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Arnold I. Brenner, DO, MMM, CPE,*, June Koshy, MD,* Jose Morey, MD,*
Cheryl Lin, MD,* and Jason DiPoce, MD*
Bone imaging continues to be the second greatest-volume nuclear imaging procedure,
offering the advantage of total body examination, low cost, and high sensitivity. Its power
rests in the physiological uptake and pathophysiologic behavior of 99m technetium (99mTc) diphosphonates. The diagnostic utility, sensitivity, specificity, and predictive value of
99m-Tc bone imaging for benign conditions and tumors was established when only planar
imaging was available. Currently, nearly all bone scans are performed as a planar study
(whole-body, 3-phase, or regional), with the radiologist often adding single-photon emission computed tomography (SPECT) imaging. Here we review many current indications for
planar bone imaging, highlighting indications in which the planar data are often diagnostically sufficient, although diagnosis may be enhanced by SPECT. 18F sodium fluoride
positron emission tomography (PET) is also re-emerging as a bone agent, and had been
considered interchangeable with 99m-Tc diphosphonates in the past. In addition to SPECT,
new imaging modalities, including 18F fluorodeoxyglucose, PET/CT, CT, magnetic resonance, and SPECT/CT, have been developed and can aid in evaluating benign and malignant bone disease. Because 18F fluorodeoxyglucose is taken up by tumor cells and Tc
diphosphonates are taken up in osteoblastic activity or osteoblastic healing reaction, both
modalities are complementary. CT and magnetic resonance may supplement, but do not
replace, bone imaging, which often detects pathology before anatomic changes are appreciated. We also stress the importance of dose reduction by reducing the dose of 99m-Tc
diphosphonates and avoiding unnecessary CT acquisitions. In addition, we describe an
approach to image interpretation that emphasizes communication with referring colleagues
and correlation with appropriate history to significantly improve our impact on patient care.
Semin Nucl Med 42:11-26 2012 Elsevier Inc. All rights reserved.
lucose (FDG), and positron-emission tomography (PET) imaging and briefly reviews the re-emergence of 18F sodium
fluoride bone PET imaging. We also emphasize how making
use of all available information can enhance our interpretation of planar images, and finally we present an overview of
the role of planar imaging for most common indications for
bone imaging.
Although computed tomography (CT), magnetic resonance imaging (MRI), PET, SPECT, and SPECT/CT have developed into excellent tools for evaluating patients with suspected bony pathology, planar bone imaging has stood the
test of time. More than 3,450,000 bone scans were performed
in the United States in 2005.3 Nearly all bone scans performed still use planar images as their foundation, with
SPECT adding complementary information.
Physiology
The skeleton is a living, active organ that changes during the
normal physiological process of growth and remodeling and
11
A.I. Brenner et al
12
in response to pathologic processes.5 Bone is constantly
changing, with an ongoing level of bone resorption (osteoclastic) and bone formation (osteoblastic). Osteoblasts form
an osteoid matrix that is later mineralized with hydroxyapatite crystals. 99m-Tc diphosphonates chemisorb6 and bind to
the hydroxyapatite crystals in proportion to local blood flow
and osteoblastic activity and are therefore markers of bone
turnover and bone perfusion. They rapidly localize to bone
and clear quickly from background, making them favorable for imaging. Even a 5% change in bone turnover7 can be
detected on bone imaging, whereas on radiographs and CT,
40%-50% of mineral must be lost to detect lucency within
the bone.8-10 Therefore, bone imaging can often detect disease-related dysfunction before anatomic changes are appreciated.11
Bone imaging is sensitive for both primarily osteoblastic
and primarily osteolytic processes. Even a tiny amount of
bony destruction causes an intensely osteoblastic healing
process that surrounds the lytic area. Fractures, osteomyelitis, and lytic metastases are all examples of bony destruction
that can allow early detection of the associated healing process on bone imaging.
Sometimes pathologic bone image findings are characterized by cold areas. This may be caused by very aggressive processes (ie, bone metastasis), indolent processes
that induce little healing reaction (ie, Brodies abscess,
indolent bony metastatic disease, plasmacytoma/neuroblastoma), or disruption of blood flow (ie, cold osteomyelitis, bone infarcts, avascular necrosis, frostbite or gangrene; Fig. 1).12
Figure 1 (A) Patient with metastatic carcinoma of the lung. Note the multiple areas of increased bone agent uptake in a
pattern consistent with metastasis as well as several photopenic areas in the sternum and left sacroiliac joint. (B) A
64-year-old diabetic woman with cellulitis and ulcer of the right great toe on physical examination. Note the nonvisualization of the distal right great toe consistent with biopsy-proven osteomyelitis.
Bone scanning
proving spatial resolution, and enhancing tissue contrast.15
SPECT may improve sensitivity, specificity, and predictive
value in specific situations and may enhance lesion detection
and characterization. If the bone scan were considered a hotdog, SPECT would be a savory condiment, such as mustard
or sauerkraut, which improves its flavor.
Unlike SPECT imaging of the brain and myocardial perfusion, which are routinely performed as stand-alone studies,
SPECT bone imaging has not emerged as a stand-alone procedure. Almost all bone scans are performed as planar studies, with the addition of SPECT imaging of selected areas.
Recent new approaches to camera design and processing of
SPECT data, such as iterative reconstruction, have great
promise in decreasing time of acquisition, patient absorbed
dose, and perhaps improving the sensitivity and resolution of
SPECT data. These innovations are targeted at nuclear cardiology,16 but soon may represent another improvement in the
diagnostic utility of bone scans.
13
14
Modern Applications
of Planar Bone Imaging
Detection and Monitoring of Bone Metastases
In the United States, 350,000 patients develop bone metastases each year.31 The overall sensitivity for detecting bony
metastases is 95%, with a false-negative rate of 2%-5%.32
Whole-body planar bone imaging has been a mainstay for
detection of skeletal metastases21 for more than 35 years. The
ability to image the entire skeleton makes planar bone scintigraphy unique compared with other radiographic techniques and MRI, resulting in a rapid, cost-effective survey of
the entire skeletal system for detection of patterns diagnostic
of bone metastases. It is easy for the patient, has no contraindications, and is very sensitive.33 Planar regional and magnified images may be acquired, on the basis of symptoms and
history, to better evaluate suspicious areas on whole body
imaging.
Multiple sites of abnormal bone agent uptake characterized by pattern of distribution, change over time, or definitive
findings on correlative CT, MRI, or radiographic studies, are
consistent with bone metastases. Only 8%-15%34 of patients
with proven metastases have a single lesion.35 A variant
whole-body bone scan pattern of metastatic bone disease is
the superscan diffusely increased activity throughout the
skeleton with decreased renal activity (absent kidney sign).
This usually reflects diffuse metastatic or metabolic bone disease and radiographic correlation is usually diagnostic. Photopenic areas or cold spots represent another variant seen in
very aggressive metastasis or in indolent metastasis, inducing
little healing reaction. Whole-body bone imaging is also useful in patients with malignant primary bone tumors to detect
metastases, evaluate the extent of tumor within bone, and
detect skip lesions.
In multiple myeloma and neuroblastoma, the sensitivity
for sites of bone involvement is approximately 50%,36 because these are often indolent processes that induce little
healing reaction. Therefore, skeletal survey and FDGPET/CT are more informative than whole body bone
scan.
SPECT is complementary to planar bone images and may
help to differentiate benign and suspicious lesions, particularly in the spine, where it improves predictive value.21
SPECT is more sensitive in detecting and localizing vertebral
lesions than planar imaging, with 20%-50% increase in lesion detection.17,37,38 Vertebral findings on planar and SPECT
imaging tend to follow predictable patterns that are likely to
represent benign changes, often degenerative37 and allow interpretation as no definite evidence for metastatic bone disease. For example, bone lesions that extend outward beyond
the extrapolated margin of the vertebra or show bridging of
activity across the posterior arches or vertebral bodies of
more than one vertebra can be attributed to a benign process.
Direct comparison of SPECT slices in transaxial, sagittal, and
coronal planes with matching slices on recent CT, MRI, or
PET/CT studies can often differentiate benign and malignant
lesions.
A.I. Brenner et al
Situations in Which SPECT Is Difficult
to Perform or Precluded for Technical Issues
In certain situations, a 15- to 30-minute SPECT acquisition is
not possible. Examples include nonsedated pediatric patients
or patients for whom prolonged sedation is impractical. Because even small differences in position can cause large
changes in bone images in the pediatric age group, these
patients may be held in position by experienced staff, especially when evaluating the extremities. Some popular gamma
cameras with fixed gantries make it nearly impossible, technically, to acquire SPECT images of the wrists and hands. In
these situations, planar images suffice to yield diagnostic information.
Clinical Situations in
Which the Area of Interest Is Undefined
In these cases, whole-body planar images are performed. If an
abnormality is detected, then SPECT acquisitions targeting
that area may be performed. Whole-body planar imaging can
be useful in patients with known malignancy to detect or
exclude bone metastases or in patients with suspected malignancy because of elevated serum prostatic-specific antigen or
calcium. They can also often detect characteristic findings
and anatomic distribution of Pagets disease in patients with
elevated serum alkaline phosphatase, assess disease activity,
and assess response to therapy.39 In patients with fever, bacteremia, leukocytosis, elevated sedimentation rate/C-reactive
protein (CPR), or subacute endocarditis, whole-body images
may be useful to detect a source of seeding or osteomyelitis.
In pediatric patients presenting with a limp, failure to bear
weight, or lower extremity pain, because the painful site may
represent referred pain, whole-body planar images from sacroiliac joints to feet are usually acquired, often followed by
SPECT.
Reflex Sympathetic Dystrophy (RSD)
or Complex Regional Pain Syndrome
RSD represents an abnormality of the sympathetic nervous
system40 that typically occurs after an inciting event. In these
patients, planar 3-phase bone images often suffice to demonstrate the characteristic findings of RSD diffuse generalized
increased uptake of bone agent throughout all the bones of
one extremity caused by increased generalized blood flow.
Diffusely increased juxtaarticular activity in affected joints of
the symptomatic extremity is also a sensitive indicator of
RSD.9 Planar positive predictive value has been reported as
67%-95%; negative predictive value as 61%-100%,41 sensitivity as 60%-96%, and as specificity 92%.30,42
Evaluation of the Significance of a
Bone Lesion on Radiograph, CT, or MRI
If it is unclear whether a radiographic abnormality represents
a benign or a malignant process, planar whole-body imaging
is of central importance to assess for other involved sites.
Then, regional and SPECT imaging focused on the abnormal
area are usually performed to help characterize the finding as
likely benign, suspicious, or indeterminate by bone scintigraphy. Direct comparison of the bone scan with CT or MRI in
matching coronal, sagittal, and transaxial images is often
Bone scanning
helpful. In general, if the radiographic abnormality corresponds with a normal area on bone scintigraphy, it is very
likely benign. If there is increased bone agent uptake, the
index lesion may be benign or malignant.
Osteomyelitis
Osteomyelitis causes bony destruction that is followed by a
robust osteoblastic healing response; therefore, bone imaging
can detect osteomyelitis before radiographic findings are evident. In the clinical setting of bacteremia, subacute endocarditis, or fever of unknown origin, planar whole-body imaging
represents the principal imaging approach. If the clinical
findings point to a specific location, 3-phase bone imaging is
usually performed, which may include whole-body format
images, complimented by SPECT over the region of interest
or abnormality pinpointed on planar imaging.
MRI is a valuable tool for diagnosis of osteomyelitis when
the site of infection is clinically evident. However, when the
site of infection is unclear, choosing a site for MRI study is
difficult. The authors of recent studies have also demonstrated the usefulness of FDG-PET in the diagnosis of osteomyelitis. Stumpe et al.43,44 reported sensitivity of 100% and
specificity of 83-99%. Nevertheless, because data on the
clinical role of FDG PET in assessment of infection and inflammation are sparse, FDG-PET may have limited value in
diagnosis of uncomplicated cases of acute osteomyelitis compared with the combination of physical examination, evaluation of biochemical markers, and 3-phase 99mTc bone imaging or MRI.25
Pediatric Osteomyelitis
Causes of osteomyelitis include hematogenous spread, direct
inoculation, and local extension from contiguous infection.
Although the hematogenous route of infection is the most
common route of spread in pediatric osteomyelitis, it accounts for only 20% of cases in adult osteomyelitis.45 The
characteristic finding of osteomyelitis on 99m-Tc scintigraphy is increased activity in bone on all 3 phases (Fig. 2).46,47
Although 3-phase imaging is preferred, patient cooperation
and sedation are not always possible for all phases. Delayed
bone images are the most definitive phase, because there is no
osteomyelitis unless the delayed images are abnormal, even
in the setting of increased blood flow and/or blood pool activity.48,49 There is typically a generalized pattern of diffuse
bone agent uptake related to hyperemia noted in the normal
bones of the extremity involved with focal osteomyelitis. This
should be expected and not mistaken for multifocal osteomyelitis or septic arthritis a negative bone scan can often relieve concern for significant pathology.50 In addition to diagnosing or excluding osteomyelitis, bone images can help
detect occult fractures or toddlers fractures,51 which may
represent the true source of the patients symptoms (Fig. 3).
The metaphyses of long bones have rich blood supply and
relatively sluggish flow and can serve as a medium for implantation and proliferation of bacteria.9,52 In infants, metaphyseal vessels penetrate the epiphysis, allowing passage of
infection through the epiphysis into the joint space.53 Thus,
osteomyelitis of the proximal femur is usually associated with
15
septic arthritis in children younger than 1 year of age.54 Pressure from joint fluid can compromise the femoral head
growth center and may represent a surgical emergency.51,55
When children are older than 2, few vessels cross the epiphyseal plate, protecting the epiphysis and joint from infection
and therefore the most common site of osteomyelitis is the
metaphysis. Thus, osteomyelitis usually involves only 1
bone, even in the setting of septic arthritis. Multifocal osteomyelitis rarely occurs, however may be seen in neonates and
immunocompromised patients.
Metabolic Bone Disease,
Such as Hyperparathyroidism
Planar whole-body bone images are necessary, often followed
by regional planar images and perhaps complementary
SPECT imaging. Patients with hyperparathyroidism typically
present with diffusely increased activity throughout the skeleton with faint or no visualization of the kidneys (absent
kidney sign), commonly referred to as a superscan. There is
usually more uptake in the skull and distal extremities in
hyperparathyroidism as compared to diffuse metastatic disease.56 Other findings may also include detection of brown
tumors or metastatic calcifications within the thyroid gland,
lungs or stomach.
Rhabdomyolysis and Other Soft-Tissue Abnormalities
Planar whole body and regional bone images, complemented
by SPECT imaging, are useful for detection and evaluation of
heterotopic ossification or myositis ossificans and help determine if this is an ongoing process (Fig. 4).57
In myoglobinuria, with or without a known history of
significant trauma, detection of soft tissue bony uptake in
sites of rhabdomyolysis may help evaluate the severity and
etiology of the pathologic process.58 Similarly, in electrocution injury, planar bone imaging can often determine the
extent of soft tissue injury.59,60 In dermatomyositis and polymyositis, whole-body imaging may allow detection of many
of the soft-tissue lesions, which are often bone agent avid
(Fig. 5).61,62 Planar imaging can often show evidence of bursitis, which may be the true cause of patient complaints in the
absence of other bony abnormalities.
Bone agents may be taken up in soft-tissue tumors, pleural
effusions, ascites, liver, or stroke. Proposed mechanisms of
uptake include local tissue necrosis; damage causing increased tissue calcium deposition; hyperemia; altered capillary permeability; adsorption onto soft tissue calcium; and
binding to enzyme receptors or denatured proteins.63
Child Abuse
Whole-body planar imaging is often complementary to other
radiographic studies in cases of suspected child abuse. Although older fractures may not be seen on bone scan, the
finding of fractures of different ages older fractures on skeletal survey and more recent fractures on bone scan may be
diagnostic. Bone imaging is particularly useful in diagnosing
rib fractures in infants, which are nearly always related to
abuse.64,65 Planar scintigraphy may detect 25-50% more areas of involvement than radiography, and may allow recognition of periosteal trauma (Fig. 6).51,66
16
A.I. Brenner et al
Figure 2 A 6-year-old boy who presented with painless right-sided limp for 3 days, fever, elevated ESR, and a normal
white blood cell count. The radiograph on the same date as the bone scan was normal. (A) Sequential anterior flow
images show increased flow to the right proximal femur. (B) Blood pool images show increased blood pool activity in
the same area. (C) Delayed images also show increased activity in the right proximal femur consistent with acute
osteomyelitis.
Bone scanning
17
Figure 3 Toddlers fracture in an 18-month-old boy who presented with inability to bear weight, swelling, and point
tenderness over the right tibia. An initial radiograph was interpreted as normal. A bone scan was then performed which
demonstrated uncharacteristic increased activity extending beyond the metaphysis. Because of this finding and the
patients age, a differential, including toddlers fracture was suggested. A repeat radiograph with oblique positioning
demonstrated a toddlers fracture.
18
A.I. Brenner et al
Figure 4 (A) These images depict a 76-year-old male with a history of bilateral hip replacements 24 years earlier and a
bilateral revision 4 years ago. Note the active bone agent uptake within heterotopic bone superiorlateral to the
prostheses bilaterally consistent with an active process. (B) This image is a plain radiograph depicting the heterotopic
bone formation corresponding to findings on bone scan.
Figure 5 These images depict a 15-year-old boy diagnosed with dermatomyositis at age 6. Note multiple sites of
soft-tissue uptake corresponding to clinically evident abnormalities.
Bone scanning
19
tients, with no plan for reoperation, and elevation of only ESR
or only CRP levels, should be reevaluated clinically within
three months.
Figure 7 A 57-year-old woman with a history of lung cancer metastatic to the brain (after left craniotomy). Note the
increased uptake along the periosteal margins of the long bones characteristic for pulmonary hypertrophic osteoarthropathy.
A.I. Brenner et al
20
Figure 8 (A) These images depict a 39-year-man with new-onset right hip pain, pain in the left hip for a few years, pain
in the left shoulder for 3 months, and pain in the right shoulder for 2 years. Note the absence of activity in the right
femoral head consistent with early avascular necrosis. There is a combination of cold and hot areas in both shoulders
and left femoral head consistent with revascularization and reossification phase of avascular necrosis. (B) A 25-year-old
woman with right hip pain for 1 month and the left hip for 3 years. Note the combination of a cold area with increased
uptake in bilateral hips characteristic of avascular necrosis.
Osteoporotic patients are at high risk for osteoporotic insufficiency fractures. Patients with back pain often are found
to have compression fractures on radiographs, CT or MR.
Sometimes these patients present with hip or groin pain and
have radiographic findings consistent with fracture of indeterminate age. Bone scans are helpful in determining if the
fracture is recent and explains the patients symptoms. Therefore, if the bone scan is positive, the fracture is likely recent,
and if negative, it is probably not recent.76
Spondylolysis represents stress related microfractures induced by trauma that may be too subtle to be detected radiographically.77 Bone SPECT is better in detection of spondylolysis
than conventional radiography and often demonstrates abnormalities not evident on planar bone scintigraphy,15,78,79 aiding in
patient management. Bone SPECT may detect abnormalities not
recognizable on other radiographic modalities in 25%-40% of
patients.80
Predicting Growth Arrest
Growth arrest is most commonly related to post-traumatic
premature closure of the physeal plate. Injury involving
the growth plate may disrupt epiphyseal vessels. Planar
images comparing the affected bone to the contralateral
Bone scanning
Figure 9 An 84-year-old man with low back and right hip pain after
left arthroplasty 4 months earlier. (A) Note the increased uptake
across the sacrum in an H pattern consistent with recent sacral
compression fracture with shearing forces on the sacroiliac joints.
(B) CT image shows osteoporosis and did not demonstrate this
recent fracture.
21
pool activity.82 Although SPECT imaging is complementary, diagnostic findings are usually evident on planar images.
Avulsion injuries are often not readily apparent on radiography. Planar bone imaging often shows increased
blood pool and delayed bone agent uptake along the superficial cortical bone at the site of avulsion (Fig. 11).9 In
plantar fasciitis and Achilles tendonitis,82 3-phase bone
images often complemented by SPECT imaging may play
an important role in localizing the inflammatory focus.
Stress fractures, microfractures and periosteal trauma
are overuse injuries72 that typically occur in normal bones
in response to abnormal stresses,7 such as unusual or repeated physical activity. This initiates bone remodeling
focally, ultimately leading to pain.82 They are difficult to
diagnose radiographically and at presentation, plain radiographs are often normal. There is a wide spectrum of objective findings on scintigraphy, based on the extent of
injury. Scintigraphic classification of stress fracture has
been graded based on the degree of injury, ranging from
mild increased uptake in the cortex to marked increased
uptake across the width of the bone (complete fracture).
Focal, thicker areas of uptake can usually be interpreted as
a stress fracture, particularly if fusiform or diamond
shaped.83 Some authors maintain that stress fractures are
more likely to have associated hyperemia on three-phase
bone imaging, particularly on blood pool images.56 However, the diagnosis always requires characteristic abnormalities on delayed definitive bone images (Fig. 12).
Linearly increased activity along the periosteal surface
of bone is usually diagnostic of shin splint or significant
periosteal trauma.84,85 Whole-body format imaging is ideally performed, allowing better evaluation of symmetry
and relative intensity of bone agent uptake, followed by
regional images in several positions. If fibular involvement
is suspected, anterior and posterior images in the pigeon
toe position or lateral and medial views will separate the
tibia and fibula. SPECT imaging is particularly helpful
when inspecting three-dimensional reconstructions in
cinematic display, comparing relative intensities in each
extremity and in assessing the thickness and shape of abnormal uptake.
A.I. Brenner et al
22
Figure 10 A 14-year-old boy who had a Salter Type II fracture (metaphyseal fracture extending to the physis) of the distal
right femur 1 year before imaging. Note the absence of the normal epiphyseal plate activity in the distal right femur
suggesting growth arrest.
case, if the CT will improve upon the sensitivity, specificity and diagnostic accuracy of bone imaging alone. If so,
then CT acquisition over a limited area (decreasing Dose
Length Product and absorbed dose) may occasionally be
valuable.86
Figure 11 A 13-year-old female dancer with right hip pain. Note the increased uptake in the right ischium consistent with an avulsion fracture.
Bone scanning
23
Figure 12 A 14-year-old girl with right leg pain. Note the fusiform increased uptake in the distal right tibia consistent
with a stress fracture.
Value-Added Nuclear
Medicine: Nuclear Medicine
Physician/Radiologist as a Physician
Close communication with referring physicians is integral in
nuclear medicine. Planar bone imaging is a useful tool; however, it is most accurate when interpreted with the appropriate history. We need to speak the language of our referring
physicians. Knowing the history and specific clinical question assures that imaging is tailored to the individual patients
clinical need. When the clinical question is not clear, we
should consult with referring physicians to understand the
clinical context. Policies and procedures should assure that
all necessary clinical information is available. Within the
electronic medical record environment, we are revising our
electronic ordering system to better capture history appropriate to the study. Technologists and schedulers should ask
patients pertinent questions before imaging, such as sites of
pain, dates and details of orthopedic surgery or recent trauma
and reports of complementary imaging studies. An anatomic
drawing marking the location of pain, swelling or ulcer is
helpful in correlating bone scan findings to involved sites
(Fig. 13).
A.I. Brenner et al
24
Figure 13 This anatomic drawing is used by technologists and physicians to mark the location of pain, swelling, or ulcer
and is helpful in correlating bone scan findings to involved sites.
Conclusions
The power of bone imaging lies in the physiological uptake
and pathophysiologic behavior of 99 m-Tc diphosphonates.
Its clinical utility, sensitivity and specificity was established
based on planar imaging data. Planar bone imaging data are
often sufficient for diagnosis and may be enhanced by
SPECT. New imaging modalities, including 18F-FDG-PET,
CT and MR are complementary to 99 -m-Tc bone imaging.
18F-FDG-PET and 99m-Tc bone imaging reflect different biological processes (FDG uptake by tumor cells; MDP uptake
by osteoblastic activity). We can lower radiation doses by
prescribing lower injected doses and minimizing unnecessary additional imaging. We are physicians and should all
adopt a value-added approach to image interpretation.
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