Comparison of -99m and Iodine 123 Imaging of Thyroid Nodules: Correlation with Pathologic Findings

Zvonko Kusié,David V. Becker, Eugene L. Saenger, Peter Paras, Peter Gartside, Terry Wessler and Sime Spaventi

DepartmentofNuclear Medicine and Oncology,UniversityHospital “Dr.M. Stojanoviê'@Zagreb, Yugoslavia;Division ofNuclear Medicine, Department ofRadiology, The New York Hospital-CorneilMedical Center, New York; E. L. Saenger Radioisotope Laboratory, Department ofRadiology and Division ofEpidemiology and Biostatistics, University ofCincinnati Medical Center, Cincinnati, Ohio; and National Centerfor Devices and Radiological Health, FDA, Spring, Maryland

available from on-site generators. Iodine-123, however, Threehundredandsixteenpatientswith solitaryor domi is -produced, considerably more expensive, nant thyroidnoduleswere imagedboth with technetium and, with a 13-hr physical half-life, presents significant 99m- (@“Tc)pertechnetateand iodine-i23 (1231).The im logistical problems. Finally, the issue is further compli ageswereindependentlyinterpretedbyfivereaders.Iodine cated by the fact that the valueof thyroid scanningfor scanswere preferred,but differenceswere smalland in cancer detection has been challenged and its clinical 27%—58%of the casesthere was no differencein quality usefulness questioned (12,13) between the two radionuclides. Discrepancies between 99mTcand 1231imageswere found in 5%—8%of cases, Since the introduction of [99mTcjpertechfletate for twiceas oftenin multinodulargoitersas in singlenodules. routine thyroid imaging, a number of cases of thyroid Cytologic/histologicexaminationwas performedon all carcinoma appearing scintigraphically hot with [@mTc] nodulesbut nocorrelationwasfoundbetweenthe pathol pertechnetate and cold with radioiodine have been ogyandthetypeof discrepancy.Twelvecarcinomaswere rather dramatically reported (14—21).The result of found (4%) but none in nodulesshowinga discrepancy. these findings has been the frequent recommendation There was great variationamongthe observersaboutthe that nodules appearing hot with pertechnetate should preferencefor radionuclidesand about the existenceor be re-imaged with an ofiodine in order that the typeof discrepancies.Theslightlybetteroverallqualityof diagnosis of thyroid malignancy is not overlooked. 1231 scans is probably not of diagnostic significance and However, other case reports (22-29) and comparative @ does not justify the routine use of insteadof @“Tc. studies ofthe two radionucides (9,30,31) indicated that Routinereimagingof @“Tchot noduleswith radioiodine for cancerdetectiondoesnot appearto be necessary. benign thyroid lesions are the more likely cause of discrepant findings. Thyroid carcinoma has also been JNucIMed1990;31:393—399 found with another, less frequent type of discrepancy, increased iodine uptake relative to pertechnetate (32). The BureauofRadiologicalHealth(BRH),Foodand Drug Administration (FDA), being interested in reduc everal systematic comparative studies using tech tion of dose delivered to the organs during netium-99m- (99mTc)pertechnetate and radioiodine nuclear imaging procedures, appointed an Advisory (@@‘I,12511231)have been performed in attempts to Task Force on Short-LivedRadionuclidesfor MediCal clarify their respective roles in thyroid imaging. Some Applications. This group recommended that compara showed definite superiority of radioiodine (1—4),but tive studies of [99mTc]pertechnetateand 1231as imaging other authors found the results so similar that they were agents for nodular goiter be undertaken to clarify dif not able to choose one radionuclide as better (5—11). ferences between these two radionucides. The BRH There is similar disagreement about the clinical signif designed a comprehensive study ofthis issue using these icance of discrepant scan findings. The controversy , including cytologic or histologic becomes even more complex if economic factors are follow-up(33). considered. Technetium is inexpensive and readily MATERIALSANDMEThODS ReceivedJuly5, 1989;revisionacceptedNov.21, 1989. The study was conducted in the University Hospital “Dr. For reprintscontact: ZvonkoKusi@,MD,Departmentof NuclearMedI one andOncology,UniversityHospital @Dr.M. Stojanoviô,―Vinogradska Mladen Stojanovié―in Zagreb, Yugoslaviaaccording to a 29,41000Zagreb,Yugoslavia. protocol developed by the BRH FDA's

Technetium-99m and Iodine-i 23 Thyroid Scans Comparison •Kusic et al 393 Laboratoryin collaborationwiththe UniversityofCincinnati definitely normal to definitely abnormal); impression (normal, MedicalCenter. multinodular goiter, cold nodule, hot nodule, and diffuse Entry into the study was limited to patients with a solitary goiter); discrepant area; comparison of @mTcand 1231scan; or dominant nodule on palpation of the thyroid, which was and comparison of 1231(l-hr) and 123!(20-hr) scans. performed by two experiencedthyroid specialistsprior to Each patient had three films, one each for [@mTcJpertech@ imaging. Three hundred and sixteen patients (283 women and netate, 1231at 1 hr, and 1231at 20—24hr. Each film contained 33 men, mean age 42 yr) came from the northwest part of four scans: Yugoslavia,which, until recently,wasan areaofmild endemic goiter.No patienthad a historyofchildhood neckirradiation. 1. Anterior view with a marker on thyroid cartilage and The procedureand purpose of the study were explained and suprasternal notch. individual signed consent was obtained. Controls were 20 2. Sameviewwith a marker on the nodule. clinically and biochemically euthyroid women, mean age 35 3. Right oblique view. with normal thyroidson palpationand no historyof thyroid 4. Left oblique view. disease. The initial image was obtained 20 to 30 mm after an The 1,008 films (three films for each of the 336 subjects: injection of 185 MBq of [@mTc]pertechnetate.Two-hundred 316 patients and 20 controls) were coded, randomized, and thousand counts were collected using the l40-keV photopeak grouped into five batches. In addition, for the first trial, the and 20% window on a scintillation camera (GE 400T, Mil scanswiththe markeron the noduleweremasked.It consisted waukee, WI) with a 5-mm pinhole collimator. Images were of two readings, and was double blinded with respect to recorded on x-ray film. A skin-to-aperturedistance was re radionuclide and patient. Each reader read one batch (201 corded (in the majority ofcases it was 7 cm). An anterior view films) in the first reading. In the second reading, the readers with a marker on the thyroid cartilage and suprasternal notch changed batches so that each film was seen by 2 different also was obtained. The image was repeated with additional readersconstitutingone pair. Five batcheswere read by five markers on any palpable nodules. Oblique views at 45°were differentpairsof readers,as follows:AB,CA, BD, EC, DE. obtained in all patients. In the second trial, the films were unmasked and each Within 1 wk, the patients were again studied, using an oral reader read the same batch as in the first reading. dose of 14.8—18.5MBq of 1231.This preparation(provided by The third trial consisted of direct (simultaneous) compari Malhinckrodt, Vienna, Austria) was free of 1241and had <2% son ofthe three films ofeach patient (99mTc,123Jl-hr, 123!20- with 1251Patients had only liquids for 4 hr hr). For this trial, the films were decoded, unmasked, and prior to administrationof activity. Images and uptakes were reorganized, and identified by patient and radionuclide. obtainedat 1hrand 20—24hrafteradministrationof 1231The There was no attempt to imposerules of interpretation or same instrument, imaging view, and distance was used for criteria evaluation on the readers because it was deemed both radionuclides.Imageswith 1231wereobtainedwitha total important that each reader represent his individual experience of 100,000counts or an imagingtime of 10 mm, whichever and attitude. If rules of interpretationhad been imposed, any came first,usingthe l59-keVphotopeakand 20%window. conclusion of the study might have been less applicable to Cytologic examinations of all palpable nodules were per general(usual)clinicalpractice. formed subsequent to imaging studies. Sixty patients, who were subsequentlytreated surgically,had histologicfindings StatisticalMethods available. The locations of the abnormalities found on palpa The data from the image readingforms for all 336 patients tion and areas biopsied were marked on anatomic drawings and controls were keyed with verification into a permanent of the thyroid and correlation with scan findings was estab computer file. The study was organized to follow a balanced lished by one of the physicians who had originally examined incomplete block design (34). This method permitted the five the patients. readers to read only 40% ofthe films to complete the study. In addition to the medical historyand physicalexamina Frequency tabulations and percentages were obtained by tion, laboratory tests were obtained including serum thyrox creating contingency tables. The amount of association rep me, triiodothyronine, thyrotropin, TRH test, antithyroid an resentedby the data containedin the tableswascomputedby tibodies, and ultrasound for the majority of patients. Hyper chi-squareanalysis using the method of Cramer (35). The thyroidism was diagnosed in 18 patients, the rest were presence of significant heterogeneity among readers for these euthyroid. tabulations was determined by log-linear model analyses. Imageswerereadindependentlyby fiveexperiencedreaders The data for image quality and image interpretationwere (DVB, RSB,ZL, WPL,and ELS)qualifiedin nuclearmedicine analyzed by variance analysis. The values that were not avail image analysis who were not familiar with the patients or able due to the design ofthe study were estimated by the least images. The images were presented to them without medical squaresmethod for theseentries. history, laboratory, cyto-histologicor technical data. All of the readers routinely use [@mTc]pertechnetate as a thyroid RESULTS imaging agent in their institutions. The observations of the five readerswere recordedon a form, which requiredcatego When [99mTc]pertechfletateand 1231scanswere eval rized notations of: image quality (on a five-level scale from uated simultaneously for each patient (Trial 3) there excellent to unusable); image thyroid size; image thyroid was almost general agreement that 123!scans were “bet @ symmetry;image distributionofactivity, iflocalized; location ter―than 99mTc (Table 1). The number of cases ofirregularity; image interpretation (on a five-levelscale from reported as showing no difference was large (27%—

394 The Journalof NuclearMedicine•Vol. 31 •No. 4 •April1990 IComparison TABLE TABLE3 of [@“‘Tc]PertechnetateScans1@I and 123I Associationof DiagnosticImpressionwith the Comparison of @Tcand 1@lScans better99mTc thanthanbetter better@“Tc 1231 @ differenceReader% @Tc,%No betterthanthan casesA of cases of cases% of differenceImpressionof1231,%@‘Tc, %No casesNormal31681Multinodularcasesof cases% of 3835l>TcB27 3527Tc>iC38 4058I>TctD2 goiter185032Cold 5147l>TCtE 2 nodule194239Hot 4145I>TCt. 14 nodule235324Diffuse goiter93457

difference.tNonsignificant Significant difference. . The reading was double blinded with respect to radionuclides and patient identification and with a 58%). Among the reasons mentioned for preference of mask obscuring scans showing location of the palpable one radionuclide were: lower background, sharper edges nodules. All readers preferred 20-hr 123!scans to [99mTc] resulting in better contrast, and absence of esophageal pertechnetate scans; four readers also preferred 1-hr 1231 activity. scans over [@mTc]pertechnetate scans. The same com In a comparison of 1-hr and 20-hr 123!scans, the 20- parison with unmasked films demonstrated that know hr 1231scans were preferred in a significant number of ing the location ofthe nodule did not make a substantial instances by all observers, but in 35%—58%ofcases no change in the preference for radionuclide. difference was indicated. Interobserver agreement did not differ significantly Association ofimage interpretation with the compar for @mTcand 123!scans in categories of image quality, ison of[@mTcJpertechnetate and 123!scans for all readers image interpretation, and diagnostic impression. There combined is summarized in Table 2. For the majority was no correlation between uptake values (32%-55% ofglandsjudged as normal, no difference between @mTc at 20 hr) and preference for radionucides. Correlation and 1231scans was found. However, for abnormal glands of location of palpable nodules with location of scan it was apparently easier to choose one radionucide as abnormality did not show significant difference between better, and the 1231images were generally preferred, 99mTcand 1231images. although there remained a large number of cases in Evaluation of categories of diagnostic impression which no difference was indicated. Comparison of di based on 99mTcand 1231scintigraphy was done blindly agnostic “impression―for scans made with the two without knowledge of location of nodule. There was radionuclides (Table 3) shows a preference for 1231in all great variation among the readers, but every reader categories, although there are large numbers of cases found the lowest percentage of normals and the highest where no difference was noted, especially for glands percentage of multinodular goiter on @mTcscintigra considered “normal―or a “diffusegoiter.―In all cate phy. This observation is in accordance with the finding gories of image interpretation and impression, 20-hr that 99mTcimages of abnormal glands were more likely 23! images were considered better than 1-hr 1231 images to be classified as abnormal than were 1231scans (on a but with a large percentage ofcases reported as showing scale from definitely normal to definitely abnormal). no difference. Both radionucides weresimilarin demonstratingcold Independent evaluation of each film based on image and hot nodules. quality produced a ranking of preference for radio Because of the crossover nature of the trial, which precluded each reader from seeing all images, it is only possible to estimate the overall frequency of discrep TABLE2 Association of Image InterpretationComparison1231with th ancies at 5%—8%.Of the discrepancies reported, there of @“Tcand 1231Scanse was agreement about the type of discrepancy between two readers who saw the same cases in only one-fifth of better99mTc thanImage better these instances. In as many as two-thirds ofthe discrep differenceinterpretationthan1231% @“Tc,%No ant cases, there was disagreement about the very exist casesDefinitely of cases of cases% of ence of a discrepancy. Some readers were more likely 1486Probablynormal 0 to find discrepancies than others—but most often in 2176Indeterminatenormal 3 different images. The most frequent type of discrepancy 2274Probably 4 was technetium, normal or cold with iodine, cold or 3641Definitelyabnormal 23 normal. Technetium hot/iodine cold was somewhat less abnormal 19 4635 frequent. In one-sixth of the cases, discrepant scan

Technetium-99m and Iodine-i 23 Thyroid Scans Comparison •Kusic et al 395 findings did not correspond to the palpated nodule. Discrepancies were found twice as often in multinodu lar than in solitary nodule goiter. Examples of the types of discrepancies found are shown in Figures 1 through 3. Table 4 lists cytologic or histologic findings of lesions with discrepant scan findings. There is no correlation between the observed type of discrepancy and cytology or histology of the nodule. There were 12 carcinomas found in the study, but none of them was found in the A @‘@- B nodules showing discrepancy. Two cancers were found in the glands with discrepant images but did not corre FIGURE2 late with scintigraphic discrepancy. Palpablenoduleintheleftlobe.(A)Nonfunctioningregionon In two patients with technetium hot/iodine cold dis [@“Tc]pertechnetatescan.(B)Increaseduptakeinthenodule crepancy, the TRH test was normal. In three patients on 1@lscan. Histology:follicularadenoma with technetium hot/iodine normal discrepancy, TRH tests were: normal, blunted, and flat. In two patients with iodine hot/technetium normal discrepancy, TRH Only two pairs of readersin our study had statistically test was normal as well as in one patient with iodine significant agreement in preference for one radionuclide hot/technetium cold discrepancy. while three did not. There seemed a greater variation among the observersthan between the radionuclides. The 20-hr 123!scans were preferred in our study to 1- DISCUSSION hr scans, but the differences were small and there were The overall quality of 1231thyroid scans has been a large number of cases in which no difference was judged better than @mTcscans in some reported com noted. The relativelyhigh uptake at 1hr in our patients parative studies (1,4), although the clinical significance (5%—15%) and large dose (14.8—18.5 MBq) may ac of such findings has not been conclusively demon count in part for the good quality of early 123!scans, strated. In the present study, all readers showed a gen which were satisfactoryfor clinical purposes. To obtain eral preference for 1231,but the differences between 100,000 counts with 1231at 1 and 20 hr required < 10 iodine and technetium images were small and could mm in almost all our patients. Ryo et al. (11) found 1- not be considered to be of diagnostic importance. In a hr 1231scans of poor quality. The 4-hr and 24-hr scans large proportion of cases (27%—58%)scans with both with 1231were found to be of equal diagnostic value radionuclides were judged by the different readers to be (36). Our study indicates the possibility of obtaining equal in quality. Differences between average scores for satisfactory 123!images in even shorter time if uptake is quality of 99mTcand 123!scans were very small, but the high. Normal values are still rather high in Yugoslavia large number of cases contributed to their significance. (25%—45%at 24hr). The major reasons for preference of 123!in this and The prevalence of reported discrepancies between other studies were lower background and the greater 99mTc and radioiodine scintigrams varies (1,2,3,7,8, clarity of the picture, but images obtained with both 10,11,37) and probably depends on many factors: se radionuclides yielded essentially the same information.

@ ; .@ -

A B A B FIGURE 3 FIGURE1 Palpable nodule in the lower part of the left lobe corresponded Palpablenoduleintheisthmuswasaboutequalinfunctionto to anareaof apparentlynormal[@“Tc]pertechnetateconcen the remainderof the glandon [@TcJpertechnetatescan(A) tration(A)butabsent1231concentration(B).Histology:follicular andcoldon1231scan(B).Histology:follicularadenoma adenoma

396 TheJournalof NudearMedicine•Vol.31 •No.4 •April1990 omous nodules may have different degrees of function FindingsNumberTypeDiscrepantImagesTABLE: Cytolog4ic or Histologic seen in the relatively suppressed normal thyroid tissue (38). One autonomous nodule with significantly better histology@‘Tcof discrepancyof casesCytology or function in the suppressed tissue with 1231as compared to 99mTcwas found in the present study. In some hot/1231normal2 goiter 1 Hemorrhagiccystt patients with scan discrepancy and hot nodule seen 1 Severeacuteinfiammationt only with one radionuclide, a TRH test was performed. cysf99mTc 1ColloidColloid goiter with In one-third of the cases with positive [@mTcJpertech@ netate uptake and negative 1231uptake, the TRH test hOt/1@Icold1 goitert was abnormal (flat or blunted). In all cases with a 1 Hemorrhagiccystt 1 Lymphocyticthyroiditist positive 1231uptake and negative [@Tc]pertechnetate 1 Colloid goiter with cyst uptake, the TRH test was normal. Although the most goiter9smTc 2ColloidColloid sensitive study (the suppression test) was not performed, the results suggest that not all nodules which are hot normal/1231cold4 goitert only with one radionuclide show autonomous function. 1 Normalthyroid@ 1 Lymphocyticthyroiditi& There seems a greaterprobabilityof autonomy in nod adenom&s9mTc 1ColloidFollicular ules appearing hot only with @mTcthan in nodules appearing hot only with 1231but the number of such adenom&99mTcnormal/123Ihot1Follicular cases was rather small. cold/'231normal4 goitert In the present study, the @“Tcimages were more 3 Hemorrhagiccystt 2 Follicularadenoma likely to be described as abnormal and classified as neoplasmt99mTc 1ColloidFollicular representingmultinodular goiters than 123!scans. The pathophysiology and significance of such findings has coid/'@I hot1 goitert not been clarified. In 1983, Ryo et al. reported that 1 Hemorrhagiccystt more lesions with increased uptake can be demon adenoma. 1ColIoldFollicular strated on 99mTcscintigraphythan on 1231scintigraphy (1 1). They concluded that the sensitivity of@mTc scan Histology.t fling in detecting lesions is higher than that of 123!.In Cytology. our study, the frequency of that kind of discrepancy, however, was not high. The use of ultrasound is prob lection of patients, the imaging procedures (timing of ably desirable to assist in establishing the diagnosis in the images, scanning equipment), use of 1311or 1231, such situations. Occurrence of the multinodular image criteria used for evaluating images, etc. Usually 24-hr pattern in a palpatory uninodular goiter is not uncom radioiodine images were reported, although some au mon (11,39). The value of finding multiple scan ab thors used earlier times, even 20 mm after i.v. admin normalities in palpatory uninodular goiter has been istration (4). In some studies, a large proportion of the questioned. Such findings may make cancer in the subjects had no thyroid abnormality or had Graves' nodule less likely. disease (1,3) and a low frequency of discrepancy was Few discrepancies between 1-hrand 20-hr 123!scans found. This is in contrast to the studies where a high were noted, although there were some variations in the proportion of the patient population had nodular or degree of function in the present study. In two cases, 1- multinodular goiter (2,11,20). It appears in all studies hr 1231scans were more similar to 99mTcthan to the 20- that the patients with multinodular goiter have the hr 1231scans. The quantitative differences between areas highest frequency of discrepancy. In the present study, of normal and deficient organic binding may increase patients were selected for inclusion because of finding with time (9). on palpation of a solitary or dominant nodule with Oblique views generally were felt to minimize the presumed greater risk ofmalignancy. In addition, image incidence ofdiscrepancies in the present study. On rare evaluation and precise correlation of the pathologic or occasions, however, oblique views introduced a discrep cytologic findings with scan abnormalities in multinod ancy which was not seen on the anterior view. In ular goiter is usually difficult. However, a number of multinodular goiters, different areas sometimes showed multinodular goiters were inevitably included. The rel different kinds of discrepancies. atively low frequency of discrepancies (5%—8%)in the Cytologic and histologic examinations of nodules present study, is probably due to patient selection. with discrepantimages have revealeda varietyof lesions Discrepancies were found twice as often in multinodu (9,14—16,19,22,26,27,29,30). The lack of correlation lar image patterns than in images showing a solitary reported in the literature between the type of discrep abnormality. ancy observedand histology ofthe nodule is confirmed The radioiodine scan and technetium scan of auton in the presentstudy. Microscopic foci ofcarcinoma that

Technetium-99m and Iodine-i 23 Thyroid Scans Comparison •Kusic et aJ 397 could not be the cause of the discrepant scan finding ACKNOWLEDGMENTS have been reported (30). In the present study, a similar Presented in part at the 35th Annual Meeting ofThe Society case of lack of correspondence of carcinoma and scan of Nuclear Medicine, San Francisco, June 14—17,1988. discrepancy in the same gland was found. The authors thank Dr. Richard S. Benua, Dr. James R. The most frequent explanation for positive @mTc Hurley, Dr. Zeljka Labar, Dr. Paul W. Lee, Dr. Harry R. uptake and negative radioiodine uptake has been that Maxon, Dr. Hiroshi Nishiyama, Dr. Ivo Padovan, and Dr. these nodules retain the ability to concentrate mono Ivo @lausfor their cooperationand Dr. David N. Charkesfor valent anions (pertechnetate and iodine) but have lost his criticalreviewof the manuscript.The authors are grateful to Mallinckrodt Diagnostica (Byk Sangtec), Vienna, Austria, the ability to organify iodine (23), allowing it to be for generouslydonating the initial supply of 1231.This study readily discharged. Some lesions which are hot on 99mTc would not have been possible without the cooperation of the scan and not visualized on radioiodine scan may be technical staff and secretarial expertise of Miijana Ivathé autonomous and have a rapid iodine turnover in the from the Department of Nuclear Medicine and Oncology, nodule (24). In the present study, no malignancy was University Hospital “Dr.M. Stojanoviá,―Zagreb, Yugoslavia. found in patients with 99mTcpositive and radioiodine This material is based on work supported by the U.S.- negative scans. Detailed review ofthe literature suggests YugoslavJoint Fund for Scientificand TechnologicalCoop that the frequency of thyroid carcinoma with such eration, in cooperation with DHHS/FDA under Grant No. discrepancy is very low. In addition to four case reports 02-660-F. (14,16,1 7,18) in three studies comparing the two REFERENCES radionuclides (15,20,21), only three cases were re 1. Atkins HL, Klopper JF, Lambrecht RM, Wolf AP. A com ported. In all of these studies, ‘@‘Iwas used for radioi parison of technetium-99m and iodine-l23 for thyroid im odine with the relatively poor resolution aging.AmiRoentgen1973;117:195—201. of the rectilinear scans in some studies. In one study, 2. Gorowski T, Chomicki OA. Some comparative studies using the unusually high number of discrepancies caused by 99mTcand ‘@‘Iin thyroid scanning. Nuk/earmedizin 1976; 15:268—272. cancers particularly follicular (twice as many as all cases 3. Prince JR. 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Technetium-99m and Iodine-i 23 Thyroid Scans Comparison •Kusic et al 399