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Bone Scintigraphy: Lessons Learned From 5000 Horses
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Bone scintigraphy is an important part of comprehensive lameness and sports medicine evaluation; it can help to provide answers to important lameness questions. Bone scintigraphy is often the only way to diagnose conditions of the upper limbs and axial skeleton and to document the presence of stress-related cortical and subchondral bone injury. Additionally, it has prompted the discovery of new lameness conditions in horses.
1. Introduction
In 1981, conventional radiography was still being refined and was the mainstay of lameness imaging. Xeroradiography was used by some referral centers and was useful for the evaluation of the interstices of bone for such abnormalities as incomplete fractures. However, edge enhancement made evaluation of the margins of bones difficult, and it had limited value in the evaluation of soft tissues. Ultrasonographic imaging was in its infancy, and the mystery of proximal suspensory desmitis, as we know it today, was just being described.
Over the last 24 yr, much has changed. Ultrasonographic evaluation has revolutionized our understanding of soft-tissue injuries, and currently, magnetic resonance imaging (MRI) is rapidly gaining popularity and holds great promise. Computed tomography (CT) is available at a small number of referral centers. Computed and digital radiography are now common and have upgraded from conventional radiography.
The foresight, perseverance, and hard work of pioneers of equine scintigraphy have developed, evaluated, and refined this modality into a well-recognized and respected imaging technique [1-4]. These researchers paved the way for a new generation of "scintigraphers," of which I am one, that includes many private and university practitioners. Recent advances in gantry design, readily available refurbished and reliable equipment, and affordable, versatile computer hardware and software have helped further refine equine nuclear medicine. I have imaged 5000 horses in my university referral practice over the last 12 yr and have an enormous respect for this imaging tool. Many questions about clinical lameness that were not answered with radiography are now understandable using scintigraphy. In particular, I have an interest in lameness of the fetlock joint in racehorses.
2. Answers to Lameness Questions
Nuclear scintigraphy is an enormously useful tool in lameness diagnosis when used with reasonable expectations and proper case selection. It is an important ancillary imaging modality, but it is not an "answer machine". Often, clients expect that a single pass of the gamma camera or a single trip into the magnet for MRI will provide answers to what are often chronic, complex, and multifaceted lameness problems. Additionally, scintigraphy cannot provide an answer to every lameness problem, but it can provide useful and interesting clinical information that can then be factored into the total lameness picture.
Subchondral Bone Pain in the Fetlock Joint
The metatarsophalangeal joint (MTPJ) has historically been under-recognized as a source of hindlimb lameness, but, in my practice, it was equal in importance to the tarsus; in fact, it is one of the most important sources of pain in the Standardbred (STB) racehorse [5,6]. In the mid to late 1980s, I recognized a perplexing problem, primarily in the STB MTPJ. Clinical signs consistently included decreased performance and a short, choppy gait or stride in horses with bilateral lameness and mild to moderate lameness in horses with unilateral hindlimb lameness and effusion; a positive response to lower-limb flexion tests was absent or inconsistent. Historically, horses could be "blocked sound" but not "injected sound", according to trainers and referring veterinarians. Low plantar perineural diagnostic analgesia was most consistent in abolishing pain, but, in some horses, intra-articular analgesia was effective or partially effective. Conventional radiographs and xeroradiographs were negative or equivocal in most horses, but occasionally, mild sclerosis of the subchondral bone of the third metatarsal bone (MtIII) was seen. Scintigraphy provided the answer. Focal areas of increased radiopharmaceutical uptake (IRU) in the subchondral bone of MtIII were the hallmark of this clinical syndrome [7-9]. The most common area of IRU was the distal, plantarolateral aspect of MtIII; often, IRU was bilateral (Fig. 1).
Figure 1. (A) Lateral and (B) plantar delayed-phase scintigraphic images of a 4-yr-old trotter with maladaptive or non-adaptive bone remodeling of the distal plantarolateral aspect of the left MtIII. Focal IRU (arrows) in the subchondral bone of MtIII is the most common scintigraphic finding in the metatarsophalangeal joint. In: Dyson SJ, Pilsworth RC, Twardock AR, Martinelli MJ. Equine Scintigraphy. Newmarket, UK: Equine Veterinary Journal 2003; 153-189 [9].
Stress Remodeling and Maladaptive or Non-Adaptive Remodeling
The name maladaptive or non-adaptive bone remodeling has been used, but remodeling is a difficult concept to explain. The concept that bone changes shape and strength, modeled and remodeled, in response to the magnitude and direction of strain (Wolff's law) explains many of the changes in bone morphology seen in the sport horse, particularly in young racehorses. Repetitive cyclic loading of bone in racehorses causes predictable change in both cortical and cancellous bone, although those of cortical bone are better understood. Stress fractures of cortical (long) bones can lead to catastrophic bone failure and breakdowns. Adaptive changes in bone in response to repetitive cyclic loading include modeling, micromodeling, and remodeling [10]. Modeling is the change in shape of a bone, and the most familiar change is the dramatic change in the dorsal cortex of the third metacarpal bone (McIII) in Thoroughbreds that is caused by the addition of normal lamellar or abnormal fiber bone in response to changes in strain [10,11]. Micromodeling occurs in cancellous bone, and it is the normal process by which trabecular bone in the subchondral region strengthens and changes shape because of compressive and tensile forces. This process results in subchondral sclerosis; if accelerated, this process can result in deposition of biomechanically inferior woven rather than lamellar bone [10]. Bone remodeling is the process by which formed bone in both regions undergo resorption and replacement by mature lamellar bone. During resorption, bone porosity increases, and stiffness decreases. When microdamage or microfracture formation outpaces bone deposition in the remodeling process, both cortical and cancellous bone are subject to fracture. In cortical bone of the McIII, high-strain cyclic fatigue has been proposed to cause decreased stiffness, which in turn causes the bone to strengthen [11]. Dorsal cortical fractures or stress fractures may develop if high-strain cyclic fatigue occurs when the remodeling process of bone resorption is dominant [11].
In the clinical situation, the concept of a continuum of stress-related bone change in both the cortical and cancellous bone is useful in understanding the pathogenesis of predictable stress-related bony injury that ultimately leads to the development of lameness, fractures, and osteoarthritis (OA). This process is sometimes referred to as "adaptive bone change" in the normal portion of the spectrum and "non-adaptive" when the process becomes pathologic. It is proposed that normal bone undergoes modeling and remodeling as a response to training to strengthen and endure cyclic fatigue. Cortical thickening and subchondral sclerosis are normal events, but when the process becomes pathologic, sequential bone changes of stress reaction, stress fracture, and catastrophic fracture sometimes occur. Stress reaction is a term used to indicate abnormal bone remodeling that is scintigraphically, but not radiographically, apparent; it is thought to precede stress fracture. Recent studies of the dorsal cortex of the McIII and other long bones such as the tibia, humerus, and ilium show stress-related bone changes exist before fracture. Microfractures and periosteal callous indicative of stress fracture preceded complete fracture in both the humerus and pelvis [12,13]. Stress-related changes of cortical bone are familiar radiographically, because thickened areas of cortex, linear areas of radiolucency corresponding to new periosteal bone formation, proliferative changes, and oblique fracture lines all represent stress fracture.
However, stress-related changes of the cancellous bone are more difficult to see radiographically, and diagnosis can be challenging. A remodeling scheme of the distal McIII and MtIII similar to that seen in cortical bone has been proposed to account for subchondral bone changes and overlying cartilage damage and fracture [7,8,14]. The term traumatic osteochondrosis was suggested to describe the remodeling process of the distal McIII/MtIII in Thoroughbreds [15]. This disease has also been termed osteochondritis dissecans (OCD) of McIII, implying that the problem is developmental in nature; this term is misleading, because the injury is an acquired stress-related lesion [16,17]. While the distal aspect of the McIII/MtIII is a region commonly subject to stress-related bone changes, the carpal bone, in particular the third carpal bone (C-3), and the distal tarsal bones are also commonly affected [16].
Subchondral bone plays a huge role in the development of joint disease, and therefore, I prefer to use the term OA rather than degenerative joint disease. The term OA implies that there is inflammation (deterioration) of the bone (osteo) and the joint (arthro). OA describes the overall degenerative process occurring in the subchondral bone, the overlying articular cartilage, and the synovial membrane, and it highlights the importance of the subchondral bone. This is particularly important in young racehorses who can have substantial subchondral bone changes. Understanding the role of subchondral bone is crucial in the diagnosis of injury, particularly in the early diagnosis of young racehorses, and it aids explanation to clients, trainers, and colleagues. For instance, common clinical findings of synovitis (effusion) or radiographic changes such as marginal osteophytes occur later in horses with OA; however, in many of these patients, obvious scintigraphic findings and subtle radiographic changes such as sclerosis of subchondral bone or mild radiolucency will be present. It is well accepted that many of the common articular fractures, such as carpal chip fractures and McIII/MtIII condylar fractures, usually occur in abnormal bone. Although fractures could be single-event injuries originating from a "bad step" or "hole in the racetrack," they are more commonly the last event that occurs in abnormal bone. In summary, stress-related subchondral bone changes are thought to be a normal adaptive response of cancellous bone to training. However, the process often becomes maladaptive or non-adaptive. Ischemia (controversial) of dense subchondral bone, microtrauma or microfractures, mechanical trauma to overlying cartilage caused by dense subchondral bone, and weakened subchondral bone caused by intense resorption pre-disposes the horse to the development of articular fractures (such as chip or condylar fractures) or OA.
Bone scintigraphy is of tremendous value in identifying early stress-related changes in bone and in monitoring healing. Focal, mild to intense areas of IRU in cortical or subchondral bone indicate active bone remodeling and possible fracture. Predictable sites of stress reaction or stress fracture occur in young racehorses undergoing intense race training. In cortical bone, these sites, such as the humerus, tibia, and pelvis, are well known and accepted. In cancellous bone, the common sites include the distal aspect of McIII (medial > lateral) and the distal aspect of MtIII (lateral > medial). In the continuum of events that leads from the normal adaptive response of cortical or cancellous bone to a maladaptive or non-adaptive process (pathologic bone) and subsequent fracture or OA, abnormal scintigraphic findings often precede lameness, which in turn precedes radiographic evidence of remodeling changes or fracture. In subchondral bone, scintigraphic evidence of focal areas of IRU can help the clinician identify regions of sclerosis or radiolucency, particularly if special radiographic views are used to evaluate subchondral bone. I find it interesting that lameness is more likely to be abolished using perineural rather than intra-articular analgesia. This finding supports the idea that overlying cartilage damage occurs relatively late in this process; additionally, pain is emanating from subchondral bone. This could also explain the lack of clinical signs such as effusion, the positive response to flexion tests, and the lack of response to intra-articular medication. Client communication can be difficult in young horses with stress-related subchondral bone injury simply because the classic signs of OA or fracture do not exist either clinically or radiographically. This process may be best understood by clients by referring to quotes such as "...he was making progress faster than his bones were keeping up" (Bramlage) or "...he outran his bones" (Searcy) [18].
The Distal Phalanx
Our recent retrospective study of racehorses with fractures of the distal phalanx confirmed that the most common distribution of distal phalangeal fractures is the lateral aspect of the left forelimb and the medial aspect of the right forelimb [19]. Medial fractures are most common in the hindlimb [19]. In some racehorses with "sore front feet," I have found mild-to-intense IRU in the central and palmar aspects of the distal phalanx in lateral aspect of the left forelimb and the medial aspect of the right forelimb; this is the same distribution found in horses with distal phalangeal fractures (Fig. 2) [19,20]. Increased radiopharmaceutical uptake of the distal phalanx was seen in horses examined for poor performance or lameness that later developed fractures in the distal phalanx in the same location, a finding that has led us to believe that forelimb distal phalangeal fractures are the result of a continuum of stress-related bone injury (stress fracture) rather than a single-event traumatic injury [19,20]. The distal phalanx seems prone to the effects of maladaptive or non-adaptive remodeling, and in the forelimbs, distribution may be determined by the effects of counterclockwise racing. Focal areas of IRU in subchondral bone of the distal phalanx are likely similar to those in the distal aspect of MtIII/McIII and may lead to fracture of the distal phalanx or OA of the distal interphalangeal joint (Fig. 3).
Figure 2. Lateral (left two images) and dorsal (left front is on the right) delayed-phase scintigraphic views of both distal forelimbs. IRU is seen in the distal phalanges in a typical pattern of the lateral aspect of the left forelimb and medial aspect of the right forelimb. In: Dyson SJ, Pilsworth RC, Twardock AR, Martinelli MJ. Equine Scintigraphy. Newmarket, UK: Equine Veterinary Journal 2003; 153-189 [9].
Figure 3. (A) Solar delayed-phase scintigraphic image and (B) dorsolateral palmaromedial oblique xeroradiographic view of the left forelimb distal phalanx in a 3-yr-old STB filly. IRU in the subchondral bone of the distal phalanx was seen 6 mo before these images were taken, but radiographs were negative. The filly was rested and returned to work only to develop acute, pronounced lameness localized by palmar digital analgesia. Intense IRU in subchondral bone of the distal phalanx in A corresponds to the incomplete fracture (A, arrows) seen in the horizontal oblique xeroradiographic projection. In: Dyson SJ, Pilsworth RC, Twardock AR, Martinelli MJ. Equine Scintigraphy. Newmarket, UK: Equine Veterinary Journal 2003; 153-189 [9].
Palmar Digital Analgesia
The most common cause of lameness in all types of racehorse and non-racehorse sport horses involves the foot or digit and can be abolished by palmar digital analgesia (PDA) [21]. I have long disagreed with the common perception that PDA only abolishes pain associated with the palmar one-third of the foot. In my clinical impressions, PDA abolishes pain from a majority of the foot and pastern region and can abolish pain associated with conditions of the fetlock joint such as mid-sagittal fractures of the proximal phalanx, fractures of the proximal sesamoid bones (PSBs), and MtIII/McIII condylar fractures [5,20]. Of 164 racehorses and non-racehorse sport horses in which lameness was abolished using PDA, findings included non-adaptive remodeling/fracture of the distal phalanx (41 racehorses), subchondral trauma/remodeling (20 non-racehorses), combination of navicular disease/subchondral trauma (19 non-racehorses), soft-tissue injuries of the foot (7 horses), OA of the distal interphalangeal joint (7 horses), OA of the proximal interphalangeal joint (6 horses), undiagnosed foot soreness (6 horses), laminitis (4 horses), old wing fractures of the distal phalanx (4 horses), dorsal laminar trauma of the distal phalanx (3 horses), mid-sagittal fractures of the proximal phalanx (2 horses), IRU of the cartilages of the foot and proximal aspect of the distal phalanx (2 horses), trauma of the proximal palmar aspect of the middle phalanx (1 horse), navicular bone fracture (1 horse), and distal phalangeal extensor process fracture (1 horse) [20]. Pain was not limited to the palmar aspect of the foot, and in fact, conditions involving the dorsal aspect of the foot and pastern were numerous, confirming my clinical suspicion that PDA is a comprehensive block capable of abolishing pain from a majority of the foot, pastern, and, in some horses, fetlock region (Fig. 4). Recent studies have confirmed that PDA abolishes pain from a majority of the foot including the toe region and that differential blocking of horses with lameness in this region is problematic because of communications between synovial cavities, the close proximity of nerves to synovial structures, and the potential diffusion of local anesthetic solution [22-26].
Figure 4. (A) Dorsal (left two images) and flexed dorsal (right image) delayed-phase scintigraphic images and (B) the dorsomedial palmarolateral oblique digital radiographic projection of the fetlock joint of a 4-yr-old STB pacer with right forelimb lameness localized to the digit by palmar digital analgesia. Focal mild to moderate IRU can be seen in the right forelimb fetlock region (A, dorsal image), primarily on the medial aspect. In the flexed dorsal image, focal IRU can be seen involving the distal aspect of the McIII and medial PSB. A non-displaced apical fracture of the medial PSB can be seen in B.
Bone scintigraphy has been invaluable to me in diagnosis of horses with lameness abolished with PDA. In my referral practice, horses with abnormalities of bone far outnumber those with soft-tissue injuries, but, in many horses, the sources of pain may be multifocal. The early results with MRI suggest that there is often more than one lesion, and this modality will undoubtedly be useful in correlating the clinical and other imaging information. I urge practitioners who are pioneering MRI to keep in mind the importance of bone, in particular the subchondral bone of the distal phalanx and navicular bone, when developing image sequences to evaluate this complex area and to opine a final diagnosis.
Stress Fractures
Acute, pronounced lameness after training or racing that abates within a few days only to recur when the horse is worked again is a common anamnesis in a racehorse with a cortical stress fracture. Before nuclear medicine techniques, this diagnosis was made sparingly at our hospital, but now, using bone scintigraphy, the diagnosis is readily made in 50 - 100 horses each year. Radiographic and ultrasonographic examinations may be useful in delineating cortical defects in racehorses with stress fractures of the pelvis and other long bones, but bone scintigraphy is the consummate imaging modality for diagnosis of stress fractures. A straightforward diagnosis can be made even in areas (upper hindlimb and pelvis) where radiographic evaluation is difficult or potentially dangerous if general anesthesia is required (Fig. 5 and Fig. 6).
Figure 5. Dorsal oblique delayed-phase scintigraphic image of the left hemipelvis in a 3-yr-old Thoroughbred filly racehorse with pelvic stress fractures (arrows) involving the base of the tuber sacrale in the ilial wing (cranial fracture) and body of the ilium.
Figure 6. (A) Delayed-phase scintigraphic images of a typical proximal, caudal medial humeral stress fracture in a Thoroughbred in race training. Radiographically, the region is difficult to evaluate, but focal intense IRU is easily seen in this lateral scintigraphic image. (With permission, Davidson EJ, Ross MW. Clinical recognition of stress-related bone injury in racehorses. Clin Tech in Equine Pract 2003; 2:296-311). (B) Delayed-phase scintigraphic images of a humeral stress fracture in a 2-yr-old STB racehorse with a rare cause of forelimb lameness. Lateral (upper two images) and cranial images showing unusual IRU of the caudal medial humeral cortex in this STB with bilateral forelimb lameness. A diagnosis of cortical bone injury consistent with bilateral humeral stress fractures was made. In: Dyson SJ, Pilsworth RC, Twardock AR, Martinelli MJ. Equine Scintigraphy. Newmarket, UK: Equine Veterinary Journal 2003; 153-189 [9]. Kraus BM, Ross MW, Boswell R. Humeral stress fractures in 4 Standardbreds. Vet Radiol Ultrasound 2005; submitted for publication.
3. New Diagnoses
Scintigraphy is one of the few ways to diagnose abnormalities of the upper limbs and axial skeleton. In our study of 128 horses with hindlimb lameness or poor performance, scintigraphy was useful in identifying abnormalities of the pelvis and skeletal muscle including the tuber coxae (25 horses), tuber ischii (9 horses), coxofemoral joint (10 horses), ilium (5 horses), tuber sacrale/sacroiliac region (22 horses), greater trochanter (1 horse), cranial femoral cortex (1 horse), skeletal muscle surrounding the pelvis (34 horses), and multiple areas (11 horses) [27]. It was difficult to correlate lameness and abnormal scintigraphic findings; however, in 44 horses, the scintigraphic abnormality was thought to be the primary source of lameness [27]. Scintigraphy was useful in establishing the diagnosis in horses with severe lameness as the result of displaced fractures of the pelvis, including the coxofemoral joint, without the potential dangerous use of general anesthesia. Scintigraphy was not only useful in the diagnosis of previously described clinical problems, but it also allowed us to investigate previously unrecognized or rarely described causes of hindlimb lameness.
Fracture or Enthesopathy of the Tubera Ischii
Fracture or enthesopathy of the tubera ischii can be a straightforward diagnosis if swelling is pronounced and there is disparity in pelvic heights and widths. In some horses with chronic hindlimb lameness, diagnosis can be challenging. Horses may have a history of running backwards into a stationary object or falling backwards, and there may be subtle defects or atrophy of the semimembranosis and semitendinosis muscles. Fracture or enthesopathy of the tubera ischii can readily be diagnosed using bone scintigraphy. Adjunctively, ultrasonographic imaging allows evaluation of the origins of the caudal thigh muscles to detect muscle injury or the presence of fracture fragments (Fig. 7).
Figure 7. (A) Dorsal and (B) caudal delayed-phase scintigraphic images of a 2-yr-old Arabian with acute right hindlimb lameness and mild swelling and pain in the right caudal thigh region. Focal, moderate IRU (arrows) can be seen in the right tuber ishium consistent with fracture or enthesopathy. Ultrasonographic evaluation revealed hemorrhage and tearing of the caudal thigh muscles. Diagnosis of this injury is difficult to make and confirm without scintigraphic examination.
A rare cause of hindlimb lameness is injury to the gastrocnemius muscle at the origin on the distal, caudal femur at the musculotendinous junction or in the tendonous portion and bursa. Bone modeling from fracture or enthesopathy at the origin of the gastrocnemius muscle on the distal caudal femur can be readily seen using delayed-phase scintigraphic imaging [28].
Fracture or Enthesopathy of the Third Trochanter of the Femur
Fracture or enthesopathy of the third trochanter of the femur is a difficult if not impossible diagnosis to make without using bone scintigraphy, and it was a diagnosis that I did not previously make (Fig. 8) [27]. The superficial gluteal muscle inserts at the third trochanter, and avulsion injury, fracture, or enthesopathy at insertion can occur. In our study, 10 horses had IRU of the third trochanter [27]. All were racehorses, there were no localizing clinical signs, and all horses had mild to moderate lameness scores (1 - 3 based on a scale of 0 being sound and 5 being non-weight bearing) [27]. Lameness was attributed to the third trochanter in four horses; primary lameness was determined to be in other limbs in three horses, and, in three horses, source of lameness was not identified [27].
Figure 8. Lateral delayed-phase scintigraphic image of the right upper hindlimb showing focal, moderate IRU (A, arrow) of the third trochanter of the femur in a 4-yr-old STB trotter with primary (baseline) lameness of the left forelimb (OA of the distal interphalangeal joint). Enthesopathy of the right third trochanter may be a compensatory lameness issue, because diagonal compensatory lameness in trotters is common. In: Dyson SJ, Pilsworth RC, Twardock AR, et al. Equine Scintigraphy. Newmarket, UK: Equine Veterinary Journal 2003; 153-189 [9].
Skeletal Muscle Injury
Damaged skeletal muscle behaves like damaged bone during scintigraphic examination. Muscle injuries are best seen on delayed-phase rather than pool (soft-tissue) phase images. In general, two patterns of IRU of skeletal muscle are seen: generalized rhabdomyolysis and localized IRU of individual muscle bellies (Fig. 9). Generalized IRU of skeletal muscle in racehorses is in most instances an unexpected scintigraphic finding that may well explain poor performance; it may even explain lameness after a work or race. Comprehensive evaluation including scintigraphic examination is important in any sports medicine program. Increased radiopharmaceutical uptake can be seen up to 7 - 10 days after the last race or training session. Only mild elevations in CK and AST enzymes are usually seen.
Although it is compelling to incriminate muscle injury as a primary source of pain in horses with IRU of individual muscle bellies, the authentic source of lameness is usually elsewhere. The primary source of pain is usually found somewhere else in the ipsilateral limb (Fig. 9). It is possible that horses compensate for painful conditions in the lower limb and develop muscle strain or other injury in the upper hindlimb.
Figure 9. Dorsal right hemipelvic delayed-phase scintigraphic image of a 2-yr-old STB pacer with right hindlimb lameness. There is moderate to intense IRU in the right gluteal muscle. Damaged skeletal muscle is easily imaged in delayed (bone) phase images. The primary source of pain was an ipsilateral dorsal cortical MtIII fracture, and the relationship between the two abnormalities is unknown.
Enostosis-Like Lesions
For years, small radiodensities in the medullary cavities of long bones, in particular the McIII/MtIII, were thought to be incidental radiographic findings [29]. In some horses, they are still likely to be incidental, but, by using bone scintigraphy, we have described a new clinical syndrome causing lameness in some horses. We coined the name enostosis-like lesions (ELLs) to describe these medullary opacities. ELLs are focal or multifocal areas of IRU within the medullary cavity of long bones that correspond radiographically to multiple round or irregularly shaped radiodensities [29]. In our study of 10 horses with ELLs, lameness was attributed to ELLs in five horses, whereas ELLs were thought to be incidental findings in the other five horses [29]. ELLs of the radius, humerus, and tibia (in particular, those that are large, focal areas of intense IRU) are more likely to cause lameness than small ELLs found in the McIII/MtIII (Fig. 10). Lameness can be acute or chronic and can be unilateral or involve more than one limb simultaneously or at different times. Two scintigraphic views are required to differentiate medullary from cortical uptake. It is imperative to differentiate ELLs from cortical IRU seen with stress fractures.
Figure 10. (A) Lateral and (B) caudal delayed-phase scintigraphic images of both femurs of a 12-yr-old Warmblood admitted for scintigraphic evaluation for right hindlimb lameness. Focal, intense IRU is seen in the medullary cavity of the right femur in both views, and a diagnosis of ELLs was made. Three months earlier, acute right forelimb lameness prompted delayed-phase scintigraphic examination of the forelimbs, and a diagnosis of ELL of the right humerus was made (A, lateral views).
Etiology of ELLs is unclear, and the condition has often been referred to as bone islands or bone infarcts. Pathophysiological and radiographic findings are similar to dogs with panosteitis, and there are characteristics similar to bone infarcts, bone islands, and intramedullary osteosclerosis seen in people [29]. Histopathological evaluation of a bone biopsy of an ELL in the distal humerus in a Warmblood was consistent with stress fracture [a].The precise etiology remains unclear, but identification of horses with this unique syndrome requires scintigraphic examination.
4. Bone Scintigraphy and Radiography/Radiology
Bone scintigraphy has taught me the importance of detailed radiographic examination and has prompted me to take additional and sometimes "designer" radiographic views that help to sharpen my radiological interpretation. There is nothing like a "hot spot" on a bone scan to allow for varied interpretation of a radiograph.
Seeing focal areas of IRU in the distal McIII/MtIII (Fig. 1) prompted the acquisition of "down-angled" oblique radiographic views to adequately evaluate the condyles of McIII/MtIII for sclerotic and radiolucent changes (Fig. 11). These views are now routinely taken and have improved our ability to evaluate the palmar/plantar aspect of the metacarpophalangeal joint/MTPJ; however, small osteochondral fragments in the dorsal aspect of these joints can be missed on the down-angle oblique projections. On conventional horizontal oblique views, the PSBs obscure the ability to evaluate the distal aspect of McIII/MtIII, and, in the hindlimb, there is often overlap of the distal aspect of the PSBs and the proximal aspect of the proximal phalanx. Flexed dorsopalmar/plantar views are useful in the radiographic evaluation of maladaptive or non-adaptive bone injury.
Figure 11. (A) Dorsomedial palmarolateral digital radiographic view of the MTPJ taken with the conventional horizontal radiographic beam and (B) a dorsal 25 - 30° proximal palmaromedial (down-angle) oblique digital radiographic view. With a horizontal radiographic beam, the medial PSB overlaps the distal McIII, whereas with the down-angled radiographic beam, the space between the PSBs and the proximal phalanx is opened to allow evaluation of radiolucent and sclerotic changes (arrow) associated with maladaptive or non-adaptive bone remodeling of the distal medial aspect of McIII. (With permission, Davidson EJ, Ross MW. Clinical recognition of stress-related bone injury in racehorses. Clin Tech in Equine Pract 2003; 2:296-311.)
Recognition of focal areas of IRU in subchondral bone of the distal phalanx representing areas of maladaptive or non-adaptive bone remodeling and stress fractures in racehorses and areas of subchondral bone injury associated with OA of the distal interphalangeal joint in non-racehorses prompted us to rethink radiographic evaluation of the foot. Rather than rely only on elevated, down-angled views of the wings of the distal phalanx, we now use a horizontally directed radiographic beam with the foot elevated on a block to acquire standard oblique views on horses in which lameness is abolished using PDA (Fig. 3) [19,20]. Horizontal oblique views are advantageous in evaluating the subchondral bone of the distal phalanx for the presence of radiolucent defects, in evaluating the distal phalanx for the presence of incomplete fractures, in evaluating the margins of the distal interphalangeal joint for osteophyte formation, and in evaluating the dorsal aspect of the distal phalanx for proliferative changes associated with chronic inflammation (dorsal laminar tearing) [20].
Modeling of the navicular bone was a common scintigraphic finding in the study of horses with lameness abolished using PDA, and it confirmed the importance of the palmar proximal palmar distal (skyline, tangential) radiographic view [20]. Often, conventional views of the navicular bone will be negative or equivocal, but sclerotic and radiolucent changes in the medullary cavity of the navicular bone, the blending of the medullary cavity and palmar cortex, and palmar cortical changes can only be seen on this radiographic view. This view is now routinely taken in horses in which lameness is abolished using PDA.
The dorsoproximal dorsodistal (skyline, tangential) radiographic view of the distal row of carpal bones is now considered routine in the radiographic evaluation of the carpus. Dorsal, lateral, flexed lateral, and flexed dorsal scintigraphic views of the carpus can be used to pinpoint lesions to the radial fossa of C-3, and critical review of skyline projections can be done with this information in mind. Careful positioning and exposure of the radial fossa are the keys in the diagnosis of maladaptive or non-adaptive bone remodeling of C-3 in young racehorses, and the differentiation of this problem from the more advanced changes associated with incomplete fracture or subchondral lucency of C-3 are very important.
In horses with early OA of the tarsometatarsal and distal intertarsal joints and in those with frontal slab fractures of the third tarsal bone (T-3), scintigraphic examination routinely reveals IRU in the dorsolateral aspect of the distal tarsus [26]. The dorsomedial palmarolateral oblique (DMPLO) view is the most important radiographic view for the evaluation of subtle changes associated with early OA and incomplete T-3 slab fractures.
5. Authentic Negative and False-Negative Scans
Negative scintigraphic examination can in itself provide a clinical direction by ruling out active bony remodeling. For instance, a horse is entered in a stakes race but develops acute hindlimb lameness after its last work. Expecting a problem in the foot, the veterinarian wants to ensure that incomplete fractures or stress-related bone is not present. A dressage horse has a chronic obscure performance problem of questionable musculoskeletal origin. A negative whole-body bone scan would ensure that a training intensity change could be achieved without further exacerbating an existing bony lesion. Negative or equivocal hindlimb scans in horses with pronounced lameness lead me to suspect lameness of the stifle region and help me diagnose proximal suspensory desmitis, particularly in non-racehorse sport horses. The sensitivity of stifle scintigraphy seems to be low, and many conditions of this joint fail to produce marked scintigraphic changes. Many horses with proximal suspensory desmitis will lack substantial IRU on delayed-phase images. Bone scintigraphy should not be used as a means to diagnose proximal suspensory desmitis, although modeling at the suspensory origin, stress reaction, stress fracture, or avulsion fracture of the McIII/MtIII will be present in some horses. The sensitivity of pool-phase scintigraphic imaging is questionable because of several factors, including the persistence of the radiopharmaceutical in nearby vessels and the early radiopharmaceutical in the bone. Lesions such as proximal suspensory desmitis must be active and pronounced, and pool-phase images must be carefully interpreted.
Differentiating authentic from false-negative scans requires careful interpretation of images and acquisition of as many views as possible. False-negative scans do occur but most result from problems with limb or camera positioning, body part to camera distance, shielding by overlying soft tissues or bone, background radiation particularly involving the bladder during examination of the pelvis and upper hindlimb, and physeal activity. Distance is a key factor that limits the number of counts contributed by lesions distant to the camera and dramatically affects resolution of the scan. Lesions on the medial aspect of the limb can easily be missed if only a lateral view is taken (Fig. 12).
Figure 12. (A) Lateral and (B) dorsal delayed-phase scintigraphic images of both distal forelimbs and (C) delayed-phase solar image of the right forelimb of a Thoroughbred racehorse with intermittent right forelimb lameness and poor performance. In the lateral view of the right forelimb in A, normal radiopharmaceutical uptake of the distal phalanx is seen, and a diagnosis cannot be made. In the dorsal and solar images, note focal, moderate to intense IRU of the medial palmar process consistent with fracture of the medial wing of the distal phalanx, which was confirmed on radiographic examination. Without the lateral image available for review, the lesion could easily be missed (false negative).
Authentic negative bone scans are not common in horses with stress-related bone injuries. This is because scintigraphic evidence of maladaptive or non-adaptive bone remodeling precedes lameness, and lameness is what prompts referral for scintigraphic examination. However, in horses with acute, traumatic bone injuries such as from a kick or fall, there is a lag phase in bone modeling; within 7 - 10 days of the injury, it is possible to have a false-negative bone scan, particularly in the pelvis where background radiation, distance, motion, and shielding are important factors negatively affecting the quality of the bone scan. Binding of the radiopharmaceutical is dependent on bone modeling or bone formation that is caused by osteoblastic activity, and maximal IRU occurs 8 - 12 days after bone injury [30,31]. Blood supply, long thought to be important in radiopharmaceutical uptake, must be adequate during distribution, but recent evidence exists that there is little relationship between perfusion (blood supply) and bone metabolism (IRU) [32]. During the lag phase before peak osteoblastic activity (after acute fracture), the bone scan could be negative. I have had limited experience imaging horses with known history of bone trauma early after injury, and, to my knowledge, the lag phase has not been studied to date in horses. If follow-up images cannot be obtained at least 9 - 12 days after injury, then the bone scans should be delayed and the images should be carefully interpreted (Fig. 13).
Figure 13. Dorsal left hindlimb and right hindlimb delayed-phase hemipelvic scintigraphic images at (A) 1 day and (B) 9 days after this Thoroughbred racehorse fell and developed acute severe right hindlimb lameness. The initial study in A showed normal radiopharmaceutical uptake (arrow) of the right ilial shaft, but the follow-up study showed focal IRU. There is a lag phase of osteoblastic activity that may account for negative bone scans, particularly of the pelvis, immediately after a traumatic event.
6. False-Positive Bone Scan
Multifocal areas of mild IRU are common particularly when imaging any upper-level sport horse or seasoned racehorse. It is imperative to correlate clinical, scintigraphic, and other findings to accurately determine the primary source of pain in a lame horse or the source(s) of poor performance. Therefore, false-positive scans are common and are not as important as false-negative scans. In some horses, findings may be inexplicable but should be confirmed using diagnostic analgesia whenever possible (Fig. 14).
Figure 14. (A) Lateral and (B) flexed-lateral tarsus delayed-phase scintigraphic images of a 4-yr-old STB trotter with left hindlimb lameness abolished with PDA (*). There is a focal area of intense IRU (A, arrow) in the region of the tarsocrural joint. In the flexed lateral image, focal intense IRU can be seen involving the talus and is consistent with subchondral trauma or fracture of the talus; however, the primary source of pain is abolished using PDA. Note that the additional views improve accuracy of the bone scan. The diagnosis was a soft-tissue injury in the left hindlimb digit, because pain was abolished with PDA and not tarsocrural analgesia (false positive).
7. What About OCD?
Scintigraphic evidence of osteochondrosis, particularly of the hock and stifle in young horses, is often obscured by intense nearby physeal activity. Subtle areas of IRU of the distal glenoid and proximal humerus, proximal plantar aspect of the proximal phalanx, cranial intermediate ridge of the distal tibia, and distal medial femur may indicate the presence of osteochondrosis. Careful interpretation of caudal views of the stifle can help in the diagnosis of osseous cyst-like lesions of the medial (and lateral) femoral condyles.
8. Case Selection and Accurate Interpretation of Images
Case selection is important in determining the usefulness of the bone scan in providing the definitive diagnosis. Racehorses are ideal patients, because these young horses undergo high-impact exercise and are particularly prone to stress-related cortical or subchondral injury. On the other end of the spectrum are older show horses, particularly large breeds such as Warmbloods, that compete in low-level dressage or other performance events. Low-impact exercise coupled with advanced age decrease the usefulness of the technique. Scintigraphic examination may provide disappointing information regarding chronic OA, particularly of the fetlock joint. It is sometimes difficult to find a correlation between scintigraphic and radiographic changes in the tarsus. Scintigraphic examination is useful in horses with lameness of the foot and proximal metacarpus/metatarsus and in horses with back problems.
An additional problem occurs when imaging horses in cold weather, particularly if horses are shipped long distances immediately before injecting the radioisotope. This is more of a problem in large-breed horses, older horses, and horses housed in barns without heat. Delayed (bone-phase) images show expected bone uptake in the upper limbs but distal to or including the tarsus and carpus; scans resembling pool-phase images are obtained, often with compensatory IRU in the distal tibia or radius. This phenomenon may be related to relatively poor blood flow in the distal extremities or the shunting of blood from the periphery during the radiopharmaceutical distribution, and it can be minimized by using distal extremity wraps, exercising the horse before injection, and administrating acetyl promazine. In a recent study, environmental temperature and perfusion and uptake of the radiopharmaceutical were correlated, but there was no relationship between lameness and uptake [33]. In that study, bandaging had no effect, but exercise for 15 min before injection of the radiopharmaceutical consistently improved blood flow and bone uptake [33].
Two important factors that determine the usefulness of the bone scan include: the horse is clinically lame at the time of the scan, and the lameness has been localized. Scintigraphy provides a "functional evaluation" of bone remodeling at one point in time. If a horse with a history of chronic lameness has been rested for several months before evaluation, the chances of seeing increased bony remodeling are greatly diminished.
9. Improving the Accuracy of the Bone Scan
To improve overall accuracy, multiple views should be used. For instance, to determine the position of a focal area of IRU in the fetlock joint, it is important to have lateral, dorsal (plantar), and flexed lateral images. With this information, rather than reporting a finding of a "hot spot in the fetlock joint," the clinician can say that "there is a focal area of IRU involving the distal, plantarolateral aspect of MtIII," which is a much more accurate description of the area of abnormal bony activity. Flexed lateral views of the hock, flexed dorsal views of the carpus, and solar or palmar images of the foot are important. To diagnose medial femorotibial joint disease, a caudal view is mandatory. A bare minimum of two views should be taken, but additional views such as a flexed lateral view will often reveal the precise location of the area of IRU (Fig. 12 and Fig. 14).
10. What About Nerve Blocks?
I do not hesitate to perform bone scintigraphy in a horse in which nerve blocks have recently been performed, but a minimum of two views are mandatory to determine if IRU is artifact in soft tissues as a result of the block or indeed authentic IRU involving bone. Seldom are there artifacts in delayed images with distal-limb perineural or intra-articular analgesia, but after the peroneal and tibial nerve block, focal IRU is seen in delayed images over the cranial tibial cortex in all horses. Without the caudal view showing that the uptake is clearly in the soft tissues (hemorrhage or muscle damage), inadvertent diagnosis of a tibial stress fracture could be made (of course, a tibial stress fracture involving the cranial cortex is unusual).
11. What About Photopenia?
Photopenia in delayed-phase images is most often the result of subperiosteal abscessation, but it can be caused by ischemia of the distal extremity. Careful differentiation between an authentic photopenia area and the normal poor-bone uptake that occurs in horses as a result of shunting blood from the periphery during the distribution phase of the radiopharmaceutical is critical. Photopenia in flow and pool-phase images of the foot may correlate to areas of increased pressure in the hoof capsule from abscessation, hemorrhage, or bruising within the hoof capsule.
12. Using Bone Scintigraphy as a Screening Tool
Bone scintigraphy is best used in lame horses in which lameness has been localized, but it has also proven to be useful in comprehensive sports medicine examination of horses with poor performance. After uncovering areas of IRU, reevaluation for subtle signs of lameness or performance issues and use of selective diagnostic analgesic procedures can be used to "retrofit" clinical signs with the scintigraphic findings. This is particularly useful in racehorses with high-speed lameness conditions. Scintigraphy is often used in horses with hindlimb lameness because of the danger associated with diagnostic analgesia, particularly in Thoroughbred racehorses. Scintigraphic findings should always be used in conjunction with historical and clinical information.
Footnotes
[a] Ross MW, Boswell R, Pool R. Personal communication. 2000
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