Ga-67 Citrate Imaging in Malignant Lymphoma:

Final Report of Cooperative Group

Gould A. Andrews*, Karl F. Hubner, and Robert H. Greenlawf

Oak Ridge Associated Universities, Oak Ridge, Tennessee

in a large cooperative study of Ga-67 uptake in non-Hodgkin's malignant

lymphoma, 76% of untreated patients showed positive uptake in one ormore lesions. The percentage of knoirn individual lesions seen on scan ivassignificantly lower; thus, negative findings at any one site may have muchless significance than positive findings. After treatment, the number oflesions seen decreases sharply, but the role of Ga-67 in evaluating responseto therapy is uncertain, esjtecifdly in viete of the fairly large number oflesions ¡indétectablebefore therapy. Histologie type plays a role in Ga-67uptake. Large lesions are much more effectively detected than small ones.In spite of numerous false-negative results, Ga-67 scanning is a usefulmethod in evaluating the extent of untreated disease and the presence oflesions posttherapy.

J NucíMecí19: 1013-1019, 1978

This is the final report of a cooperative study onthe localization of Ga-67 in malignant lymphomaundertaken by several investigators in different institutions. Work done in Hodgkin's disease is not in

cluded here, having been reported previously (1,2).A preliminary publication on malignant lymphomaincluded results on 168 untreated patients (J). Weare now bringing together data for all treated anduntreated cases, including the previously reportedgroup.

The total series includes 296 studies on untreatedand 394 studies on treated patients. The only selection requirement was histologie proof of diagnosis.In these 690 studies, 2,994 sites of special interestwere examined for disease. A few patients werestudied more than once—i.e., before and after therapy—but no special interpretation has been madeof these, and they have been included as separateindividual studies.

METHODS

The earlier paper on Hodgkin's disease (7) gives

details on procedures, which were the same as forthe malignant-lymphoma series. For each study,carrier-free Ga-67 citrate was given intravenously ina dose of 0.045-0.05 mCi per kilogram body weight.At 48 or 72 hr, after efforts had been made to emptythe colon with laxatives and enemas, each patient was

scanned with a rectilinear scanner set to acceptgamma energies from 160 to 320 keV. Contrast enhancement and background erase were not used.The results were encoded for computer handling,according to the methods described earlier (4).

RESULTS

Table 1 summarizes the total data on which thisreport is based, including the numbers of studies ontreated and untreated patients of the various histologie types. A "study" is a whole-body evaluationwith Ga-67 for the presence of disease. A "site" is

an area of the body harboring known or suspecteddisease; inclusion as a site is based upon clinical,radiologie, or radiotracer findings suggesting lymphoma in that specific local area. These findings hadto be fairly definite; for example, a location wouldnot be considered as a "site" simply because it con

tained the lymphatic drainage from a known lesion.Since one patient could have multiple areas of in-

ReceivedFeb. 13. 1978;revisionaccepted Apr. 27, 1978.For reprints contact: Karl F. Hübner,Medical and Health

Sciences Div.. Oak Ridge Associated Universities, P.O. Box117. Oak Ridge, TN 37830.

* Present address: Div. of Nuclear Medicine, Universityof Maryland Hospital. Baltimore, MD 21201.

* Present address: Dept. of Diagnostic Radiology, Marsh-field Clinic, Marshfield, Wl 54449.

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ANDREWS, HUBNER, AND GREENLAW

CelltypeLymphocytic,

welldifferentiatedLymphocytic,poorlydifferentiatedMistiocyticMixed

cellUndifTerentiatedBurkitt'sGiant

follicularTypenotspecifiedTotalTABLE

1.CASEUntreated32791024144034296STUDIESOFStudiesTreated3910315436101447394MALIGNANTTotal

studies7118225677145481690LYMPHOMAUntreated1184734062159130711,305SitesTreated188439580183284192481,689Totalsites3069129863983717193192,994

volvement, the number of sites is, of course, muchgreater than the number of patient studies. Obviously, the number of scanned areas bearing lymphnodes was much larger than the number of singled-out "sites" of probable or likely involvement. The

method of coding sites has been previously reported (4).

Histologie types and treatment. Tables 2 and 3show the numbers of positive results in untreatedand treated patients, classified by histologie type.Studies were recorded as positive if any definitelesion was seen, equivocal if the most suggestivearea was doubtful, and negative in the absence ofany definite or equivocal lesion. These tables tend,of course, to emphasize the positive and do not bringout the presence of sites negative to scan that mayalso be present in patients with positive or equivocalstudies. There were 65% positive studies for thewhole group, 76% for the untreated, and 57% forthe treated.

The histiocytic type, represented by substantialnumbers, consistently showed a high percentage ofpositive gallium studies, as much as 89% positive inthe untreated cases. Next in avidity for the nuclidewere the mixed-cell and poorly differentiated lym-phocytic types, ranging from 58 to 70% of the studies. The undifferentiated and Burkitt's lesions were

represented by too few cases to draw definite conclusions, but all of the small group of Burkitt's were

positive.Table 4 deals with individual sites as related to

histologie types and treatment. The percentagesshould be read horizontally and apply separately toeach treatment category; that is, all untreated sitesfor any one histologie type add up to 100%, etc.With treatment there was a distinct increase in negative sites in general. The reason that the total numberof sites is smaller than in Table 1 is that some sitesin radiation-treated patients had not been includedin the beam.

Results in individual scan sites as related to diagnostic data and clinical expectations. Table 5 ismade up entirely of sites found positive. The vertical

TABLE 2. GENERAL RESULTS OF Ga-67 SCANS

IN 296 STUDIES ON PATIENTSWITHUNTREATEDMALIGNANTLYMPHOMAPositiveHistologie

TypeLymphocytic,

welldifferentiatedLymphocytic,

poorlydifferentiatedHistiocyticMixed

cellUndiff erentiatedBurkitt'sType

notspecifiedTotal(No

patientswithreported.)No.195890282424225untreated%59738970501006976"giantNegativeNo.It161212101062%352111282503121follicular"EquivocalNo.25011009disease%660225003were

TABLE 3. GENERAL RESULTS OF Ga-67 SCANS

IN 394 STUDIES ON PATIENTS WITHTREATED MALIGNANTLYMPHOMAPositiveHistologie

typeLymphocylic,

welldifferentiatedLymphocytic,

poorlydifferentiatedHistiocyticMixed

cellUndifferentiatedBurkitt'sGiant

follicularTypenotspecifiedTotalNo.1859952341422226%46576264401001004857NegativeNo.1738521360021147%4437333660004637EquivocalNo.4670000421%1065000066

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CLINICAL SCIENCESDIAGNOSTIC NUCLEAR MEDICINE

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columns classify them according to degree of substantiation of the lesion by other means, eithershortly before or shortly after the scan study. Thedata in the horizontal lines indicate the pre-scan

clinical opinion about the presence of disease at thesite. The percentage figures read horizontally. (SeeDiscussion for comments.)

Among 419 untreated sites explored surgically—excluding nonlymphomatous lesions and equivocalscan results—we found 52% true-positive scans,42% false-negative scan results, only 2% false-positive scan results, and 4% true-negative scanresults. Only 23 of the 419 biopsied lesions did notcontain lymphoma; thus the ability of the scan togive true-negative results is not adequately tested.In treated patients subjected to a repeat biopsy, theresults relating scan findings to histologie proof wereabout the same.

Relationship of scan findings to stage of disease,therapy, and symptoms. Table 6 gives results forscans and individual sites, classified vertically aspositive, negative, or equivocal, and horizontally according to clinical status and stage of treatment. Thepercentages, with studies separated from sites, addup vertically. This table gives evidence for the general effectiveness of therapy in converting lesionsfrom positive to negative. The fewest positive studiesand sites were in treated patients without symptoms.

Anatomic regions. Table 7 shows the results ofanalyzing five major lymph-node areas for effectiveness of Ga-67 in detecting lesions there, with andwithout prior treatment. This is based on "sites" as

previously defined. The results, which include 2,780sites, are expressed as the percentage (read horizontally) in each category; the categories are defined bylymph-node area and treatment status.

Size of lesion. All proved or apparent lesions,treated and untreated, that could be measured bypalpation or by radiographie images comprise Table 8. No lesion less than 1 cm in diameter was seen.Above this diameter, detectability by scan increasedprogressively with increasing size.

Lymphangiography, scans, and surgical findings.Table 9 gives results for 232 abdominal and pelvicsites that were examined by both lymphangiographyand scanning. If we make the reckless assumptionthat all of these sites contained malignant tissue,then the lymphangiograms yielded 149, whereasscans yielded only 91. In 28 cases included but notseparately designated in Table 9, surgical exploration yielded proof of lymphoma and in this group

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ANDREWS, HUBNER, AND GREENLAW

TABLE 5. POSITIVE FINDINGS AT INDIVIDUAL SITES AS RELATED TO DIAGNOSTIC DATA ANDCLINICAL EXPECTATIONS IN BOTH UNTREATED AND TREATEDGROUPSClinician's

expectation (before scan) of lesion atsiteNonradiotracer

evidence oftumorbeforeor shortly afterscanProvenApparentEquivocalLocal

painNoevidenceSurgicalexclusionNonmalignantAfter

extirpationUnknownTotalsKnownNo.25024716000810522%714410000359038SuspectedNo.582738311173723457%174950799333018934UnsuspectedNo.423665212815329311%1263814661122278523Believed

absentNo.043150535273%01272556134665

the lymphangiogram was superior, yielding 15 positives, 12 negatives, and one equivocal, whereas thegallium scans yielded only 11 positives, 14 negatives, and three equivocáis.

DISCUSSION

In spite of the uncertainties and changing practices in classifying malignant lymphomas, thereappeared to be considerable uniformity among institutions at the time of this study, and enough differences in gallium uptake among the groups tojustify listing the separate histologie types, althoughwe recognize that there was undoubtedly some lackof consistency in histologie classification. Approximately 60% of the cases consisted of only two types,the poorly differentiated lymphocytic and the his-tiocytic. The overall percentage of positive scans in296 studies on untreated patients was 76%, withonly 3% equivocáis. Of those that were negative,we believe that very few, if any, could be explainedby total removal of the disease by diagnostic surgery

before the scan; thus there were about 20% in whichthe scan study completely failed to show the disease.Of those categories with adequate numbers of cases,the poorly differentiated lymphocytic and the histio-cytic groups had the highest incidence of positivestudies. The patients with Burkitt's tumors, although

very small in number, were all positive; furthermore,the amount of uptake in tumor was high, yieldingscans in which lesions showed extreme contrast withnormal tissue; and with no equivocal results. Thusone might be justified in predicting that Ga-67 willbe very useful in detecting and evaluating thisdisease.

From the data on individual sites, a somewhatdifferent picture emerges. In these untreated cases,where histologie confirmation is available for specificareas, we find a low percentage of false-positive*

scan readings (2%) but a disappointingly largenumber of false negatives, i.e., confirmed lesions thatwere not shown by the scan (42%). Thus positivefindings are highly significant but negative ones much

TABLE 6. PHASE OF DISEASE, THERAPY,ANDUntreatedStudiesPositiveNegativeEquivocalTotalSitesPositiveNegativeEquivocalTotalNo.225629296708533931,334%7621353407Patients

undergoingtreatmentNo.5945711116026523448%5341ó36604EarlyfollowupNo.34232597514514234%5839332626SYMPTOMSLate

followup,with evidenceofrecurrenceNo.11436815838535337775%7223549456Late

followup,without

symptomsNo.1343561201608188%2171810864

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CLINICAL SCIENCESDIAGNOSTIC NUCLEAR MEDICINE

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less so. When we compare the results in malignantlymphoma with those in Hodgkin's, we find that the

overall detection rate is significantly poorer in theformer than in the latter, and that in Hodgkin's there

was less variability with histologie type, except fora somewhat reduced uptake in the lymphocyte-predominant category of Hodgkin's.

From the studies on patients with malignant lymphoma who have been treated, we can draw information about the effects of therapy, even though thepretreatment and posttreatment groups are not comprised of the same patients. The previous existenceof a lesion in a local area was generally acceptedas a justification for considering that area a "site" in

a posttreatment evaluation. The average percentageof positive studies falls to 57% (Table 3), showingthat in a considerable number of patients all lesionsdisappeared, or lost their ability to concentrate Ga-67, as a result of therapy. When we analyze thesedata (Table 4) by dealing with a large number ofindividual sites, we see again that treatment reducesthe number that are positive. However, in the smallgroup of giant-follicular lymphomas, both forms oftreatment appear to have been ineffective in reducinguptake. In general, it appears that chemotherapy maybe slightly more effective than radiotherapy in converting positives to negatives; this is different fromthe results with Hodgkin's disease. It might be sug

gested that some poor results with radiotherapy ineither group could be explained by the presence oflesions outside the radiation portal, or, more likely,development of new lesions after therapy. It is puzzling to find in lymphoma that the results of radiationand chemotherapy combined are not as good as thosewith chemotherapy alone in decreasing the incidenceof positive scans. The responses to chemotherapy, asdenoted by the lowering of the percentage of positivesites, were especially pronounced in the histiocytictype, and apparently also in the nonspecified and thesmall group of Burkitt's tumors.

Table 5, rather puzzling but interesting, is comprised entirely of positive sites, and shows how theserelate to the physician's opinions and to objective

data of other types. Some of the apparent discrepancies may be explained by delays of a few days between the scanning and the other diagnostic procedures. We note that in 28% of the positive sites,disease was clinically unsuspected or believed absent,yet demonstrable on scan. This number, involving atotal of 384 sites of which about half had no supporting evidence from other diagnostic tests, maybe erroneously high because of false-positive scanresults, but in view of the low number of false posi-

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ANDREWS, HUBNER, AND GREENLAW

TABLE 8. SIZE OFTUMORScan

resultsNeg.

andeqv.Pos.Percentage

pos.Largest<100016939462878349DETECTEDdiameter

in35892614385860cm5194369>52913081

TABLE 9. RESULTS OF SCAN FINDINGS ANDLYMPHANGIOGRAMS IN 232UNTREATEDABDOMINAL

AND PELVIC LYMPH-NODESITESLymphangiogramsPositiveNegativeEquivocalTotal

scanfindingspercategoryScanPos.6030191findNeg793510124ngsEqv.107017Totalper

category1497211

lives in the surgically explored group, it appears thatthe great majority were actual lesions. Thus, thescan calls attention to significant numbers of lesionsnot otherwise discovered. The results in Table 5 arevery similar to those found for Hodgkin's disease;

however, local pain appeared a more frequent indication of a lesion in lymphoma than in Hodgkin's.

The results in Table 6 confirm the effectivenessof therapy in generally reducing the number of positive scans. The value of ^- for the studies in Table 6

is 78.2. With four degrees of freedom, this shows avery strong association between treatment status andscan findings. Again, as in Hodgkin's disease, the

scan is most likely to be negative in the late-followupasymptomatic group but does reveal a significantnumber of unsuspected disease sites. In the latefollowup with symptoms, the percentage of positivestudies returns almost to the pretreatment level.

In general, this study does not show fully the degree of success achieved with therapy. Many of thescan studies done after treatment had been startedwere not timed so as to show the maximal degree ofimprovement. Furthermore, the reduction in sizethat was shown in many lesions is not reflected in therecorded results.

In considering Table 7, it is important to recallthat the listing of a site had to be based on someclinical, historical, radiographie, or radiotracer reason for considering that local area. In general, if weassume that the criteria for determining sites werethe same as for Hodgkin's disease, the overall inci

dence of positive results in untreated cases is lower

for lymphoma. In both treated and untreated groups,detection appeared best for the thoracic region andsomewhat poorer for axillary, abdomino-pelvic, and

inguinal regions.Table 8 shows that the incidence of positive scan

findings increases with the size of the lesion; this islike the situation in Hodgkin's disease, except that

in lymphoma detectability continued to increaseabove the 5-cm diameter.

Table 9 shows a higher incidence of positives bylymphangiography than by scan for abdominal andpelvic disease, and if we assume that there were notmany false positives, lymphangiography will be themore sensitive detector of disease in this region.Surgical and histological results, available for only asmall number of patients, tend to confirm this impression to some degree.

In malignant lymphoma the histologie type influences Ga-67 uptake to a greater extent than inHodgkin's disease, the highest incidence of positive

results being seen in histiocytic and, probably, Bur-Jcitt's forms of lymphoma, the lowest in the small-cell

lymphocytic type.Whereas the Ga-67 scan shows less detection sen

sitivity in malignant lymphoma than in Hodgkin's

disease, it nevertheless provides a valuable, nonin-vasive method of discovering unknown lesions inboth treated and untreated lymphoma patients. Positive findings are highly significant, but negative scanstudies are not strong evidence for the absence ofdisease. Presumably the failure of treatment to makea previously seen lesion become undetectable by gallium scanning is a sign of unsuccessful therapy, although this has not been clearly proven. Many of thegeneral comments about the cooperative study havealready been published in the Hodgkin's disease

paper (7) and will not be repeated here.

FOOTNOTE

* For the purposes of this report we have defined asfalse positive any site coded as positive and later provedto have no lesion of any kind. There is. of course, anothersmall group of patients (approximately 2% in the untreatedgroup) that have other significant lesions giving positivescan findings.

ACKNOWLEDGMENTS

Active members participating in the Protocols (in addition to the authors) include: Richard S. Benna, MemorialSloan-Kettering Cancer Center, New York, N.Y.; CharlesBoyd, University of Arkansas School of Medicine, LittleRock, Ark.; A. Bertrand Brill. Vanderbilt University, Nashville, Tenn.; Frank Del.and. University of Florida Collegeof Medicine. Gainesville. Fla. (present address: Universityof Kentucky School of Medicine. Lexington. Ky.); C. LowellEdwards, ORAU Medical Division. Oak Ridge, Tenn. (present address: Rockford School of Medicine, Rockford. III.);Ben I. Friedman, University of Tennessee College of Medicine. Memphis, Tenn. (present address: Morton F. Plant

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CLINICAL SCIENCESDIAGNOSTIC NUCLEAR MEDICINE

Hospital, Clearwater, Fla.); Gerald S. Johnston, NIH Clinical Center, Bethesda, Md.; Mohammed Moinuddin, University of Tennessee College of Medicine, Memphis, Tenn.(present address: Baptist Memorial Hospital, Memphis.Tenn.); Thomas P. Haynie, The M. D. Anderson Hospitaland Tumor Institute, Houston, Tex.; David Preston, University of Kentucky School of Medicine, Lexington, Ky.(present address: University of Kansas Medical Center,Kansas City, Kan.); B. J. L. Sauerbrunn, Veterans Administration Hospital, Washington, D.C.; Charles David Teates,University of Virginia School of Medicine, Charlottesville,Va.; Robert H. Wilkinson, Duke University Medical Center,Durham, N.C.; and Joseph B. Workman, University ofMaryland Hospital, Baltimore, Md. (present address: DukeUniversity Medical Center, Durham, N.C.).

Much of the early work in organising the group and theprotocols was done by Ralph Kniseley, ORAU MedicalDivision, Oak Ridge. Tenn. (present address: 1024 E.Locust, Emmett. Id.). Histologie sections on part of thecases were reviewed in Oak Ridge by R. M. Kniseley, C. C.Lushbaugh, and B. M. Nelson, to whom the authors expresstheir gratitude. Computer assistance from Martha Han

sard. Howard Harmon, and Tom Akin is gratefully acknowledged.

This article is based on work supported by the Divisionof Biomédicaland Environmental Research, Joint AEC-NIHInteragency Agreement 40-266-71, and American CancerSociety Grant CI-54.

REFERENCES/. JOHNSTONC, BKNUARS, TEATESCD, et al: "TGa-citrate

imaging in untreated Hodgkin's disease: Preliminary report

of cooperative group. / NucíMed 15: 399-403. 19742. JOHNSTONGS, Go MF, BENUARS, et al: Galliiim-67

citrate imaging in Hodgkin's disease: Final report of coop

erative group. J NucíMed 18: 692-698, 19773. ORÉENLAw RH, WEINSTEIN A. BRILL AB, et al: "Ga-

citrate imaging in untreated malignant lymphoma: preliminary report of cooperative group. J Nncl Med 15: 404-407, 1974

4. KNISELEY RM: A coding index for tumor scanning. InThe Cooperative Croup to Study Localization of Radio-plmrmaceuticals. USAEC Report ORAU-119, Oak RidgeAssociated Universities. 1973

3rd ANNUAL WESTERN REGIONAL MEETINGTHE SOCIETY OF NUCLEAR MEDICINE

October 13-15, 1978 Vancouver Hotel Vancouver, B.C., Canada

Glen Hamilton, M.D., Chairman of the Scientific Program Committee of the Western Regional Chapters ofthe Society of Nuclear Medicine, announces the 3rd Annual Western Regional Meeting of the SNM.

The Introductory Invited Speaker for this year's meeting is Lee Lusted, who will present an hour-long talk on"Medical Decision-Making in Nuclear Medicine." In addition, four-hour refresher courses on the following

topics will be offered: Gallium Imaging, Steven Larson, M.D.; Renal Imaging, Thomas Rudd, M.D.;Venography and Lung Scanning, Wil B. Nelp; and Radioimmunoassay, Ed Mincey, M.D.

One of the special features of the program will be combined scientific and review sessions on thecardiovascular system.

The Award Committee takes great pleasure in announcing that Joseph P. Kriss,M.D., Professor of Medicineand Radiology at the Stanford University Medical Center, has been named recipient of the SNM WesternRegional Award for distinguished service to nuclear medicine. The award will be presented on Friday, Oct. 13,1978.

The Technologist Section has planned a 5-hr sessionon cardiac anatomy, pathology, and physiology for the

nuclear medicine technologist. VOICE credit for this session has been applied for.The remainder of the program will consist of contributed papers submitted by clinicians, research scientists,

and technologists.For further information contact:

Jean Lynch, Administrative Coordinator3rd Western Regional MeetingP.O. Box 40279San Francisco, CA 94140

The 3 rd Annual Western Regional Meeting will have commercial exhibits and all interested companies areinvited. Please contact the Western Regional SNM office (address above), Phone: (415) 647-1668 or 647-

0722.

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1978;19:1013-1019.J Nucl Med.   Gould A. Andrews, Karl F. Hubner and Robert H. Greenlaw  Ga-67 Citrate Imaging in Malignant Lymphoma: Final Report of Cooperative Group

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