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Review Article *Corresponding author Catherine L McCarthy, Department of Radiology Nuffield Orthopaedic Centre, Oxford University Hospitals, Windmill Road, OxfordOX3 7LD, United Kingdom, Tel: Radiological Review of Unusual +441865738196, Email: catherinemccarthy@doctors. org.uk Submitted: 26 October 2020 Femoral Fractures Accepted: 06 November 2020 Snehansh R Chaudhary, Nathan Edwards and Catherine L Published: 09 November 2020 Copyright McCarthy* © 2020 Chaudhary SR, et al. Department of Radiology, Nuffield Orthopaedic Centre, Oxford University Hospitals, OPEN ACCESS United Kingdom Keywords Abstract • Unusual femoral fractures • Atypical femoral fracture (AFF) Femoral fractures may be caused by direct acute trauma or other causes which are • Stress fracture broadly classified into stress fracture, insufficiency fracture, atypical femoral fracture • Insufficiency fracture or pathologic fracture and may be grouped together as unusual femoral fractures. • Pathologic femoral fracture Familiarity and recognition of the specific imaging features of unusual femoral fractures is important to ensure early identification, characterisation and appropriate management of these fractures. The aim of this review to is to illustrate the characteristic imaging features of unusual femoral fractures and the role of different radiological modalities including plain radiographs, Computed Tomography (CT), Magnetic Resonance Imaging (MRI), technitium-99m bone scintigraphy and single-photon emission computed tomography (SPECT).

ABBREVIATIONS area of underlying bone pathology. This may be either due to an AFF: Atypical Femoral Fracture; CT: Computed Tomography; underlyingA pathologic bone fracture,tumour (benign by definition, or malignant) is any fracture or non-neoplastic through an MRI: Magnetic Resonance Imaging; SPECT: Single-Photon Emission Computed Tomography; PET: Positron Emission Tomography; STIR: Short T1 Inversion Recovery; ASBMR: The skeletal or metabolic abnormality although a fracture as a result] and American Society for Bone and Mineral Research weof the have latter presented group itof as disease such in processes this paper. is commonly classified INTRODUCTION under insufficiency fracture due to secondary causes [1,7,8 Femoral fractures may be caused by direct acute trauma or form a spectrum of fractures of the femur which are not directly causedStress, by insufficiency, straight forward atypical acute and trauma pathologic and femoral maybe fractures grouped together as unusual femoral fractures (Table 1). These fractures other causes which are broadly classified into stress fracture, fracture. have unique imaging features and recognising them is important insufficiency fracture, atypical femoral fracture or pathologic for appropriate and timely treatment of patients. The aim of this by overuse from chronic repetitive stress on normal bone and is usuallyA stress seen fracture, in weight-bearing also referred bones to as of fatigue athletes. fracture, is caused femoral fractures on different radiological modalities including review to is to illustrate the key imaging features of unusual

plain radiographs, Computed Tomography (CT), Magnetic An insufficiency fracture, also known as fragility fracture, and single-photon emission computed tomography (SPECT). Resonance Imaging (MRI), technitium-99m bone scintigraphy asresults well from as secondary normal stresses causes through such as bones renal osteodystrophyof reduced strength, and STRESS FRACTURES hyperparathyroidismwhich is primarily due amongst to senile many or postmenopausal others [1]. osteoporosis, Stress fractures are typically caused by chronic repetitive Bisphosphonates have been in wide use to prevent fragility injury on weight-bearing bones in athletes. Stress fractures in the 2] after multiple clinical trials [ ] established region [ ] and more commonly on the medial aspect [ ]. fractures, [ 3,4 ] Femoralfemur usually stress occurfractures in thehave femoral a higher neck chance and of intertrochanteric healing because their long-term efficacy. In 2005, suppressed bone turnover the compressive9 load passes through the medial side of 10 the was first suggested as a complication of bisphosphonates [5 characteristic and distinct patterns of femoral fractures caused femur [11 byand bisphosphonate in 2008,the term therapy ‘atypical [6]. fracture’ was coined based on ]. However, proximal femoral fractures, fractures with a fracture line greater than 50% of the femoral neck width and Cite this article: Chaudhary SR, Edwards N, McCarthy CL (2020) Radiological Review of Unusual Femoral Fractures. Ann Orthop Rheumatol 7(1): 1092. Chaudhary SR, et al. (2020)

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Table 1: Fractures due to direct acute trauma Classification of femoral fractures. Unusual femoral fractures • o Stress fracture (overuse due to chronic repetitive stress) • o . Primary – senile or postmenopausal osteoporosis Insufficiency fracture . Secondary

• Osteogenesis imperfect a, osteopetrosis, polyostotic fibrous dysplasia, Paget’s disease • Exogenous corticosteroids, oestrogen/testosterone deficiency, hyperparathyroidism, osteomalacia, endocrine/nutritional/haematological/hereditary disorders renal osteodystrophy, scurvy (Vit C deficiency), rheumatoid arthritis, gout, Wilson’s disease, other Previous irradiation, stress shielding from total hip replacement, organ transplantation, tabes

• o Atypical femoral fracture (bisphosphonate related) dorsalis, high-dose fluoride therapy o Pathologic fracture (fracture through underlying pathology) . . Malignant Benign – unicameral bone cyst, aneurysmal bone cyst, fibrous dysplasia, enchondroma, giant cell tumour Secondary metastasis – breast, lung etc. • Primary bone sarcoma – osteosarcoma, Paget’s sarcoma, myeloma, lymphoma, chondrosarcoma • fractures with the slightest displacement are still considered to be high-risk for developing into complete fractures [12]. fractures. On plain radiographs, one of the earliest signs of stress Radiographs are considered to be first line imaging for stress lucency of the cortex (Figure 1) and histologically corresponds toresponse microcrack is the formation“grey cortex [13,14 sign”]. which As injury refers persists to subtle and ill-defined healing begins, periosteal reaction, endosteal callus and focal cortical thickening may be seen. In later stages of higher grade injuries, a transverse lucent fracture line indicative of a cortical break may become apparent [15]. In areas with a greater proportion of trabeculae such as the femoral metaphysis, there may be A) B) indistinct intramedullary blurring and sclerosis as the earliest signs on x-ray [16], which progresses to an intramedullary Figure 2 Plain radiograph and 2b Coronal CT image of a chronic stress sclerotic line (Figure 2) due to microcallus formation along fracture along the medial femoral neck demonstrating intramedullary remodelled trabeculae [16,17]. Displacement and comminution linear sclerosis (arrows) due to microcallus formation along the are not characteristic features of stress fractures. Despite these fracture.. radiographic signs, the sensitivity of radiographs are reported to be approximately in the range of 25% for early stage injury and 50% for late stage injury [18]. If radiographs are negative, then MRI should be the next approaching 100% [19]. On MRI, a low signal fracture line with investigation to consider, reporting a specificity and sensitivity

A) B)

Figure 3 Coronal STIR and 3b Coronal T1 MR images of an acute medial femoral stress fracture demonstrating a low signal fracture line (arrow) with surrounding high STIR and low T1 marrow and Figure 1 Plain radiograph of a stress fracture along the medial femoral periosteal oedema (Fredericson Grade 4). The low T1 signal intensity has a heterogeneous appearance with foci of intervening preserved (arrow) of the medial femoral cortex. high T1 fatty marrow signal. neck with subtle ill-defined lucency (grey cortex sign) and irregularity

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Central surrounding osseous or soft tissue oedema may be seen (Figure sciences, what is deemed correctable or uncorrectable may not 3) [20]. MRI features of stress fractures can be graded (Table only be debatable but can also change over time. 2) according to Fredericson et al [21 It is reasonable to think of the imaging features of 22], by using fat ] classification system or their slightly modified version by Kijowski et al [ although their aetiology and epidemiology are vastly different. T1-weighted sequences. insufficiency fractures as largely similar to stress fractures, saturated T2-weighted (fluid-sensitive) and non-fat saturated CT may have a role in demonstrating a fracture line with requires the radiologist to have a broad knowledge of the adjacent sclerosis and reaction depending on the age of the skeletalIdentifying manifestations subtle insufficiency of a wide range fractures of metabolic in these and conditions systemic for stress fractures approaching nearly 100% [19]. secondly apply the principles of fracture detection on different fracture (Figure 2b). CT is also reported to have high specificity imagingdisorders modalities to firstly (Figures recognise 4 and the 5). underlying pathology, and On Technitium-99m bone scintigraphy (planar bone scan), stress fractures are seen as a focal area of increased uptake. ATYPICAL FEMORAL FRACTURES Although planar bone scan is considered to be a sensitive Atypical femoral fractures (AFFs) are a relatively uncommon 19]. A comparative study reported a much lower sensitivity of planar use of medications that suppress osteoclastic-mediated bone boneinvestigation scan at around for stress 50% fractures, when performed it is less specificalone but than approaching MRI [ turnover,type of femoral including insufficiency bisphosphonates fracture and linked denosumab to the long-term[8,29,30]. 92% when performed with SPECT [23]. Biopsy of stress fractures The pathogenesis has been attributed to the suppression of bone should always be avoided as histologically it may be confused marrow turnover and remodelling at the site of repetitive tensile with aggressive bone turnover [8]. stress along lateral cortex of the subtrochanteric and proximal diaphysis of the femur [29,30]. Biomechanical factors that INSUFFICIENCY FRACTURES accentuate this tensile stress, including an increased standing femorotibial angle and femoral bone curvature, are associated postmenopausal osteoporosis. with an increased risk of AFFs [31]. Insufficiency fractures primarily result from senile or There are many secondary causes [1,7 AFFs result from minimal or no trauma [32]. Patients usually fractures (Table 1) with some recent case reports demonstrating present with prodromal symptoms, typically dull or aching femoral fractures due to gout [24 ] of insufficiency25], pain in the groin or thigh [30] 26 27]. Secondary AFFs may be subtle and consequently missed, with potential for ], Wilson Disease [ progression to a complete fracture. The [early9]. The radiological American Societyfindings for of orvitamin uncorrectable D deficiency causes [ ] and [28 ]. Paget’s Correctable disease [ causes include conditionsinsufficiency such fractures as renal may be osteodystrophy, thought of in terms osteomalacia of correctable and diagnosisBone and of Mineral this entity Research and differentiate (ASBMR) have it from developed other femoral specific hyperparathyroidism while uncorrectable causes include disease fractures,clinical and including imaging criteria exercised-induced to precisely stressdefine AFFs fractures, to aid low- the energy osteoporosis-related fractures, pathologic fractures and high-energy fractures (Table 3) [30,33,34]. consideringprocesses such that as with osteogenesis continuous imperfecta, advancements polyostotic in medical fibrous dysplasia and Paget’s disease amongst many others. It is worth

Table 2: Grading of MRI features of stress fracture using Fredericson21 22 Grade 1 – periosteal oedema and Kijowski classifications. Grade 2 – periosteal and mild marrow oedema seen on T2w images only Grade 3 – periosteal and marrow oedema seen on both T1w and T2w images. Grade 4a – intracortical signal change without a linear shape with periosteal and marrow oedema Grade 4b – linear intracortical fracture line with periosteal and marrow oedema

Figure 4 Plain pelvic radiograph demonstrating slender bowed osteopaenic femora with marked cortical thinning consistent with osteogenesis

imperfecta. There are multiple insufficiency fractures with pseudoarthroses (arrows) and modelling deformity (arrowheads). Ann Orthop Rheumatol 7(1): 1092 (2020) 3/8 Chaudhary SR, et al. (2020)

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A) B)

Figure 5

symmetrical, Plain orientated radiograph perpendicular and 5b Coronal to theCT imagecortex of with a patient adjacent with sclerosis. osteomalacia demonstrating femoral head flattening, shortened femoral necks and femoral bowing. There are insufficiency fractures or looser zones (arrows) of the medial proximal femora which are typically bilateral and

Table 3: Atypical femoral fracture: Major and minor features [30]. Major features

Associated with no or minimal trauma, as in a fall from standing height or less • Location anywhere along the femoral diaphysis, from just distal to the lesser trochanter to just proximal to the supracondylar flare • Non-comminuted • IncompleteTransverse orfractures short oblique involve configuration only the lateral cortex; Complete fractures extend through both cortices and may demonstrate a medial spike • Minor• features Localised periosteal reaction of the lateral cortex Generalised increase in cortical thickness of the femoral diaphysis • Prodromal symptoms such as dull or aching pain in the groin or thigh • Bilateral fractures and symptoms • Delayed healing • • Use of pharmaceutical agents • Comorbid conditions (such as vitamin D deficiency, rheumatoid arthritis, hypophosphatasia) • An early plain radiographic feature of AFFs issubtle focal Other imaging modalities should be considered for patients periosteal or endosteal thickening of the lateral cortex of the on long term antiresorptive therapy with classical prodromal subtrochanteric or proximal femoral diaphysis, referred to as 9]. 9,11]. More generalised MRI, CT and bone scintigraphy have a higher sensitivity and diffuse lateral femoral cortical thickening may also occur (Figure symptoms and equivocal or negative radiographic findings [ 7).cortical An incomplete‘beaking’ or transverse‘flaring’ (Figure radiolucent 6) [ line known as the [9,35]. MRI is the preferred imaging modality, enabling detection ofspecificity periosteal for and detecting endosteal early oedema AFFs compared (high T2 and to plain STIR radiographs signal), and cortical thickening (Figure 8). Subsequent progression to the low signal cortical fracture lines (Figure 10b and 10c) [9,29,36]. medial‘dreaded femoral black line’ cortex can results sometimes in a complete be noted fracture in the region which of is CT can detect focal intracortical bone resorption, subtle cortical typically transversely orientated and non-comminuted. The thickening and periosteal reaction not evident on radiographs fracture may have a short oblique orientation medially leading to (Figure 7b and 7c) [9]. Technitium-99m bone scintigraphy a characteristic medial cortical spike (Figure 9) [9,11]. Additional demonstrates focal avid radiotracer uptake at the fracture site centred on the lateral femoral cortex (Figure 10d). It is important healing [9]. Initial involvement of the lateral femoral cortex to assess for cortical involvement to help differentiate AFFs from differentiatesfindings include AFFs periosteal from the stress classical reaction exercised-induced and delayed fracturefemoral other pathologies including bone infarction, osteomyelitis and stress fractures and pseudofractures secondary to osteomalacia, malignancy, all of which typically demonstrate diffuse radiotracer which usually occur on the medial cortex due to compressive uptake centred on the medullary cavity [9]. load through the proximal femur [9]. Atypical femoral fracture atypical femoral fractures is important to ensure an early accurate lesion, unlike pathologic fractures [9]. Once a unilateral AFF is Familiarity with the specific imaging characteristics of margins are well defined with no associated destructive bone diagnosed, it is important to image the contralateral femur given clinician to enable optimal treatment, prevention of progression the propensity for these fractures to occur bilaterally (Figure 10) todiagnosis complete and femoral prompt fractures communication and associated of findings complications to the referring [8]. [9,32]. Up 62.9% of patients demonstrate a contralateral femoral fracture, most commonly within a year of the index fracture and PATHOLOGIC FRACTURES with similar imaging features, including location along the femur Pathologic fracture secondary to a tumour can be either due [32]. to a primary bone tumour or secondary metastasis. The femur

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Figure 6 Plain radiograph illustrating focal periosteal and endosteal C) thickening (arrow) of the lateral cortex of the proximal femoral

Plain radiograph of an incomplete transverse radiolucent diaphysis, an early sign of AFF referred to as cortical ‘beaking’ or Figure 8 ‘flaring’. lateral cortical thickening. AFF line referred to as the ‘dreaded black line’ (arrow) traversing the

fallen into the cystic matrix of the lesion may be seen [41]. An MRI is customarily performed to characterise the lesion and may identify stress response seen as increased marrow oedema (high T2 and STIR signal) surrounding an otherwise benign appearing lesion, which can be suggestive of an impending fracture. Fractures through benign femoral lesions can achieve complete healing with low risks of non-union or avascular necrosis [40]. Malignant pathologic fractures can be either due to malignant primary bone tumour or secondary metastasis. According to

myeloma and lymphoma were the most common primary malignanta population-based bone tumours study, to osteosarcoma, present as pathologic Paget’s sarcoma, femoral A) B) C) fractures [42]. In our experience, pathologic femoral fractures through chondrosarcoma is not uncommon (Figure 13). The Figure 7 Plain radiograph, 7b Coronal CT and 7c Axial CT images femur is the third commonest site of bone metastasis after the demonstrating more generalised diffuse lateral femoral cortical spine and pelvis [43], and the commonest cause for femoral thickening (arrows) indicative of pending AFF. metastasis is from breast or lung primary [44,45]. Fractures through malignant bone tumours carry a poorer prognosis with a is the commonest site of pathologic fracture through a primary considerable number of cases requiring amputation [42]. bone tumour [37,38], and it is vital to distinguish them into Plain radiographic and CT features of malignant pathological benign or malignant lesions, as their management and prognosis can be substantially different. permeative lesion with endosteal scalloping, cortical destruction The proximal femur is a common location for benign primary orfractures aggressive include periosteal a fracture reaction traversing [46]. A mineralised a more ill-defined tumour bone tumours [39]. Some of the common benign primary bone matrix (Figure 13), associated soft tissue mass and fracture in an tumours that can lead to pathologic femoral fracture are giant unusual location such as avulsion fracture of the lesser trochanter [47,48] in adults should always raise suspicion of underlying unicameral bone cyst, aneurysmal bone cyst and enchondroma malignancy. Multiplicity of lesions is a helpful clue for metastatic [cell40]. tumour Pathological of bone fractures (Figure 11), through fibrous benign dysplasia femoral (Figure lesions 12),

diseaseMRI (Figuremay be 14)useful or myelomato differentiate but is notpathologic always definitive.fractures from are usually identified on plain radiographs as a break in the of the lesion. In the case of simple bone cysts, the characteristic plain radiographs [8]. MR assessment should be based on the continuity of the cortex and often sclerotic well-defined margin marginstress or and insufficiency homogeneity fractures, of the T1 which signal can abnormality be problematic around on ‘fallen fragment sign’ representing a cortical fragment which has Ann Orthop Rheumatol 7(1): 1092 (2020) 5/8 Chaudhary SR, et al. (2020)

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may be inconspicuous as tumour erodes trabecular bone and 8]. Other features such as an associated soft tissue component or muscle oedema may be presentinfiltrates on the MRI fracture [8]. space (Figure 11b) [ Positron emission tomography (PET-CT) can also be helpful in differentiating malignant pathologic fractures from stress or

focal or linear tracer uptake in the later [51]. insufficiency fracture, with diffuse tracer uptake in the prior and CONCLUSION Femoral fractures caused by an absence of acute trauma or by low-energy trauma must be investigated thoroughly with imaging. Awareness of the relevant imaging features of unusual

and appropriate management. Plain radiography is recommended femoral fractures ensures timely identification, characterisation

Figure 9 Plain radiograph illustrating progression to a complete AFF which is typically non-comminuted, transversely orientated laterally with a short oblique orientation medially leading to a characteristic medial cortical spike (arrow).

A) B)

Figure 11 a: Plain radiograph and 11b Coronal T1 MR image of a pathological fracture through a tumour extending into the femoral

A) B) with a giant cell tumour of bone. The T1 signal abnormality has a homogenousepiphysis with mass-like a relatively appearance well-defined that margin is clearly (arrows) delineated consistent from adjacent normal fatty marrow. The fracture line is inconspicuous as

tumour infiltrates the fracture space.

C) D)

Figure 10 a: Plain radiograph, 10b Coronal STIR MR image, 10c Axial T2 fat saturated MR image and 10d Technitium-99m bone scan of bilateral AFF. Lateral symmetrical femoral cortical thickening with subtle incomplete fracture lines (arrows) can be seen on the plain radiograph, low signal lateral cortical thickening (arrows) with high signal intramedullary oedema is present on the MRI and focal radiotracer uptake (arrows) is demonstrated on the bone scan at the fracture site centred on the lateral femoral cortex. A) the fracture [49,50]. In stress signal intensity associated with the fracture line correlates to or insufficiency fractures, T1 low margin and heterogeneous appearance due to patchy intervening preservedoedema and fatty haemorrhage marrow (high and T1) demonstrates signal intensity a poorly (Figure defined 3b). In tumoral pathologies, low T1 signal is at least partly caused Figure 12 Coronal CT image of a transverse pathological mid femoral diaphyseal fracture through a well delineated lesion with a ground like abnormality (Figure 11b) or diffuse replacement of the fatty marrowby tumour with and tumour seen as [ 8,49,50a more]. well-defined In such cases, homogenous the fracture mass- line dysplasia. glass matrix (arrows) and no aggressive features indicative of fibrous

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