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DOI: 10.1148/radiol.2233011072
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(Radiology 2002;223:758-764.)
© RSNA, 2002

Nuclear Medicine

Osteomyelitis: Diagnosis with 99mTc-labeled Antigranulocyte Antibodies Compared with Diagnosis with 111In-labeled Leukocytes—Initial Experience1

Christopher J. Palestro, MD, Samuel L. Kipper, MD, Frederick L. Weiland, MD, Charito Love, MD and Maria B. Tomas, MD

1 From the Divisions of Nuclear Medicine of Long Island Jewish Medical Center, 270-05 76th Ave, New Hyde Park, NY 11040 (C.J.P., C.L., M.B.T.), Tri-City Medical Center, Oceanside, Calif (S.L.K.), and Sutter-Roseville Medical Center, Roseville, Calif (F.L.W.). From the 1999 RSNA scientific assembly. Received June 19, 2001; revision requested August 10; revision received October 5; accepted November 12. Supported by a grant from Palatin Technologies, Princeton, NJ. Address correspondence to C.J.P. (e-mail: palestro@lij.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To compare a technetium 99m–labeled murine immunoglobulin M monoclonal antigranulocyte antibody that binds to human polymorphonuclear leukocyte CD15 antigens with indium 111 (111In)–labeled leukocytes in the diagnosis of appendicular skeletal osteomyelitis.

MATERIALS AND METHODS: Twenty-four patients suspected of having infected joint replacement (n = 12), diabetic pedal osteomyelitis (n = 8), or long bone osteomyelitis (n = 4) were imaged 5, 30, 60, and 120 minutes after antibody injection. Following injection, one patient experienced moderate joint pain exacerbation that resolved spontaneously. Patients underwent imaging with 111In-labeled leukocytes and three-phase bone imaging. All studies were interpreted alone. Images obtained in antibody and 111In-labeled leukocyte studies were also interpreted with the bone scans. One reader, without knowledge of other study results or final diagnoses, reviewed and interpreted images in a random order. Sensitivity, specificity, and accuracy were calculated for the antibody study at each time point, the 111In-labeled leukocyte study, the three-phase bone scanning procedure, and dual-tracer studies.

RESULTS: There were 11 cases of osteomyelitis. Bone scintigraphy was sensitive (1.0) but nonspecific (0.38). Images obtained in the 120-minute antibody study were sensitive (0.91), moderately specific (0.69), and comparable to those obtained in the 111In-labeled leukocyte study (0.91 sensitivity, 0.62 specificity). When interpreted with bone scans, images obtained in the antibody and 111In-labeled leukocyte studies showed improved sensitivity and specificity (1.0 and 0.85 and 1.0 and 0.77, respectively).

CONCLUSION: Use of the monoclonal antigranulocyte antibody was comparable to the use of 111In-labeled leukocytes in the diagnosis of appendicular skeletal osteomyelitis. The combined results of the monoclonal antibody study and bone scanning were more accurate (0.91) for diagnosing this entity than were the results of any of the other studies.

© RSNA, 2002

Index terms: Bones, infection, 44.21, 45.21, 46.21 • Bones, radionuclide studies, 44.12169, 45.12169, 46.12169 • Indium, radioactive • Monoclonal antibodies, 44.12166, 45.12166, 46.12169


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Nuclear medicine has an important role in the diagnosis of musculoskeletal infection. Although three-phase bone scintigraphy has an accuracy of 90% or greater for the diagnosis of osteomyelitis in otherwise normal bone, the specificity of the test decreases in the setting of preexisting conditions such as fracture, presence of orthopedic hardware, and neuropathic joint disease (1). Efforts to enhance the radionuclide diagnosis of so-called complicating osteomyelitis have focused on the use of gallium and, more recently, radiolabeled leukocyte scintigraphy, which is now considered the radionuclide standard of reference for the diagnosis of osteomyelitis, except in imaging of the spine (2). There are, however, disadvantages to imaging with leukocytes. The procedure is labor intensive and requires in vitro handling of blood products. An in vivo method of labeling leukocytes that would enable the safe, rapid, and accurate diagnosis of osteomyelitis is, therefore, desirable.

The purpose of our preliminary investigation was to evaluate and compare a technetium 99m (99mTc)–labeled antigranulocyte monoclonal antibody (MoAb) (LeuTech; Palatin Technologies, Princeton, NJ) with indium 111 (111In)–labeled leukocytes for diagnosing osteomyelitis of the appendicular skeleton.

A murine monoclonal immunoglobulin M antibody that was originally raised against stage-specific embryonic antigen-1 and is produced by a hybrid hybridoma cell line, RB5, was evaluated. The CD15 antigen on human polymorphonuclear leukocytes corresponds to the stage-specific embryonic antigen-1 present in mice embryos, and specific binding of the anti–stage-specific embryonic antigen-1 antibody to human neutrophils has been demonstrated (3,4). Systemically administered radioactivity concentrates in areas of infection or inflammation where leukocytes have accumulated, and there are data that indicate that the MoAb is useful for imaging infection in humans (3,5–7).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
In all cases, written informed consent was obtained after the nature of this study, which was approved by the institutional review boards, had been fully explained to each patient.

Radiopharmaceutical Preparation
The agent was supplied as a lyophilized sterile formulation in a kit containing 250 µg of antibody. At the time of use, 0.20–0.35 mL of 99mTcO, containing 740–1,480 MBq of 99mTc, was added to the kit, and the mixture was incubated at 37°C for 30 minutes. Following the incubation period, a sufficient volume of 500 mg/mL ascorbic acid injection was added to the vial to bring the final preparation volume to 1 mL. After the addition of ascorbic acid, quality control was performed with instant thin-layer chromatography. The mean radiochemical purity of the injected dose was 98.39% ± 1.15 (SD). Each dose, which was drawn immediately before use, was administered to the patient within 6 hours after reconstitution. Patients were injected with 370–740 MBq (75–125 µg) of the 99mTc-labeled antibody, depending on the time interval between preparation and injection of the MoAb.

Patient Population
Patients eligible for entry into the study included those over 18 years of age who were suspected of having osteomyelitis involving a prosthetic joint, a long bone, or, in the setting of diabetes, underlying a pedal ulcer and who had a peripheral leukocyte count of at least 2,500/mm3. In addition, at least one of the following signs or symptoms was required to be present: localized pain, nonhealing skin ulceration, fever higher than 37.8°C for at least 3 days, leukocyte count in excess of the upper limits of normal, erythrocyte sedimentation rate in excess of the upper limits of normal, radiographic findings suggestive of osteomyelitis, or positive blood or wound cultures. Patients were required to undergo 111In-labeled leukocyte scintigraphy within 24 hours and a bone scanning procedure within 1 week of the investigational study. Final diagnoses were based on clinical, radiologic, and histopathologic and/or microbiologic results. Twenty-four patients (10 men and 14 women between 48 and 91 years of age) were enrolled in this study. Indications were as follows: prosthetic joint infection (n = 12), diabetic pedal osteomyelitis (n = 8), and long bone osteomyelitis (n = 4).

Imaging
MoAb imaging.—Imaging was performed with a large-field-of-view gamma camera equipped with a low-energy, high-resolution, parallel hole collimator. Energy discrimination was accomplished by using a 20% window centered on the 140-keV photopeak of 99mTc. Images were acquired at 5, 30, 60, and 120 minutes after injection of the tracer.

At each time point, 5-minute planar images were acquired with a 256 x 256 x 16 matrix. For long bone and prosthetic joint studies, anterior, posterior, lateral, and medial (when possible) views were obtained. For pedal osteomyelitis cases, dorsal, plantar, medial, and lateral views were obtained. One patient experienced moderate exacerbation of joint pain after MoAb administration. The pain, which was mild in intensity, resolved spontaneously, and the patient was able to complete the protocol. No other adverse events occurred.

Imaging with 111In-labeled leukocytes.—Prior to injection of the radiolabeled antibody, 40 mL of whole blood was withdrawn for labeling with 111In-oxine, according to the method of Thakur et al (8). Eighteen to 24 MBq of 111In-labeled autologous leukocytes were injected immediately after completion of the MoAb protocol, and imaging was performed 18–30 hours later. Images were acquired with a large-field-of-view gamma camera equipped with a medium-energy parallel hole collimator. Energy discrimination was accomplished by using a 15% window centered on the 174-keV photopeak and a 20% window centered on the 247-keV photopeak of 111In. Images were acquired for 10–15 minutes per view with a 128 x 128 x 16 matrix. The views obtained were the same as those obtained in the MoAb study.

Three-phase bone scintigraphy.—Three-phase bone scintigraphy was performed with 740 MBq of 99mTc-methylene diphosphonate. Imaging was performed with a large-field-of-view gamma camera equipped with a low-energy, high-resolution, parallel hole collimator. Energy discrimination was accomplished by using a 20% window centered on the 140-keV photopeak of 99mTc. Dynamic acquisitions were performed with a 64 x 64 x 16 matrix. Static images were acquired with a 256 x 256 x 16 matrix. For the dynamic and blood pool images, the view most appropriate for the region of interest was used. For the delayed images, the views acquired were identical to those obtained in the MoAb and 111In-labeled leukocyte studies.

Image Interpretation
The images obtained in the MoAb and 111In-labeled leukocyte studies were initially interpreted alone. Subsequently, they were interpreted in conjunction with the bone scans. A single reader, who had no knowledge of the results of the other studies or of the final diagnoses, reviewed the studies in a random order and interpreted them according to the criteria in the following paragraphs.

MoAb study.—Images were interpreted as positive for osteomyelitis when focally increased bone activity relative to adjacent bone activity or to activity in the corresponding contralateral region was identified. For positive studies, the time at which the image first showed positivity, as well as any change in intensity over time, was noted.

111In-labeled leukocyte study.—Images were classified as positive for osteomyelitis when focally increased bone activity relative to adjacent bone activity or to activity in the corresponding contralateral region was identified.

Three-phase bone scanning.—Focal hyperperfusion, focal hyperemia, and focally increased uptake in bone on delayed images was interpreted as positive for osteomyelitis.

Dual-tracer studies.—Identical criteria were used when interpreting the bone scans together with either the images obtained in the 120-minute MoAb study or those obtained in the 111In-labeled leukocyte study. In patients suspected of having pedal or long bone osteomyelitis, combined studies were interpreted as positive for osteomyelitis if there was abnormal uptake in the same region in both studies (9–11). For patients with orthopedic hardware, combined studies were classified as positive for osteomyelitis if the distribution of the two tracers was spatially incongruent or if activity on the images obtained in the MoAb or 111In-labeled leukocyte study was hyperintense compared with activity on the bone scans (12,13).

Data Analysis
Sensitivity, specificity, and accuracy were calculated for the MoAb (at each time point), 111In-labeled leukocyte, and both dual-tracer studies.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
There were 11 cases of osteomyelitis among the 24 patients studied, including six infected joint replacements and five cases of diabetic pedal osteomyelitis. Histopathologic confirmation was available in 18 cases, including all 11 cases of osteomyelitis. In six patients, the final diagnosis of "no osteomyelitis" was based on clinical outcome. Three of these six patients responded to treatment for soft-tissue infection, and osteomyelitis was therefore clinically deemed unlikely. Two patients improved with physical therapy alone. In the sixth patient, pain originally attributed to a failed hip replacement was subsequently found to be due to inflammatory bowel disease.

Clinical data and imaging results are summarized in Tables 1 and 2. In the MoAb study, imaging at 120 minutes after the injection was slightly more accurate than was imaging at earlier times. This was due to an increase in sensitivity, with some loss of specificity (Figs 1, 2). In general, once an image showed positivity, changes in intensity over time were modest. False-positive results were associated with soft-tissue infection in cases of suspected pedal osteomyelitis (n = 2), gangrene (n = 1), and an uninfected hip prosthesis (n = 1). The one false-negative result was encountered in a patient with an infected hip replacement.


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  		TABLE 1. Clinical Data

 

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  		TABLE 2. Imaging Results

 


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  		Figure 1. Posterior images obtained in a MoAb study in a 74-year-old woman with an infected right hip replacement demonstrate symmetric activity in both hips on the image obtained at 30 minutes after injection. Increased activity on the right extending into the adjacent soft tissues, which can be appreciated at 60 minutes, is more obvious at 120 minutes (arrows). Intraoperative cultures of tissue taken from the hip joint grew Proteus mirabilis, and results of a bone biopsy were consistent with osteomyelitis.

 


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  		Figure 2. Images obtained in a MoAb study of the feet in a 76-year-old woman with diabetes demonstrate intensely increased uptake (arrow) in the right great toe. The patient subsequently underwent amputation of this digit. The final diagnosis was acute osteomyelitis.

 
Imaging with the 111In-labeled leukocytes was somewhat less accurate than was imaging with the MoAbs at 120 minutes (0.75 vs 0.79). The results of the two studies were concordant in 23 of 24 patients (0.96): There were 10 true-positive results, eight true-negative results, four false-positive results, and one false-negative result. It should be noted that, even in patients in whom the results of both studies were concordant, MoAb and 111In-labeled leukocyte uptake patterns were not necessarily identical. These differences may be related to the intervals between injection of the tracer and acquisition of the images. Images in the MoAb study were acquired within 120 minutes after injection, while images in the 111In-labeled leukocyte study were obtained about 24 hours after injection. Thus, images obtained in the MoAb study may reflect the early phase of leukocyte accumulation, while those obtained in the 111In-labeled leukocyte study may reflect a later phase of leukocyte accumulation (Fig 3).



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  		Figure 3a. (a) Images obtained in the MoAb study demonstrate intense uptake (arrow) around the periphery of the right knee in an 86-year-old man with a painful total knee replacement. Intraoperative cultures grew group ß-hemolytic streptococci. (b) Images obtained in the 111In-labeled leukocyte study (In-WBC) in this patient are also clearly abnormal and show intense uptake within the knee joint extending into the suprapatellar bursa.

 


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  		Figure 3b. (a) Images obtained in the MoAb study demonstrate intense uptake (arrow) around the periphery of the right knee in an 86-year-old man with a painful total knee replacement. Intraoperative cultures grew group ß-hemolytic streptococci. (b) Images obtained in the 111In-labeled leukocyte study (In-WBC) in this patient are also clearly abnormal and show intense uptake within the knee joint extending into the suprapatellar bursa.

 
The results were discordant in one patient: Results of the MoAb study were true-negative and results of the 111In-labeled leukocyte study were false-positive in a patient with an uninfected hip replacement (Fig 4).



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  		Figure 4a. Images obtained in an 83-year-old woman with bilateral hip replacements and left groin and hip pain. (a) The results of the MoAb study were interpreted as normal. Pelvic activity (arrow) was incidentally noted. (b) On images obtained in the 111In-labeled leukocyte study (In-WBC), there is increased activity (arrowheads) in the intertrochanteric region of the left femur; this study was interpreted as positive for infection of the left hip replacement. Abnormal pelvic activity (arrows) is also present on this study. Subsequent work-up revealed that the source of the patient’s pain was related to inflammatory bowel disease, not to a failed hip prosthesis.

 


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  		Figure 4b. Images obtained in an 83-year-old woman with bilateral hip replacements and left groin and hip pain. (a) The results of the MoAb study were interpreted as normal. Pelvic activity (arrow) was incidentally noted. (b) On images obtained in the 111In-labeled leukocyte study (In-WBC), there is increased activity (arrowheads) in the intertrochanteric region of the left femur; this study was interpreted as positive for infection of the left hip replacement. Abnormal pelvic activity (arrows) is also present on this study. Subsequent work-up revealed that the source of the patient’s pain was related to inflammatory bowel disease, not to a failed hip prosthesis.

 
The three-phase bone scanning procedure was the most sensitive (1.0) of the individual tests. The bone scanning procedure was less specific (0.38) than the MoAb study at any time point, the 111In-labeled leukocyte study, the combination of the MoAb study and the bone scanning procedure, and the combination of the 111In-labeled leukocyte study and the bone scanning procedure. When the images obtained in the MoAb study were read in conjunction with the bone scans, which changed the interpretation in three cases, both the sensitivity and specificity of the MoAb study improved. In a patient who had gangrene of the toes and a positive MoAb study, the bone scans were photopenic and the combined study was correctly classified as negative for osteomyelitis (Fig 5). The false-negative and false-positive results in the two patients with hip prostheses were correctly reclassified as true-negative and true-positive when the results of the MoAb study were interpreted together with the bone scans. In two patients suspected of having pedal osteomyelitis who had false-positive MoAb studies, the addition of bone scanning results did not alter the interpretation. In both patients, the bone scan was clearly positive. Bone biopsy and culture results were, however, negative in both cases.



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  		Figure 5. Images obtained in one patient show focally increased activity (arrows), which was interpreted as consistent with pedal osteomyelitis of the left fourth and fifth toes on both the MoAb and the 111In-labeled leukocyte studies (In-WBC). Bone scan images, however, show slightly decreased uptake (arrow) in these digits; the combined studies were interpreted as negative for osteomyelitis. The final diagnosis was gangrene.

 
Similarly, the sensitivity and specificity of the 111In-labeled leukocyte study improved when results from that study were interpreted in conjunction with bone scanning results (Fig 5).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The three-phase bone scanning procedure, as these data illustrate, is sensitive but not specific, and its role in the diagnosis of osteomyelitis, especially in patients with underlying abnormalities of the bone, is usually limited to that of a screening test (1,2,14–18). A positive bone scan, therefore, necessitates the performance of an additional confirmatory procedure. Unless the area of concern involves the spine, labeled leukocyte scintigraphy is the current radionuclide procedure of choice for this purpose (2,19). There are, however, several marked disadvantages to this technique. It is labor intensive, has limited availability, and requires in vitro handling of blood products. When 111In is used as the radiolabel, imaging is routinely performed the day after the injection of labeled cells. Image resolution is poor, and it may not always be possible to separate soft-tissue from bone infection. Normal bone marrow activity can confound image interpretation. Complementary bone or bone marrow imaging may be needed to help clarify the findings. The use of 99mTc as the radiolabel overcomes some, but not all, of these problems. Results, at least in some conditions, may be available within 3–4 hours after injection, and image quality is, of course, superior to that obtained with 111In. Bone or bone marrow imaging, especially in cases of suspected prosthetic joint infection, may still be necessary; this introduces its own logistical problems. Perhaps most important, however, the use of 99mTc does not obviate what is currently the single greatest impediment to imaging with leukocytes: the need to perform the labeling in vitro. A method comparable in accuracy to, but without the disadvantages of, in vitro labeled leukocyte imaging would be a major improvement over current methods.

The results obtained with the MoAb in this initial investigation are encouraging. The agent, which was prepared in about 30 minutes, was well tolerated, and the procedure was rapidly completed. Although the 120-minute images were the most accurate, the changes in accuracy over time were modest, ranging from 0.75 at 5 minutes to 0.79 at 2 hours. The high rate of agreement (0.96 in this series) between the results of the MoAb study and those of the 111In-labeled leukocyte study indicates that the behavior of leukocytes labeled in vivo with the antibody is comparable to the behavior of leukocytes labeled with traditional in vitro methods. The results of the MoAb study and the 111In-labeled leukocyte study were discordant in one case, an uninfected hip replacement. The 111In-labeled leukocyte study was false-positive, probably because of marrow activity, while the MoAb study was true-negative (Fig 4). Although marrow uptake of the antibody does occur, at least up to 2 hours after injection, this uptake is considerably less than that present on 111In-labeled leukocyte images. This potential advantage of imaging with monoclonal antibodies is now being evaluated in a larger series of patients.

The ideal radionuclide method for localizing infection would entail only one study. To date, however, dual-tracer studies have been found to be more accurate than a single-tracer study, primarily due to improved specificity. Labeled leukocyte images reflect accumulation of leukocytes. This accumulation is usually, though not always, indicative of infection. Moreover, even when infection is present, it is not always possible to distinguish soft-tissue from bone involvement. The addition of bone or bone marrow imaging, depending on the circumstances, can help to clarify the findings in the leukocyte study. The results in this series are in accord with this idea. False-positive MoAb and 111In-labeled leukocyte study results were associated with gangrene, soft-tissue infection, and an uninfected joint replacement. These conditions are all associated with accumulation of leukocytes, and cannot always be differentiated from osteomyelitis (2,20). The addition of bone imaging provided useful adjunctive information, and the combined studies were more accurate than either study alone.

In summary, in the population studied, use of a MoAb, which was easily and rapidly prepared, was safe, was superior to three-phase bone imaging, and was comparable to the use of 111In-labeled leukocytes in the diagnosis of osteomyelitis of the appendicular skeleton. When interpreted together with the bone scans, the MoAb study was more accurate than any other test. These data suggest that imaging with this murine monoclonal antigranulocyte antibody may, in fact, be a suitable replacement for imaging with in vitro–labeled leukocytes in the diagnosis of osteomyelitis and, as such, merits further investigation.


   FOOTNOTES
 
Abbreviation: MoAb = monoclonal antibody

Author contributions: Guarantor of integrity of entire study, C.J.P.; study concepts and design, all authors; literature research, C.J.P., C.L.; clinical studies, all authors; data acquisition, C.J.P., S.L.K., F.L.W.; data analysis/interpretation, all authors; statistical analysis, C.J.P., M.B.T.; manuscript preparation and definition of intellectual content, all authors; manuscript editing, C.J.P., M.B.T.; manuscript revision/review and final version approval, all authors.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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