Radionuclide imaging after skeletal interventional procedures

R a d i o n u c l i d e Imaging After Skeletal Interventional Procedures Christopher J. Palestro Although nuclear medicine is often used as an adjunct to planning skeletal therapeutic interventions, its role in the assessment of these various interventional procedures, after the fact, is equally important. Skeletal therapeutic interventions studied with radionuclide imaging include bone grafts, the postoperative spine, and joint replacements. Vascularized bone grafts allow the successful reconstruction of large bone gaps. Early detection of vascular compromise permits prompt reevaluation of the vascular anastomosis so that potentially reversible causes of ischemia can be corrected. Radionuclide bone scintigraphy is a simple noninvasive method to evaluate the anastomotic patency of these grafts. Scintigraphically, vascular patency is characterized by normal or diffusely increased tracer uptake throughout the graft, whereas failure of the graft presents as photopenia. Bone scintigraphy, especially single photon emission computed tomography (SPECT), is of considerable value in the work-up of patients with persistent back pain after spinal surgery. Postoperatively, spinal fusion is characterized by diffusely increased uptake of radiotracer in the fused area. In contrast, focally increased uptake has been shown to be related to bony nonunion or pseudoarthro-

ses. In patients w h o have undergone laminectomy, SPECT bone scintigraphy can localize the level of maximum instability and vertebral stress. The radionuclide evaluation of joint replacement complications, especially of hip and knee prostheses, has been extensively studied for nearly 2 decades. Bone scintigraphy is probably most useful when the images are normal. Although periprosthetic sites of increased uptake may be indicative of postoperative problems such as loosening or infection, they may also merely reflect postoperative changes. Dual tracer studies, focusing primarily on the diagnosis of the infected joint replacement, have consequently become the norm. Bone-gallium scintigraphy was the earliest dual tracer modality used, with an accuracy of 60% to 80%. The current radionuclide study of choice for diagnosing the infected prosthesis is labeled leukocyte-marrow imaging. Both leukocytes and colloid tracers accumulate in marrow, whereas only leukocytes accumulate in infection. This technique facilitates the discrimination of labeled leukocyte uptake in aberrant, but not abnormal, marrow from uptake in infection. The reported accuracy of this technique consistently exceeds 90%. Copyright 9 1995 by W.B. Saunders Company

HE TECHNOLOGICAL advances that

permit the successful reconstruction of large bone gaps. Graft viability is important because, in its absence, bony union may not occur and nonviable segments are subject to fracture. Radiographic imaging provides detailed anatomy of the reconstructed bone. Although ischemic changes may be manifest as radiolucencies, this is a late indication. Therefore, plain films contribute little to the early assessment of graft viability. Although angiography can detail the microvascular surgery, it cannot show the microcirculation that determines viability. Moreover, the invasiveness of the technique precludes its routine use. Radionuclide bone scintigraphy, in contrast, is a simple noninvasive procedure that allows an early assessment of the anastomotic patency. 1,2 Perhaps no vascularized bone grafts have been more extensively studied than those used in mandibular reconstruction. Over the past 15

T have facilitated the removal and/or replacement of diseased or damaged components of the human body have led to an improved quality of life for untold numbers of people. Unfortunately, these procedures are accompanied by their own complications, the detection of which is often an arduous task. The anatomical distortion that may result from various therapeutic interventions, as well as the composition of synthetic materials, such as orthopedic hardware, used in these procedures, can render the interpretation of high-resolution imaging modalities such as computed tomography (CT) and magnetic resonance imaging difficult, if not impossible. In contrast, radionuclide imaging which is dependent on physiological, as opposed to anatomic, parameters can be most rewarding. Although nuclear medicine has often been used as an adjunct to planning therapeutic intervention in the skeletal system, its role in the assessment of these various interventional procedures, after the fact, is equally important. BONE GRAFTS

Vascularized bone grafts, using the iliac crest, rib, and fibula with their intrinsic blood supply, Seminars in Nuclear Medicine, Vol XXV, No 1 (January),1995: pp 3-14

From the Division of Nuclear Medicine, Long Island Jewish Medical Center, New Hyde Park, NY. Address reprint requests to Christopher J. Palestro, MD, Division of Nuclear Medicine, Long Island Jewish Medical Center, 270-05 76th Ave, New Hyde Park, N Y ll040. Copyright 9 1995 by W.B. Saunders Company 0001-2998/95/2501-0001/$05. 00/0 3

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Fig 2. Irregularly increased uptake in the left anterior lilac crest is the donor site of an lilac crest bone graft, not a pathologic process.

Fig 1. (A) Anterior bone image shows diffusely increased uptake throughout a viable right mandibular vascularized Uiac crest bone graft. (B) There is a sharply defined photopenic defect in the anterior aspect of a right mandibular bone graft, consistent with graft nonviability. Focally increased uptake to just to the left of the midline is the osteotomy site.

years these grafts, especially iliac crest grafts, have been used with increasing frequency for the purposes of mandibular reconstruction. The success of this technique has resulted in expansion of its goals to include functional mandibular reconstruction with a fixed osteo-dental prosthesis. It is of the utmost importance to

Fig 3. (A) Posterior planar image of a 4g-year-old woman with postoperative back pain after L5-$1 laminectomies shows increased activity at the L5-$1 level on the right. (B) Transaxial SPECT image localizes the abnormality to the posterior elements, consistent with articular facet stress.

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Fig 4, Patterns of periprosthetic uptake in total hip replacements. (A) Normal periprosthetic uptake in a patient with bilateral total hip replacements. Activity is indistinguishable from surrounding, nonarticular bone. (B) Focal uptake at the medial aspect of the tip of a painful left cemented total hip replacement, consistent with loosening. (C) Diffuse periprosthetic uptake around the entire femoral component of this left hip replacement is consistent with infection.

confirm vascular patency after the graft procedure, as vascular occlusion may result in flap necrosis, poor would healing, and, ultimately, failure of the graft. Early detection of vascular compromise permits prompt reexamination of the vascular anastomosis so that potentially reversible causes of ischemia, such as a hematoma or vascular kink, can be corrected. Metabolically active revascularized bone grafts typically show normal or diffusely increased tracer uptake throughout the grafted bone with focally increased uptake at the osteotomy sites. However, the failed graft does not concentrate tracer and presents as a photopenic defect 3 (Fig 1). It is imperative to be cognizant of the fact that a positive scintigraphic study is useful for predicting vascular patency and osseous metabolic activity only when performed within 1

week of surgery; scans performed later may be incorrectly interpreted as showing graft viability because of uptake in new bone deposition on a nonviable graft, so-called periosteal creep. Fig et aP studied 15 patients who had undergone mandibular reconstruction with vascularized free-flap osseocutaneous scapular or iliac crest grafts. They compared the results of early (within 8 days after surgery) 99mTc MDP bone scintigraphy with long-term clinical follow-up in these patients. They also compared single photon emission computed tomography (SPECT) and planar imaging in this group. These investigators reported that the results of SPECT and planar imaging were in agreement in 13 of the 15 studies. Both studies showed increased tracer uptake (ie, graft viability) in 11 cases. Graft outcome was successful in 10 cases. In 1 patient,

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Fig 5. Combined bone-gallium imaging is often used to assess the presence of complicating osteomyelitis including, but not limited to, joint replacements. The principles of interpretation are the same, (A) Intense uptake involving L3 and L4 is obvious on this bone scan. (B) However, the gallium image is negative and the combined study is therefore negative for osteomyelitis. (C) Bone images show moderately increased uptake in L5, (D) The spatial distribution of uptake on the gallium scan is similar (congruent) to that on the bone scan. The intensity of uptake on the gallium scan exceeds (relatively) the intensity of uptake on the bone scan; therefore, the combined study is positive for osteomyelitis. (E) Bone and (F) gallium images show increased uptake in 3 upper right posterior ribs and a single right costovertebral junction. The spatial distribution and intensity of uptake on both studies are congruent, and the combined study is equivocal for infection.

repeat imaging at 10 days after surgery showed a photopenic defect on both planar and SPECT imaging in a patient who developed vascular pedicle thrombosis. In 2 patients with failed grafts, both planar and SPECT images showed

photopenic defects in the graft. In the remaining 2 patients, results of planar and SPECT imaging were discordant. Although both patients had viable grafts, planar images showed changes suggestive of vascular compromise; in

RADIONUCLIDE IMAGING IN SKELETAL INTERVENTION

Fig 5.

contrast, SPECT images showed uniform uptake throughout the bony graft. Lukash et al4 studied nine patients who had undergone mandibular reconstruction with vascularized iliac crest bone grafts. All patients underwent bone SPECT imaging 48 hours after surgery, and eight were studied again 1 year later. Eight of the nine showed increased uptake on the 48-hour images, and all eight grafts were viable. One year after surgery, seven of the eight original positive scans continued to show increased tracer uptake. The one photopenic scan was observed in a patient who had undergone radiotherapy after reconstruction. Graft biopsy confirmed obliterative endarteritis secondary to radiotherapy. Although uptake of tracer is equated with graft viability, this seemingly paradoxical finding has also been observed in patients with osteoradionecrosis, a serious complication of radiotherapy for head and neck tumors .5 Consequently, the presence of increased tracer uptake in patients who have undergone radiotherapy after mandibular reconstruction cannot automatically be equated with graft viability and more invasive procedures including graft biopsy may be necessary. The assessment of bone graft viability by means of radionuclide bone scintigraphy has not been limited to vascularized bone autografts. Bone scintigraphy has also been found to

{Cont'd).

be useful in assessing the results of bone allografts, grafts in which blood perfusion is not maintained as part of the procedure. Ramsay et al 6 used bone scintigraphy to assess nasal bone graft viability in 20 patients who had undergone augmentation rhinoplasty. Two (10%) of the 20 grafts failed, and both showed decreased tracer uptake on bone scintigraphy. In this series, the investigators found that neither three-phase bone scintigraphy nor SPECT offered additional information not available on routine planar images. Bone scintigraphy has also been reported to be useful in the assessment of acetabular and tibial bone grafts. 7,s Despite its acknowledged role in the evaluation of graft viability, a major limitation to 99mTc bone scintigraphy is its nonspecificity. Although increased uptake is equated with graft viability, it may also be caused by periosteal creep, postoperative changes, and osteoradionecrosis. There are some data to suggest that, because postoperative hyperemia and periosteal creep should not affect the bone marrow, marrow scintigraphy with technetium-labeled colloids may be useful for assessing graft viability. 9 If validated, this is a very intriguing concept and could greatly expand the role of radionuclide marrow imaging, a technique that, in this investigator's opinion, is currently underused. However, there are two potential problems. The first problem is that it is likely that the technique

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would only be useful when the bones used for grafting contain hematopoietically active marrow. The second problem is that, even when such marrow containing bones are used, because the distribution of marrow is so variable, a baseline, preoperative marrow scan would be obligatory. Finally, it is not unusual to perform wholebody bone scintigraphy on patients who have previously undergone autologous bone grafting. Careful attention to the patient's history is necessary to prevent the confusion of the graft donor site with a pathological process (Fig 2). THE SPINE

Lumbar spine surgery for relief of low-back pain, one of the most frequently performed of all surgical procedures, has a success rate of 80% to 90%. Those patients who continue to have low-back pain postoperatively are classified as having failed back syndrome. Bone scintigraphy, especially using SPECT, has been shown to be extremely useful in this population. Typically, after spinal fusion there is uniformly increased uptake of radiotracer in the fused area, probably because of widespread new bone formation. In contrast to the diffuse uptake pattern associated with a normally healing fusion, areas of focally increased uptake are associated with sites of osseous nonunion or pseudarthroses. Slizofski et al 1~ reviewed the results of bone scintigraphy in 26 patients with a history of spinal fusion for low-back pain. All patients had undergone surgery at least 6 months before imaging, and all had both planar and SPECT studies. Fifteen of the 26 were symptomatic at the time of imaging. Among the 15 symptomatic patients, when sites of focally increased uptake were considered positive for pseudarthrosis, the sensitivity and specificity of the radionuclide procedure were 78% and 83%, respectively, superior to the sensitivity and specificity for flexion-extension radiographs in this population, which were 43% and 50%, respectively. Six of the 11 asymptomatic patients also showed areas of focal uptake on bone scintigraphy, and these areas were thought to represent painless pseudarthroses. Not surprisingly, be-

cause of the complex anatomy inherent in the spinal column, the investigators found that, in 54% of the patients, SPECT contributed information not evident on planar images. These investigators concluded that SPECT bone imaging is a sensitive screening device to detect lumbar pseudoarthrosis. Recurrent back pain after spinal surgery may be caused by a condition other than that which produced the initial preoperative discomfort. Spinal instability after laminectomy, especially multilevel laminectomy, is a well-known complication of this type of procedure. The end result of this instability is increased stress on the articular facets, with resultant slippage of one vertebral body on another. Lusins et a111 reviewed the results of SPECT bone scintigraphy in 25 patients with persistent low-back pain after lumbar spine surgery. Eleven patients in this group had undergone laminectomy confined to only one level. Only 2 (18%) of these patients had abnormal SPECT studies; both showed focally increased uptake in the articular facets at the level of the laminectomy. Eight patients had undergone multilevel laminectomies and 6 (75%) had abnormal studies with the increased uptake involving primarily the facets (Fig 3). The remaining 6 patients had undergone both laminectomy and spinal fusion and all had abnormal SPECT studies. Two had abnormal uptake in the fusion mass consistent with pseudarthroses, and the other 4 showed increased uptake in the articular facets. Three of the four also showed increased vertebral body uptake of varying degrees. The investigators concluded that SPECT imaging is most useful in those patients in which there is the greatest probability for articular facet stress. They also suggested that SPECT bone imaging can more precisely locate the level of involvement than either conventional radiographs or CT. Increased sacroiliac joint uptake after spinal surgery has also been described. In one series, 15 of 43 patients with increased sacroiliac joint uptake had a history of prior lumbar laminectomy or spinal fusion. This increased uptake was thought to be the result of postoperative alterations in spinal mechanics, resulting in

RADIONUCLIDE IMAGING IN SKELETAL INTERVENTION

mechanical overloading and accelerated degenerative changes in adjacent joints. 12 THE PAINFUL JOINT REPLACEMENT

Although synthetic replacements exist for numerous joints throughout the body, the two most frequently performed arthroplasties involve the hip and the knee, with nearly a quarter

million of each of these procedures performed annually in the United States. 13,14For the most part, the outcome of hip and knee arthroplasty is extremely satisfactory in terms of pain relief and restoration of function. Postoperative complications do occur and include fracture, arthritis, and loosening with or without infection. Radionuclide evaluation of the painful joint

Fig 6. (A) Whole-body 1111n-labeled leukocyte image shows increased activity in the proximal left tibia, not a typical location for functioning bone marrow. (Note marrow expansion into both distal femurs.) (B) Static image of the same region. (C) Bone marrow/image using 99mTc sulfur colloid, performed about 90 minutes later, confirms that this is marrow, not infection.

10

Fig 7. Whole-body 111In-labeled leukocyte (left) and 99rnTcsulfur-colloid marrow (right) images of patient with osteomyelitis of the left lateral malleolus. The distribution of the two radiotracers is virtually identical, except for the left ankle, where a focus of activity is clearly seen on the leukocyte study. The marrow scan is devoid of activity in this region.

replacement has been extensively studied over the past 20 years or so, and is considered an important diagnostic tool in the work-up of this condition. Not surprisingly, the earliest radionu-

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clide evaluations of joint arthroplasties were performed with 99mTc-MI)P bone scintigraphy. Initial reports indicated that the accuracy of the technique exceeded 85%. 15,16 These results reflected the sensitivity of bone scintigraphy for detecting complications in general; however, they did not address the specificity of the technique. In the case of hip replacements, attempts at improving the specificity of bone scintigraphy have focused on patterns of periprosthetic uptake. Williamson et a117found that focal periprosthetic uptake was associated with prosthetic loosening, whereas diffuse periprosthetic uptake was more likely to be associated with infection (Fig 4). Mountford et aP 8 also found that diffuse periprosthetic uptake was highly specific but not sensitive for infection. In contrast, Williams et al a9 found that the diffuse pattern was present in both infected and uninfected hip replacements and therefore, was not specific for infection. Aliabadi et al 2~ reported that bone scintigraphy was not useful for separating infected from uninfected prostheses. Complicating the inherent nonspecificity of bone scintigraphy is the normal musculoskeletal stress that occurs as a result of the implantation of an artificial joint. For approximately 1 year after the implantation of a total hip replacement, periprosthetic uptake is very variable; beyond 1 year, most asymptomatic individuals with a cemented total hip replacement will have a normal scan, ie, periprosthetic uptake indistinguishable from surrounding nonarticular bone (Fig 4A). However, 10% of asymptomatic patients will still have some degree of periprosthetic uptake beyond this time. 2~ Periprosthetic uptake around the cementless or porous, coated

Fig 8. 99mTcsulfur colloid (left) and 11~lnlabeled leukocyte images (right) demonstrate spatially congruent activity around a left total hip replacement. Uptake in both studies is equally intense around the trochanters and at the tip of the femoral component. The combined study is negative for infection.

RADIONUCLIDE IMAGING IN SKELETAL INTERVENTION

hip replacement, more than 1 year after placement, is even more prevalent and the patterns are more variable than those encountered with the cemented variety, further complicating study interpretation.22, 23 Assessment of total knee replacements with bone scintigraphy is also extremely difficult because 89% of tibial components and 63% of femoral components, in asymptomatic individuals, show increased periprosthetic activity more than 1 year after implantation. 24 Although it has been suggested that the value of bone scintigraphy in total joint replacement evaluation can be enhanced if patients undergo serial studies, this is simply not practical in the usual clinical environment. Efforts at improving radionuclide diagnosis of postoperative complications of joint replacement, especially infection, have focused on the use of additional radiotracers. The propensity of gallium-67 to accumulate in infection was first recognized more than 2 decades ago, and the role of this radiotracer in the evaluation of the painful joint replacement has been extensively investigated. Reing et a125 described 79 patients who underwent bone and gallium scintigraphy and reported that bone scintigraphy was 100% sensitive, but only 15% specific for diagnosing the infected joint replacement. However, they found that gallium imaging was 95% sensitive and 100% specific for this entity. Rushton et a126 reported similar results. Rosenthall et a127 evaluated bone and gallium imaging in 46 patients with various types of orthopedic hardware, and developed a method for interpreting the two studies together. With some modifications, this method is still widely used for evaluating complicating osteomyelitis. Based on their observations, these investigators concluded that, when the gallium scan was negative, regardless of the bone scan results, infection was excluded with a high degree of certainty. Infection was also unlikely to be present when the spatial distribution of the two tracers was similar or spatially congruent and the intensity of gallium uptake was not greater than that of the bone agent. When the distribution of the two radiotracers was different ie, spatially incongruent, or when the intensity of

gallium uptake exceeded that of the bone agent, infection was likely to be present (Fig 5). Williams et a119 also found that lack of gallium uptake ruled strongly against infection, and that incongruent images were very specific for infection. In their series, although specific (88%)

Fig 9. 111In-labeled leukocyte (A) and ~mTc-sulfur-colloid marrow (B) images of a left total hip replacement. The distribution of the two radiotracers is incongruent; ie, there is increased periprosthetic uptake of labeled leukocytes, which is only partially matched on the marrow study, and the combined study is positive for infection.

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for infection, incongruity was not very sensitive (50%). Schauwecker et al, 28 in a review of complicating osteomyelitis, found that, when bone-gallium images were positive (or negative) for infection, they were very accurate; however, more than 70% of the patients they evaluated with the combined technique had inconclusive studies. Merkel et a129 reported that bonegallium imaging had an accuracy of 67% for diagnosing infected joint replacements in an animal model. In a subsequent review of patients with painful prostheses, these investigators reported similar results. 3~ Although offering more information than bone scintigraphy alone, bone-gallium imaging, with an accuracy ranging between 60% and 80%, was still less than ideal. Labeled-leukocyte imaging, at least in theory, would appear to be an ideal radiotracer for diagnosing the infected joint replacement, considering the fact that for the most part, labeled leukocytes do not accumulate at sites of increased bone-mineral turnover in the absence of infection. However, the results reported have been very inconsistent, with the sensitivity ranging between 50% and 100% and the specificity between 23% and 100%. 31,32 It is evident that, based on these extremely variable results, labeled leukocyte imaging, at least as the only radionuclide procedure, is not useful for diagnosing the infected joint replacement. Improved diagnostic accuracy has been achieved with combined leukocyte-bone scintigraphy and leukocyte-marrow scintigraphy. Wukich et a133 reported that the sensitivity and specificity of labeled leukocyte imaging for diagnosing infected joint replacements were 100% and 45%, respectively. When interpreted together with bone scintigraphy, using criteria similar to those used for bone-gallium imaging, the sensitivity decreased to 85%, whereas the specificity increased to 85%. Johnson et a134 found that the combined technique offered a higher specificity (95% v 50%), and a slightly lower sensitivity (88% v 100%) than labeled leukocyte imaging alone. However, our own results using this technique were less satisfactory. 32We found that the sensitivity and specificity of the combined technique were 67% and 78%, respectively, which was not better than the sensitivity and specificity of labeled leukocyte

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imaging alone (89% and 75%, respectively). Oswald et a122observed that bone and leukocyte images were incongruent in 15% of patients with asymptomatic, porous coated arthroplasties, and raised concerns about the significance of incongruent labeled leukocyte-bone images. Based on the results reported to date, combined leukocyte-marrow imaging is the current radionuclide procedure of choice for diagnosing the infected joint replacement. It must be recalled that labeled leukocytes normally accumulate in the marrow, which in adults is confined to the axial skeleton and proximal 25% to 30% of the humeri and femora. Unfortunately, there is considerable patient-to-patient variability in this normal pattern, making it difficult to distinguish uptake in aberrant marrow from uptake in infection. This undoubtedly explains in large part the inconsistent results obtained when leukocyte imaging is the sole tracer used. The addition of bone scintigraphy enhances the accuracy of the technique somewhat, but labeled-leukocyte uptake reflects marrow conditions, whereas bone-tracer activity reflects bony conditions. In contrast, labeled leukocytes and marrow tracers, such as sulfur colloid, both accumulate in marrow, regardless of its location. However, infection exerts opposite effects on these radiotracers, stimulating uptake of leukocytes while suppressing uptake of marrow tracers. Consequently, leukocyte-marrow images, which are spatially congruent, reflect only marrow activity and are negative for infection. Those images in which there is activity on labeled leukocyte images without corresponding activity on the marrow images are positive for infection (Figs 6 and 7). Numerous publications attest to the consistently excellent results obtained with this technique, with the reported sensitivity and specificity exceeding of 90% 3l'32'35-37(Figs 8 and 9). Although combined-leukocyte marrow imaging may be the current radionuclide method of choice for diagnosing the infected joint replacement, it is still not the ideal method. The ideal nuclear medicine procedure for diagnosing this entity will be a single tracer that is at least as accurate as leukocyte-marrow imaging, easily prepared, and rapidly imaged.

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14 35. Mulamba L'AH, Ferrant A, Leners N, et al: Indium111 leucocyte scanning in the evaluation of painful hip arthroplasty. Acta Orthop Scand 54:695-697, 1983 36. King AD, Peters AM, Stuttle AWJ, et al: Imaging of bone infection with labelled white blood cells: Role of

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contemporaneous bone marrow imaging. Eur J Nucl Med 17:148-151, 1990 37. Seabold JE, Nepola JV, Marsh JL, et al: Postoperative bone marrow alterations: Potential pitfalls in the diagnosis of osteomyelitis with In-Ill-labeled leukocyte scintigraphy. Radiology 180:741-747, 1991