertebral fractures [8]; diagnosis and treatment of vertebralfractures is therefore critical. While hip, vertebral, and wristfractures are the most frequent fractures associated withosteoporosis, the effect of osteoporosis on the skeleton issystemic and there is an increased risk of almost all types offractures in patients with deficient bone mass and quality.

Diagnosing Fragility Fractures

Radiologists need not only be familiar with correctlyinterpreting signs of fragility fractures but also using allavailable imaging modalities for this purpose. In 2000 astudy received major public attention that raised significantconcern about vertebral fractures being inadequately re-ported by radiologists [9]. In this study Gehlbach et al [9]reviewed the posterior-anterior and lateral chest radio-graphs of 934 women aged 60 years and older, who had beenadmitted to hospital. Radiology reports mentioned only 50%of 132 moderate and severe vertebral fractures found in thesewomen and only 17 patients had a discharge diagnosis ofvertebral fracture. All of these 132 patients were candidatesfor treatment but only a small percentage eventually receivedpharmacotherapy. Subsequently other studies showed similarfindings [10,11] and the Vertebral Fracture Initiative by theInternational Osteoporosis Foundation and the EuropeanSociety of Skeletal Radiology was launched to raise aware-ness and to train radiologists in diagnosing fractures.Figure 1 shows a typical osteoporotic fracture diagnosed on achest radiograph.

Similar studies have been performed using multidetectorCT (MD-CT) datasets that showed that without sagittal ref-ormations or dedicated evaluation of the scout radiographs a

Figure 2. Axial computed tomography of the sacrum obtained more superior (A) and more inferior (B) in a 68-year-old woman with low back pain. The left

sacral ala shows areas of increased density, which are consistent with remote insufficiency fractures (long arrows) while the right sacral ala shows fracture lines

anterior in the sacrum (short arrows) without significantly increased density superiorly (A) and mildly increased density inferiorly (B). Due to demineralization

fracture lines extending through the right sacral ala are not sufficiently visualized. Magnetic resonance imaging would be more sensitive to demonstrate the true

extent of the sacral fracture.

30 T. M. Link / Canadian Association of Radiologists Journal 67 (2016) 28e40

large number of osteoporotic vertebral fractures were missed[12,13]. Both studies strongly recommended sagittal refor-mations to improve the detection rate of osteoporotic frac-tures. In addition to chest radiographs and MD-CT vertebralfracture assessment of DXA studies has also been established[14] to diagnose osteoporotic vertebral fractures and is rec-ommended in postmenopausal women older than 70 years,

Figure 3. Coronal T1-weighted fast spin-echo (A) and short tau inversion

recovery (STIR) (B) sequences of the sacro-iliac joints in a 70-year-old

woman with bilateral chronic insufficiency fractures of the sacrum. T1-

weighted sequences show the fracture lines along with diffusely low

signal along the sacro-iliac joints (arrows). STIR sequences show a mix of

bright signal (bone marrow oedema pattern, small arrows) and low signal

(sclerotic bone, long arrows).

men older than 80 years of age and patients with height lossand diseases associated with increased risk of vertebralfractures [15].

It is critical that using all these different modalitiesosteoporotic vertebral fractures are classified in a standard-ized way and a semiquantitative grading system developedby Genant et al [16] in 1993 is recommended by mostsocieties such as the International Society of ClinicalDensitometry (ISCD), the International Osteoporosis Foun-dation and the European Society for Skeletal Radiology.According to this grading system a vertebral deformity ofT4-L4 with more than 20% height loss and a 10%-20% areaof height reduction is defined as a fracture. Four grades aredifferentiated: grade 0 ¼ no fracture, grade 1 ¼ mild fracture(reduction in vertebral height 20%-25%, compared to adja-cent normal vertebrae), grade 2 ¼ moderate fracture(reduction in height 25%-40%), and grade 3 ¼ severe frac-ture (reduction in height more than 40%).

In addition to vertebral fractures there are a number ofother fragility fractures, which are encountered not infre-quently but may be incorrectly diagnosed potentially leadingto unnecessary and potentially dangerous procedures forpatients. Among those pelvic fractures have a particularlyimportant role. Fragility fractures of the sacrum have beenmisinterpreted as neoplastic lesions and several previousstudies [17,18] focused on the importance of correctlydiagnosing sacral fractures. Radiographs are usually quitechallenging in diagnosing these fractures and only a smallpercentage of fractures (20%-38%) are identified [19]. CT isreadily available in an emergency setting and shows fracturelines and increased density, eventually also fracture callus isdemonstrated (Figure 2). It should be noted, however, thatCT is not as sensitive as bone scintigraphy or magneticresonance imaging (MRI) and sensitivities of only 60% and75% have been reported [17,20]. This is due to the fact thatthe substantial amount of bone loss in these patients makes itchallenging to demonstrate fracture lines. CT, however, mayhave an important role as a problem solving tool by

Figure 4. Sequential radiographs (A, C) and magnetic resonance imaging (MRI) of the pelvis (B) in a 75-year-old woman with a right hip hemiarthroplasty and

a left pubic symphysis insufficiency fracture. Initial radiograph (A) was obtained after low energy fall from less than standing height and persistent pain.

Suspicion for fracture led to the MRI, which demonstrated a mildly displaced and impacted superior pubic ramus fracture (B). Radiograph obtained 3 months

after the fall shows healing pubic symphysis fracture with callus formation.

31Radiology of osteoporosis / Canadian Association of Radiologists Journal 67 (2016) 28e40

identifying cortical and trabecular destruction, which areseen with neoplastic lesions such as bone metastases [21].While MRI and nuclear medicine techniques are very sen-sitive in diagnosing fragility fractures both technologies arenot very specific and differentiating fragility fractures fromneoplastic lesions can be difficult. The typical MRI findingsare bone marrow oedema pattern best seen on fluid sensitivefat saturated sequences such as short tau inversion recoverysequences and fracture lines, which tend to be better seen on

Figure 5. Anteroposterior, weight-bearing radiograph (A) and coronal fat-saturate

man with increasing medial-sided knee pain since 3 months. The radiograph doe

consistent with moderate osteoarthritis. The magnetic resonance imaging shows

(arrows) and adjacent, extensive bone marrow oedema pattern. Findings are con

loading related to medial meniscal abnormality (medial meniscus body is dimin

T1-weighted spin-echo sequences (Figure 3). In morechronic stages there may be more sclerosis, which is low inT1-weighted and short tau inversion recovery sequences. Iffracture lines are not seen MR findings may be misleadingand not infrequently result in bone biopsies or moreadvanced imaging such as positron emission tomography-CT. In addition to the sacrum insufficiency fractures arealso found in other regions of the pelvis such as the pubicbones and the supra-acetabular region; not infrequently they

d intermediated fast spin-echo sequence (B) of the left knee in a 76-year-old

s not show any deformity but medial joint space narrowing and osteophytes,

a subchondral, low intensity line consistent with an insufficiency fracture

sistent with increased bone fragility associated with altered biomechanical

utive and torn).

Figure 6. Anteroposterior left proximal femur radiographs in 72-year-old woman with 8 years of bisphosphonate therapy. Baseline radiograph (A) shows focal

cortical prominence consistent with developing, atypical subtrochanteric stress fracture. One month later the subtle cortical thickening has progressed to a

complete fracture with the typical medial spike (arrow in B). The atypical subtrochanteric fracture was treated with a long gamma nail with interlocking screw (C).

32 T. M. Link / Canadian Association of Radiologists Journal 67 (2016) 28e40

are found in patients with total joint replacements, which isrelated to altered biomechanical loading of the pelvic bones(Figure 4).

In addition to the pelvis and spine fragility fractures arealso found at other sites such as the femoral condyles and thefemoral head and may be misinterpreted as osteonecrosis. Anumber of previous studies [22e24] have documented thetypical MR and histological findings. These fractures arerelated to increased bone fragility associated with alteredbiomechanical loading. On MRI the typical findings are afracture line following the joint surface and a substantialamount of bone marrow oedema pattern (Figure 5). Typicallythese fractures are associated with accelerated osteoarthritisand not infrequently result in total joint replacement.

Complications of Osteoporosis-RelatedPharmacotherapy

Atypical subtrochanteric and femoral shaft fractures arean infrequent yet significant complication of long-termbisphophonate therapy in older individuals [1,25]. Thetypical radiologic features of these fractures are a location inthe subtrochanteric region and femoral shaft, transverse orshort oblique orientation, minimal or no associated trauma, a

medial spike when the fracture is complete, absence ofcomminution, cortical thickening, and a periosteal reactionof the lateral cortex (Figure 6) [25]. In the early stages lateralcortical thickening of the cortex is typically found whichmay progress to a complete fracture and is therefore a criticalfinding, which needs to be communicated to the clinician.

According to the American Society of Bone and MineralResearch task force in 28% of patients bilateral fractures werefound with bilateral radiographic abnormalities [26]. It istherefore imperative to always thoroughly investigate bothfemora. Fractures may be complete when they extend throughboth cortices and may be associated with a medial spike;incomplete fractures involve only the lateral cortex. Interest-ingly a number of patients have prodromal symptoms such asdull or aching pain in the groin or thigh. Atypical fractures arealso characterized by delayed healing and an increased rate ofintraoperative and postoperative complications related toaltered bone quality [27].

While complete fractures are managed surgically, typi-cally with intramedullary nailing, there is no definite proto-col as to whether incomplete atypical fractures should bemanaged with surgery or conservatively [27]. Managementof these fractures depends on the clinical findings andradiologic evidence from radiographs and MRI. Femur

Figure 7. Dual-energy x-ray absorptiometry study of the lumbar spine (A), the proximal femur (B) and the distal radius (C) obtained in a 74-year-old woman

with osteoporotic bone mineral density (BMD). The diagnosis is made using the lowest t score from L1-4, femoral neck, total femur (consists of femoral neck,

trochanteric, and intertrochanteric region, shown in blue), and one-third distal radius regions (shown in blue). In this patient the t score of the lumbar spine was

e2.7, of the neck e2.7, of the total femur e2.4, and e2.6 of the one-third distal radius region. Image A also shows previous BMD measurements obtained at

age 71 and 73 years; BMD is stable without significant change. This figure is available in colour online at http://carjonline.org/.

33Radiology of osteoporosis / Canadian Association of Radiologists Journal 67 (2016) 28e40

radiographs should be examined for cortical reaction and aradiolucent fracture line across the lateral cortex. The pres-ence of a radiolucent line on plain radiograph indicates apoor prognosis, and prophylactic fixation is recommended toprevent progression to complete fracture [28]. In the absenceof a fracture line on plain radiograph patients may bemanaged nonoperatively with no weight bearing or limitedweight bearing with a crutch, cane, or walker, and the use ofteriparatide as well as other pharmacologic modalities.However, the failure rate for conservative treatment is highand close monitoring with plain radiographs and MRI isrecommended [29].

Quantitative Measurement of Bone Density andStructure

Bone Densitometry

The standard technique to measure BMD is DXA andbased on this quantitative measurement the WHO definedosteoporosis and osteopenia in 1994 [30]. T-scores are usedto define osteoporosis, osteopenia, and normal BMD. TheT-score is the standard deviation compared to a youngnormal reference population, a T-score of �e1 is consideredas normal BMD while a T-score of <1 and >2.5 is defined as

Figure 8. Quantitative computed tomography obtained in a 73-year-old woman with osteopenic bone mineral density (BMD). Image (A) shows the axial CT

image with the calibration phantom (arrow) at the level of L1. (B) The oval region of interest (arrow) in the axial image, and (C) the analysed volume in the

sagittal plane and (D) in the coronal plane. BMD was calculated as 101.6 mg/mL, consistent with osteopenic BMD.

34 T. M. Link / Canadian Association of Radiologists Journal 67 (2016) 28e40

osteopenic and of �2.5 as osteoporotic. This definition isused for BMD of the proximal femur (neck and total femurregions of interest) (Figure 7B) and of the lumbar spine(anteroposterior projection) (Figure 7A). If these measure-ments are not available because of severe degenerativechanges of the lumbar spine or bilateral total hip re-placements the distal radius BMD (one-third radius region ofinterest) may be used (Figure 7C). The World Health Orga-nization (WHO) definition was originally only used inpostmenopausal women but can according to ISCD guide-lines also be used for men older than 50 years of age[15,31,32]. The ISCD has also published guidelines for DXAof premenopausal women, men younger than 50 years of age,and children [15,31,32]. In these populations Z scores areused comparing individual BMD measurements toage-matched reference populations; a Z score �e2 is definedas ‘‘BMD below the expected range for age.’’ It should benoted that in these populations a diagnosis of osteoporosiscannot be based on DXA alone.

DXA is a well-standardized technique with a high preci-sion (precision error 2%-2.5%) and low radiation dose (1-50microSv) [33]. DXA is indicated in women aged 65 andolder as well as younger and perimenopausal women withrisk factors for fragility fractures. In addition men 70 years ofage and older and younger men with risk factors for fractureshould undergo DXA. Patients who are considered forpharmacotherapy and those currently treated with pharma-cotherapy should also be examined with DXA [31].Follow-up DXA scans are typically performed every 1-2years to monitor treatment response [34]. Recommendedtime intervals are based on the least significant change,which is calculated using the precision error of the mea-surement multiplied by 2.77 [35]. The spine measurementhas normally the lowest precision error, but a BMD changeof approximately 5% is needed to demonstrate a significantimpact of therapy [36].

Though it is the standard measurement DXA has anumber of limitations:

Figure 9. High-resolution peripheral quantitative computed tomography

image of the distal tibia in a 58-year-old woman with type 2 diabetes and

fragility fracture. Note high detail of trabecular bone architecture visuali-

zation and increased cortical porosity (arrows), which is a typical finding

associated with diabetic fragility fractures.

35Radiology of osteoporosis / Canadian Association of Radiologists Journal 67 (2016) 28e40

1. Spine DXA is sensitive to degenerative changes andindividuals with significant degenerative disease willhave increased BMD, but this may not correlate with thetrue fracture risk.

2. DXA is an areal measurement, which is susceptible tobone size and may therefore over-estimate the fracturerisk in individuals with small body frame.

3. Structures overlying the spine and proximal femur, suchas aortic or other vascular calcifications, bowel contrast,and pancreatic calcifications may increase the BMD. Onthe other hand status postlaminectomy at the spine maydecrease BMD.

To better characterize fracture risk in osteopenic in-dividuals the WHO introduced the FRAX fracture riskassessment tool (http://www.sheffield.ac.uk/FRAX/) [37e39].It includes DXA based BMD of the femoral neck and clinicalrisk factors (previous fracture, parent fractured hip, currentsmoking, glucocorticoids, rheumatoid arthritis, alcohol, andsecondary osteoporosis) in addition to age, gender, weight,and height. From these data a 10-year probability of a hipfracture or major osteoporosis related fracture are calculated.Based on theUS-adaptedWHOalgorithmmedical therapies arerecommended if the patient is osteopenic (T-score between e1.0 and e2.5) and the 10-year probability of a hip fracture is�3% or the 10-year probability of a major fracture is �20%.

Alternatively to DXA QCT may be used to measure BMD[40]. While the WHO definition does not apply to QCT andT-scores should not be used for QCT, the American College

of Radiology introduced guidelines for evaluating QCTstudies, which are based on absolute BMD measurements.BMD values above 120 mg hydroxyapatite/mL are consid-ered as normal, from 120-80 mg/mL are defined as osteo-penic and BMD values below 80 mg/mL as osteoporotic[41]. T-scores should not be used for QCT because theywould identify a significantly larger patient population withosteoporosis than would DXA, which is explained by a fasterdecrease of QCT BMD with age than DXA BMD. Bothvolumetric and single-slice QCT techniques are used, butwhile volumetric techniques have better precision thansingle-slice techniques, they also have a substantially higherradiation dose [40]. Radiation exposure doses as low as50-60 microSv have been described for single-slice QCTusing low-dose techniques, while for volumetric QCT dosesare in the order of 1500 microSv for the spine and 2500-3000microSv for the hip [42,43]. Figure 8 shows image datasetsobtained for a volumetric scan of the lumbar spine, includingthe volumes of interest.

Compared to DXA QCT provides trabecular bone mea-surements which are more sensitive to therapy [44]. It alsoallows volumetric BMD measurements of the lumbar spineand proximal femur, which are independent of the body sizeand cross-sectional studies have shown that QCT BMD ofthe spine allows better discrimination of individuals with andwithout fragility fractures [45,46]. However, the disadvan-tages are the higher radiation dose and a limited number oflongitudinal scientific studies that have shown how QCTpredicts fragility fractures.

Recommendations for the use of QCT instead of DXAare: 1) very small or large individuals; 2) older individualswith expected advanced degenerative disease of the lumbarspine or morphological abnormalities; and 3) if high sensi-tivity to monitor metabolic bone change is required such asin patients treated with parathyroid hormone or corticoste-roids [21]. A recent study comparing DXA and QCT in oldermen with diffuse idiopathic skeletal hyperostosis demon-strated that QCT was better suited to differentiate men withand without vertebral fractures [47].

Densitometric techniques of the peripheral skeletoninclude peripheral DXA [48], pQCT [49] and digital x-rayradiogrammetry (DXR) [50], but they have limited signifi-cance clinically. They are inexpensive and easy to perform,but the different types of measurement often correlate poorlymaking it difficult to find a consensus on the best use ofperipheral measurements [36].

Diagnostic Techniques to Measure Bone Quality

Bone quality measurements are less well standardized andhave a more limited clinical application compared to BMDmeasurements. The most widely distributed measurements ofbone quality are HR-pQCT and quantitative ultrasound(QUS). Interesting newer measurements are MR spectros-copy of bone marrow and texture analysis of DXA images.

HR-pQCT was developed for imaging of trabecular andcortical bone architecture of the distal radius and tibia

Figure 10. Sagittal short tau inversion recovery sequences of the lumbar spine in a 77-year-old man with osteoporotic vertebral fractures and kyphoplasties.

Initially (A) the patient had a L3 osteoporotic fracture (arrow) which was treated with kyphoplasty (asterisk in B). (B) also shows 2 subsequent, new vertebral

fractures of L4 and L5 that developed 7 weeks after the initial kyphoplasty. Image C was obtained 5 weeks after the second kyphoplasty (L4 and L5) (asterisks)

and demonstrates 2 new fractures at T12 and L1 (arrows). Image D was performed 3 weeks after subsequent T12 and L1 kyphoplasty (asterisks) and shows also

mild new T11 fracture with bone marrow oedema pattern along the endplate (arrow).

36 T. M. Link / Canadian Association of Radiologists Journal 67 (2016) 28e40

[51e53] (Figure 9). The HR-pQCT system is produced by asingle manufacturer (XtremeCT; Scanco Medical AG,Br€uttisellen, Switzerland) and has higher spatial resolutioncompared to standard MD-CT and MRI [54]. While thereconstructed voxel size is 82 mm for the standard patientHR-pQCT protocol, the actual spatial resolution of the imageis approximately 130 mm near the center of the field of view,and somewhat less off-center (140-160 mm) [55]. Newergeneration HR-pQCT systems have a voxel size down to41 mm. The effective radiation dose is low with <3 microSv.The system allows acquisition of BMD, trabecular, andcortical bone architecture at the same time. Based on asemiautomated contouring and segmentation process, thetrabecular and cortical compartments are segmented auto-matically for subsequent densitometric, morphometric, andbiomechanical analyses. Morphometric indices analogous toclassical histomorphometry as well as connectivity, structuremodel index (a measure of the rod or plate-like appearanceof the structure), and anisotropy can be calculated from thebinary images of the trabecular bone. In addition finiteelement analysis can be applied to these datasets andapparent biomechanical properties (eg, stiffness, elasticmodulus) can be computed by decomposing the trabecularbone structure into small cubic elements (ie, the voxels) withassumed mechanical properties [56,57]. Previous clinicalstudies have shown promising results in differentiatingpostmenopausal females and older men with and withoutfragility fractures [51,58] and in monitoring therapeutic

interventions [59]. Recently structural analysis of corticalbone has been introduced to the study of HR-pQCT datasetsand cortical porosity measurements have been developed[56]. This parameter has been shown to be useful inidentifying increased fracture risk in patients with type 2diabetes [60].

It has been shown that bone marrow fat is increased inosteoporosis and that other conditions with increased fracturerisk such as diabetes mellitus, immobility and glucorticoidtherapy are also characterized by increased bone marrow fat[61]. Proton magnetic resonance spectroscopy allows tomeasure bone marrow fat noninvasively and previous studieshave shown that bone marrow fat increases with decreasingBMD and is significantly elevated in postmenopausal fe-males and older men [62e64].

QUS is a low-cost technique, which has been used for anumber of years and has been performed at a number ofdifferent anatomical sites (calcaneus, phalanges of the hand,tibia), but according to the ISCD official positions (http://www.iscd.org/official-positions/official-positions/) the onlyvalidated skeletal site is the calcaneus/heel. QUS allows tomeasure the transmission of ultrasound waves through bone,which is characterized by the velocity of transmission andthe amplitude of the ultrasound signal. Velocity is measuredas metre/second and defined as speed of sound, whichdecreases in osteoporotic bone. Broadband ultrasoundattenuation is calculated in decibel/megahertz and increasesin osteoporotic bone. A previous meta-analysis found that

Figure 11. Sacroplasty performed with fluoroscopy guidance, bone cement is located in the left sacrum (arrows in A and B). Computed tomography obtained in

a prone position demonstrates bone cement in close proximity to the sacro-iliac joint (arrow in C), where insufficiency fractures are typically located. Images

courtesy of Dr Peter Munk, Department of Radiology, Vancouver General Hospital, University of British Columbia.

37Radiology of osteoporosis / Canadian Association of Radiologists Journal 67 (2016) 28e40

both DXA and calcaneal QUS predicted fractures butinterestingly that the correlation between the 2 techniqueswas low [65]. Thus it has been suggested that the techniquemay be well suited to assess bone quality [66]. However, theproliferation of QUS devices that are technologicallydiverse, measuring and reporting variable bone parametersin different ways, examining different skeletal sites, andhaving differing levels of validating data for associationwith DXA-measured bone density and fracture risk, hascreated many challenges in applying QUS for use in clinicalpractice [67].

While QUS has been shown to differentiate individualswith and without fragility fractures [68,69] and to predictfracture risk [70], it has not been established to diagnoseosteoporosis such as DXA has and it is currently not rec-ommended to monitor treatment response according to theISCD official positions [67], as the number of large-scalestudies describing the efficacy of QUS in monitoring theeffects of treatments is limited.

Management of Fragility Fractures

A recent retrospective analysis of a nationwide inpatientsample from 2005-2011demonstrated that the absolute rateof inpatient vertebroplasty and kyphoplasty procedures forvertebral fragility fractures decreased overall, but also thatpatients with greater disease severity were treated [71]. Thedecreased inpatient volume and procedural rates wereattributed to a number of randomized clinical trials, which

showed conflicting outcomes regarding pain and quality oflife compared to nonsurgical management and sham pro-cedures [72e74].

Vertebroplasty involves a percutaneous injection of bonecement/polymethylmethacrylate into a fractured vertebralbody, generally through a unilateral or bilateral trans-pedicular route. In balloon kyphoplasty, a mostly bilateraltranspedicular or extrapedicular route is used to access thevertebral body and a balloon is introduced expanding thebone and creating a cavity with the goal to realign the end-plate of the vertebral body. After removal of the balloon bonecement is injected which fixes and stabilizes the fracture. Aprevious study showed that the level of cement leakage andnumber of reported adverse events (pulmonary emboli andneurologic injury) in balloon kyphoplasty was significantlylower than for vertebroplasty [75]. Also kyphoplasty mayrestore height and reverse wedge deformity, which is usuallynot seen with vetebroplasty. However, both techniques areconsidered to be safe and effective in reducing pain [75e77].

There is some conflicting evidence concerning new frac-tures in adjacent levels after vertebral fractures treated withkyphoplasty and vertebroplasty (Figure 10). This is based onbiomechanical studies, that have shown that the acute changein stiffness may provoke fractures in adjacent levels [78,79].Three-dimensional computer models of L2 and L3 weredeveloped, adapting material properties to simulate osteo-porosis and cement augmentation was found to restorestrength of the treated vertebra but clearly altered the loadtransfer in the adjacent vertebra [79]. Fribourg et al [80]

38 T. M. Link / Canadian Association of Radiologists Journal 67 (2016) 28e40

demonstrated a higher rate of subsequent fracture afterkyphoplasty compared with natural history data for untreatedfractures. Most of these occurred at an adjacent level within2 months of the index procedure. After this 2-month period,there were only occasional subsequent fractures, whichoccurred at remote levels. The authors therefore recom-mended that patients with an increase in back pain afterkyphoplasty should be evaluated carefully for subsequentadjacent fractures, especially during the first 2 months afterthe index procedure [80].

The first studies on the treatment of sacral insufficiencyfractures with sacroplasty were published between 2002-2005 [81e84]. Sacroplasty is similar to vertebroplasty and isusually performed under CT guidance as it provides moreaccurate needle placement, but ideally with fluoroscopymonitoring to assess leakage of bone cement or vascularembolization (Figure 11). Bone cement is injected into thefracture area and usually provides pain relief within 24hours. Sacroplasty is considered safe and practical, andprovides effective pain relief. In a recent, single-center studyincluding 53 patients no major complication or procedure-related morbidity occurred [85]. In addition significantshort-term gains in pain relief, increased mobility, anddecreased dependence on pain medication were observed.

Summary and Conclusion

This review article aims to cover the entire spectrum ofosteoporosis imaging relevant for the radiologist. Osteopo-rosis is a severely debilitating disease, which will in thefuture gain increasing importance as our population ages. Asradiologists we have a critical role in diagnosing and man-aging patients with increased risk for fragility fractures [3].First, we need to identify patients with prevalent fragilityfractures, as they are at high risk for future severe fractures,specifically we need to alert our clinicians concerning theseissues and not misinterpret these findings as malignant dis-ease prompting costly and unsafe interventions. In additionwe need to diagnose and monitor osteoporosis using quan-titative techniques such as DXA and be familiar with com-plications of medical treatments. We need to be at theforefront in developing new tools to better assess bonequality and fracture risk. Finally, we need to be part of thetreatment team performing interventional procedures to treatvertebral and sacral insufficiency fractures in concert withother clinicians adding supportive pharmacotherapies.

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