Total-Hip Arthroplasty: Periprosthetic Indium-.
111-Labeled LeukocyteActivityand Complementary
Technetium-.99m-Sulfur
Colloid Imaging in Suspected Infection Christopher
J. Palestro, Chun K. Kim, Alfred J. Swyer, James D. Capozzi,
Robert W. Solomon,
and
Stanley J. Goldsmith Departments ofPhysics-Nuclear Medicine and Orthopedic Surgery, Mount Sinai School ofMedicine, Mount Sinai Medical Center, New York, New York ses. Neither pattern nor intensity of periprosthetic
ad
Indium-i i 1-labeled leukocyte images of 92 cemented to tal-hip arthroplasties were correlated with final diagnoses. Prostheses were divided into four zones: head (including
tivity reliably separated infected from uninfected ar
acetabulum),trochanter,shaft, and tip. The presence(or
are similar (24), and because osteomyelitis typically stimulates leukocyte accumulation and inhibits sulfur
absence) and intensity of activity in each zone was noted,
throplasties.
Because the physiologic
distributions
of
99mTcsulfur colloid and labeled leukocytes in marrow
and comparedto the correspondingcontralateralzone. colloid accumulation (25), combined labeled leuko Thoughpresentin all 23 infectedarthroplasties,peripros cyte/sulfur colloid imaging was performed in an effort thetic activity was also presentin 77% of uninfectedax to differentiate physiologic marrow accumulation from throplasties,and was greaterthan the contralateralzone infectious accumulation oflabeled leukocytes. 5i % of the time. When analyzed by zone, head zone We report the patterns of periprosthetic labeled leu activity was the best criterion for infection (87% sensitivity, 94% specifIcity,92% accuracy).Fiftyof the arthroplasties kocyte activity in 92 cemented total-hip arthroplasties, as well as the results of combined ‘ ‘ ‘In-labeled leuko were studied with combined labeled leukocyte/suttur col
bid imaging.Usingincongruenceof imagesasthecriterion cytefl9mTc@sulfur colloid imaging of 50 of these arthro for infection, the sensitivity, specificity, and accuracy of
plasties.
the studywere 100%,97%, and98%, respectively.While variablepenprostheticactivity makes labeledleukocyte MATERIALS AND METHODS imaging alone unreliable for diagnosing hip arthroplasty
infection,the additionof sulfurcolloidimagingresultsin a highlyaccuratediagnosticprocedure.
Patient Population Seventy-two consecutive patients with 92 (68 primary, 24 revision) cemented total-hip arthroplasties were retrospec tively reviewed. Fifty-two patients had unilateral arthroplasties
J NucIMed 1990;31:1950—1955
and 20 had bilateral arthroplasties. There were 26 males and 46 females with a mean age of 62 yr (range: 20—87yr). The
he noninvasive diagnosis of orthopedic implant infection is challenging. Radionuclide procedures used
include technetium-99m (99mTc) bone, gallium-67(67Ga)citrate,and indium-l 11-(‘ ‘ ‘In) labeled leukocyte (WBC) scintigraphy(1—23). Our initial experiences using ‘ ‘ ‘In-labeled leukocyte
mean time between arthroplasty (range: 1 wk—17 yr).
and scintigraphy was 4.6 yr
Arthropbasties were considered infected ifoperative cultures grew out organisms (n= 19) or if gross purubence was evident at surgery (n=4). Arthropbasties were considered uninfected if operative smears revealed no leukocytes and intraoperative cultures were reported as no growth (n=33). Arthropbasties not operated on were considered uninfected if: (a) they were
scintigraphy for diagnosis ofthis entity were unsatisfac tory. While absence of periprosthetic leukocyte activity
the asymptomatic arthroplasty in a patient whose contralaterab
was seen only in uninfected prostheses, periprosthetic
the asymptomatic arthropbasty in a patient undergoing beu
activity was present in infected and uninfected prosthe
kocyte imaging for reasons unrelated to that arthroplasty (n= 10), or (c) they were a painful arthroplasty that responded to conservative (anti-inflammatory, but not antibiotic) ther apy (n=6). No patients with clinically uninfected arthroplas
ReCeivedFeb. 20, 1990;revisionaccepted May15, 1990. For reprintscontact: ChristopherJ. Palestro, MD.Box 1141. Dept. of Physics-Nuclear Medione, Mt. Sin@ Medical Center 1 Gustave L. Levy
Place, NewYork,NY10029.
1950
hip arthroplasty
was symptomatic
(n=20), or (b) they were
ties developed symptoms referable to their arthropbasties dur ing a minimum follow-up period of6 mo after imaging.
TheJournalof NuclearMedicine• Vol. 31 • No. 12 • December1990
Scintigraphy
For the 50 arthroplasties studies with labeled beukocytes
Leukocyte scintigraphy was performed 24 hr after injection of -‘-18.5 MBq (500 MCi) of autobogous mixed leukocytes labeled with ‘ ‘ ‘In-oxine, according to the method of Thakur et al. (26). Six-minute anterior and posterior images of the arthropbasties were obtained on a barge field of view gamma camera equipped with a medium-energy parallel-hole colli mator using 20% windows centered over the 174 keY and 246
keV photopeaks of ‘ ‘ ‘In. The last 50 arthroplasties were studied with @mTc@sulfur colboid imaging immediately after the labeled beukocyte study. Patients were injected with 370 MBq ( 10 mCi) of@mTc@subfur
colboid, and 6 mm anterior and posterior static images were obtained 1—2 hr later on a gamma camera equipped with a low-energy, high-resolution, parallel-hole collimator, using a 10% window centered on the 140 keV photopeak of 99mTc. Prior to 99mTcsulfur colboid injection, to confirm that the contribution of ‘ ‘ ‘In photons to the @mTc image was minimal, a 6-mm anterior view of the region of interest was obtained using a 10% window centered around the 140 keV photopeak of 99mTc and the standard intensity setting for routine sulfur colloid marrow imaging. Because no discernible contribution of ‘ ‘ ‘In photons to the @mTc image was seen in any ofthe 20
and sulfur cobboid, images were classified as congruent if the
distribution ofthe two radiotracers was spatially identical, and incongruent ifbabeled leukocyte activity was observed without
corresponding activity on the sulfur colboid images. Four criteria for diagnosing infection were selected and compared:
Criterion 1: Any periprosthetic activity. Criterion 2: Periprosthetic activity greater than the contra lateral side. Criterion 3: Labeled beukocyte activity in the head zone,
regardless of activity in any other zone. (Ret rospective analysis of activity by zone mdi cated that this was the best criterion for diag nosing infection with labeled leukocyte imag ing alone). Criterion 4: Incongruent labeled leukocyte/sulfur colboid images.
The results reported represent the consensus of independ ent, blinded, random readings by two experienced nuclear physicians, who had no knowledge of the final diagnoses.
arthroplasties so studied, this is no longer routinely performed.
RESULTS Image Evaluationand DiagnosticCriteria Each arthropbasty was divided into four zones: head (in cluding acetabubum), trochanter, shaft, and tip (Fig. 1). The
presence or absence of labeled beukocyte activity in each zone was noted. When present, the intensity of this activity was compared to the intensity of activity in the corresponding
contrabateral zone. The pattern of periprosthetic labeled leu kocyte activity around each arthroplasty was also noted. Chi square statistics were used to analyze the significance of the relationship between periprosthetic labeled leukocyte activity (n=76) by zone and the presence or absence of infection.
Twenty-three arthroplasties were infected, all opera tively confirmed. Thirteen different organisms were identified: 6 gram-positive, 6 gram-negative and 1 fun gal. Sixty-nine were uninfected, 33 operatively con firmed, and 36 by one of the previously described clinical criteria. Eleven different patterns of peripros thetic leukocyte activity ranging from no uptake in any
zone to uptake in all four zones were identified (Fig. 2). Sixteen (17%) arthroplasties demonstrated no peri prosthetic labeled leukocyte activity: none ofthese were
infected. Seventy-six (83%) arthroplasties demonstrated vary ing degrees of periprosthetic
labeled leukocyte
activity:
all 23 infected and 53 uninfected arthroplasties. Peri
Patterns of Periprosthetic Leukocyte Activity in 92 Hip Replacements 0 Uninfected 14
U,@ Infected
13
Shaft
N
Tip FIGURE1 Diagrammatic representation of the four zones into which
eacharthroplastywas divided.
Total-Hip Arthroplasty • Palestro et al
H
1,
Tp
H.Tr Tr.S Tr.Tp H+Tr H,1
+s •ip•Ip.S.Tp
FIGURE2 Elevenpatternsof periprostheticlabeledleukocyteactivity wereidentifiedamongthe92arthroplasties reviewed.N = no penprostheticactivity, H = head and acetabulum,Tr = tro
chanter,S = shaft,andTp = tip.
1951
TABLE 1 Comparisonof Criteriafor Diagnosisof the InfectedHipArthroplasty AccuracyAny Presenceof
Infected
Uninfected
Sensitivity
Specfficity
activity23/2353/69100%23%42%Activity > contralaterai zone1 5/2327/6965%61%62%Head
activity20/234/6987%94%92%Incongruent zone leukocyte/sulfurcolloid10/1
01/401
00%97%98%
prosthetic activity was greater than corresponding con tralateral zone activity in 15 infected and 27 uninfected
prostheses. The most significant finding observed following analysis by zone, of76 arthroplasties with periprosthetic
orthopedic between
implant
infection has been reported to be
60—80% (8,12,15,20,36).
Indium-l 11-labeled leukocyte scintigraphy has also been evaluated, alone, and in combination
with other
leukocyte activity, was that infection was infrequently
radiotracers and has been compared to 99mTcbone and 67Gascintigraphy,with a wide range of results reported
found in the absence ofhead zone activity (3/49), while
(10—23).
20 of 24 arthroplasties with head zone activity were infected. The difference was highly significant (x2=43.2,
p40.OOl). When 16 arthroplasties without any uptake are included, Criterion 3 yielded a sensitivity and spec ificity of 87% and 94%, respectively.
Generally,
when
used
alone,
interpretation
of this
study has been based upon either the intensity of peri prosthetic labeled leukocyte activity in comparison to various system
reference points of periprosthetic
(12,15,1 7—20) or a grading uptake (14,16,22). The re
Of 50 arthroplastiesstudied with labeled leukocyte/ sulfur colloid imaging there were 10 infected and 40
ported sensitivity of the procedure
uninfected
45% to 100% (Table 2). The low specificity is especially
prostheses. Images were incongruent
in all
10 infected prostheses and 1 uninfected prosthesis. Im ages were congruent in 39 uninfected arthroplasties.
A comparison ofthe four criteriafor diagnosis of hip arthroplasty
infection is summarized
in Table 1.
using these criteria
has rangedfrom 50%to 100%,and the specificity, from critical because of the low prevalence of arthroplasty infection in general. In our own series, with the exception of head zone activity, neither the presence of periprosthetic activity
nor the intensity of such activity accurately identified DISCUSSION TABLE 2
Pain occurs in @—20% of hip arthroplasties, and is usually secondary to loosening with or without infection
LabeledNo. Diagnosis of Orthopedic Implant Infection wit
(27). While infection occurs in 1%-4% of primary hip arthroplasties (28—31), infection rates of 32%—38%fol
ofGroup/Reference Criteria implants SensitivitySpecificity
lowing revision arthroplasty have been reported (31, 32). Therefore, accurate preoperative diagnosis and treatment of an occult infection is essential for a suc
LeukocyteImagingAloneh
Reference 16'150100%90%Reference 14'140100%92%Palestroetalt192100%23%Referencel221686%100%Refe
cessful revision arthroplasty.
Criteria used to diagnose the infected orthopedic prosthesis, including clinical history, physical exami nation, erythrocyte sedimentation rate, peripheral leu kocyte count, aspiration and culture, and plain radiog raphy, are insensitive or nonspecific or both, and their usefulness
is limited
(21,22,33).
Technetium-99m bone scintigraphy, sensitive for de tecting osseous inflammation, suffers from a lack of specificity. It is especially unreliable in the assessment
of hip prostheses during the first 12 mo after implan tation (1,4,5,9,12,1 7,22,34,35).
Sequential
@mTc bone
and 67Ga scintigraphy has been used to improve the accuracy of diagnosing prosthetic infection. Gallium, however, localizes in septic and aseptic inflammation,
and in any region of increased osseous activity. The overall accuracy ofsequential bone/gallium imaging for
1952
2024095%90%Reference 212291 00%50%Reference
535073%95%Palestro 1 alt39265%61%Reference et 43888%93%Reference 183,
2259888%73%Reference 1161 650%100%Palestro et alt79287%94% Criteria:(1) Anyperiprostheticactivity;(2) Periprostheticactiv ity > surroundingboneactivity;(3) Periprostheticactivity> con tralateralside; (4) Periprostheticactivity> symphysispubis on anterior v@w or > sacroiliac joint on posterior view; (5) Penprostheticactivity> normalmarrowactivity;(6) Criteria not specified;(7) Headzoneactivity. . Studies
performed
t Current
series.
with
111In-Iabeled
granulocytes.
TheJournalof NuclearMedicine• Vol. 3i • No. i 2 • December1990
TABLE 3 Diagnosis of Orthopedic Implant Infection by Dual-Tracer
Imaging Group/
No.of
Reference
Tracers Criteria implants Sensitivity Specificity
Reference 19A12485%85%Reference 21A12988%95%Reference 0B23092%100%Reference 1 23B254100%93%Palestro et alB2501
92%, and a specificityof 100%,while Fink-Bennett et al. (23) reported a sensitivity of 100%, and a specificity
of 93%. Using this technique we obtained a sensitivity of 100% and a specificity of 97%, which are in close accordwith theresultsof thesetwo investigators. Corn bining the results of these two series with our data, the sensitivity,
specificity, and accuracy of the procedure
are 96%, 97%, and 97%, respectively, superior to la beled leukocyte imaging alone or in combination with routine bone scintigraphy.
00%97%
This superiority is, we believe, related to the distri A: labeledleukocyteand boneimaging;B: labeledleukocyte and sulfur colloid imaging;1: incongruentbone and Ieukocyte butions ofeach ofthese tracers. Technetium-99m-MDP accumulates in bone, while labeled leukocytes and sul images;2: incongruentsulfurcolloidandleukocyteimages. . Current
fur colloid accumulate in marrow. Conditions that af
series.
fect bone may or may not exert similar effects on marrow,
the infected arthroplasty (Figs. 3—4)(Table 2). We at tribute this to the variable patterns of periprosthetic labeled leukocyte activity encountered in both infected and uninfected arthroplasties. Although the normal distribution of marrow in adults up to 70 yr old gener
and vice versa.
and marrow, even in the reported that incongruent
Therefore
incongruent
bone
i.e., labeled leukocyte, images could result absence of infection. Oswald et al. (39) labeled leukocyte and bone images were 15% of the time, even in the absence of
ally includes the axial skeleton, humeral heads, femoral
infection. Both labeled leukocyte and sulfur colloid images reflect radiotracer accumulation in the reticuloendothe
trochanters,
hal cells of the marrow, although it is unclear whether
and frequently the femoral shafts, there is
considerable individual variation. The implantation of a prosthetic device may produce additional variations. Changes in the normal distribution of marrow through
marrow activity present on leukocyte images reflects labeled leukocytes alone or in combination with free
surgical
is otherwise
manipulation
have, in fact, been demonstrated
in animals (37,38). Improved accuracy for diagnosing osseous infection using labeled leukocyte plus 99mTc@boneimaging (13,
19,21), and labeled leukocyte plus 99mTc@sulfur colloid marrow
imaging
(10,23)
has been observed
(Table
3).
The reported sensitivity and specificity of leukocyte/ bone imaging have ranged from 70% to 88%, and 75% to 95%, respectively. Using combined
aging, Mulamba
labeled leukocyte/sulfur
et a!. (10) reported
colloid im
a sensitivity
of
I I ‘In.
Alterations
in
the
normal)
distribution
produce
of
similar,
marrow
(which
or congruent,
images on both of these studies (24). Infection, how ever, may actually exert opposite effects on leukocytes
and sulfur colloid. While stimulating leukocyte accu mutation infection of bone has been reported to de crease sulfur colloid accumulation (25). These inverse effects result in incongruent images, and permit dis
crimination of infection from unusual, but not abnor mat, periprosthetic marrow distribution. In contrast to previous reports (10,23), we performed sulfur colloid imaging after, rather than before, the
FIGURE3 A 60-yr-old female with a left total-hip arthroplastyimplanted6 yr prior to im aging. (A) Anterior 24-hr labeled leu
kocyte image demonstrates peripros
A%@..:'
B
thetic leukocyte activity in the trochan
tenc,shaft,and tip regions.Although slightly heterogeneous,this activity is approximately the same intensity as the surrounding marrow activity, and less intense then marrow activity on the contralateralside. (B) Anterior sul fur colloid image performed approxi mately 1 hr after (A) revealsnearlyab sent marrow activity in the trochanteric andshaft regions.The study was inter preted as incongruentleukocyte/sulfur
colloidimages,consistentwith infec tion. An infected arthroplasty was re
movedat surgery.
Total-Hip Arthroplasty • Palestro et al
1953
FIGURE4
B
A
An 81-yr-old female with a right total hip arthroplastyinserted 15 yr prior to
imaging.(A)Anterior24-hrlabeledIeu kocyte image demonstrates intense periprostheticactivity surroundingthe trochanteric,shaft, and tip zones.This
activityis moreintensethanthecorre spendingcontralateralregion. (B) Sul
fur colloidimagerevealsdistributionof radiotracer similar to that in (A). This study was interpreted as congruent leukocyte/sulfur colloid images, with
out evidenceof infection.A loose,but uninfectedprosthesiswasremoved.
labeled leukocyte study. The advantage of this is that those arthroplasties which demonstrate no peripros thetic labeled leukocyte activity (17% in our series) need not be studied with sulfur coltoid imaging.
One false-positive labeled leukocyte/sulfur colloid study occurred. While we have no definite explanation for this occurrence, it is possible that overlying soft tissue inflammation
was the cause.
REFERENCES 1. Mclnerney DP, Hyde ID. Technetium-99m-pyrophosphate scanning in the assessment ofthe painful hip prosthesis. C/in Radiol1978;29:513—517. 2. Williamson BRJ, McLaughlin RE, Wang GJ, Miller CW,
Teates CD, Bray ST. Radionuclide bone imagingas a means of differentiating loosening and infection in patients with a painful hipprosthesis. Radiology 1979;133:723—725. 3. Weiss PE, Mall JC, Hoffer PB, Murray WR, Rodrigo JJ,
Genant HK. 99mTcmethyleflediphosphonate bone imaging
In conclusion, periprosthetic activity on labeled leu kocyte images is extremely variable, both in pattern of distribution and intensity of uptake, frequently making interpretation of these images by themselves difficult
4.
(Fig. 5). Although recognition of a significant relation between the presence of activity in the head zone and
5.
arthroplasty
infection
improves
the accuracy
of the
labeled leukocyte study when interpreted alone, the addition of sulfur coltoid imaging improves discrimi nation of physiologic labeled teukocyte accumulation in marrow from accumulation due to infection, result ing in a superior (98% accuracy in our series) test for
the diagnosis of the infected hip arthroplasty. ACKNOWLEDGMENT The authors thank Ms. Elsa Ortiz for the preparation of this manuscript.
?
I HipArthroplasty Infection
6.
7.
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99m-MDP bone scan in asymptomatic total hip prostheses.J Nuc/Med 1982;23:28—29. 8. Merkeb KD, Brown L, Fitzgerald RH, Jr. Sequential techne tium-99m-HMDP/gablium-67-citrate imaging for the evalua tion of infection in the painful prosthesis. J NucI Med 1986; 27:1413—14 17. 9. Aliabadi P, Tumeh SS, Weissman BN, McNeil BJ. Cemented total hip prosthesis: radiographic and scintigraphic evaluation. Radiology 1989;173:203—206. 10. Mulamba L'AH, Ferrant A, Leners N, deNayer P. Rombouts
JJ, Vincent A. Indium-b 11-leukocytescanning in the evabu ation of painful hip arthropbasty. Acta Orthop Scand 1983;
54:695—697. him LabeledLet@kocyte Imaging Penprosthetic Activity? No
@
Yes
SulfurCOiledImaging congwem Images No Infection
Incongwent
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I Infection
FIGURE5 Interpretative algorithmfor labeledleukocyteimagingin the diagnosisof the infectedhip arthroplasty.
1954
11. McKilbop JH, McKay I, Cuthbert OF, Fogelman I, Gray HW, Sturrock RD. Scintigraphic evaluation of the painful pros thetic joint: a comparison of galbium-67-citrate and indium 11b-labeled leukocyte imaging. C/in Radiol 1984; 35:239— 241. 12. Merkel KD, Brown ML, Dewanjee MK, Fitzgerald RH, Jr. Comparison of indium-babeled-leukocyte imaging with se quential technetium-gallium scanning in the diagnosis of bow grade muscuboskeletal sepsis. J Bone Joint Surg fAmJ 1985; 67-A:465—476. 13. Al-Sheikh W, Sfakianakis ON, Mnaymneh W, et al. Sub acute and chronic bone infections: diagnosis using In- 111, Ga-67, and Tc-99m-MDP bone scintigraphy and radiography. Radiology 1985;155:501—506. 14. Pnng DJ, Henderson RG, Rivett AG, Krausz T, Coombs
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examination of total hip arthroplasty: comparison of indium with technetium-gallium in the loose and infected canine arthropbasty.In: Welch RB, ed. The hip. Proceedings of the twelfth open scientific meeting of the Hip Society. Atlanta; 1984:163—192. Van Dyke D, Shkurkin C, Price D, Yano Y, Anger HO. Differences in distribution of erythropoeitic and reticuboen dothebial marrow in hematologic disease. Blood 1967; 30:364— 374.
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Philadelphia: WB Saunders; 1974:33—42. 39. Oswald SG, Van Nostrand D, Savory CG, Callaghan JJ. Three-phase bone scan and indium white blood cell scintig raphy following porous-coated hip arthropbasty: a prospective studyoftheprosthetic tip. JNuc/Med 1989;30:1321—1331.
25. Feigin DS, Strauss HW, James AE. Detection of osteomyebitis by bone marrow scanning [Abstract]. J NucI Med 1974; b5:P490. 26. Thakur ML, Lavender JP, Arnot RN, Silverstein Di, Segab
Editorial
DiagnosingProstheticJointInfection For the past 17 years, we have been studying the problem of how to best diagnose infection in a pros thetic joint by nuclear imaging. We
have studied prosthetic joints with various combinations
of technetium
ReceivedAug. 29, 1990; accepted Aug. 29, 1990. Forreprintscontact: NaomiAlazrakl,MD,do Director, Divisionof Nuclear Medicine,Emory Lk@iversity Hospital.1364 CliftonRoad, NE, At larna,GA30322.
bone scans, gallium, indium leuko
need to review our past history in
cytes, indium
and newer
imaging infected prosthetic joints,
infection imaging formulations in cluding indium-labeled gamma
including the hows and whys of the various radiopharmaceuticals used.
globulin and 99mTdHMPAO Pales tro et at. in this issue of JNM pre sents the case for the combination of II‘In-labeled leukocytes and
Between1973and1979,Reinget al. and Bauer et al. (1,2) reported results of trials of bone scans and
chloride,
99mTc@olloidbone marrow imag ing. To better understand why this has been so problematic a clinical diagnostic
Prosthetic Joint InfectionImaging • Alazraki
imaging
challenge,
we
gallium scans in patients suspected
of having infection or loosening of prostheses.Conclusions often stated that a normal bone scan excluded the possibility of need for surgical
1955