Efficacy of preoperative diagnostic imaging localization of technetium 99m-sestamibi scintigraphy in hyperparathyroidism

Efficacy of preoperative diagnostic imaging localization of technetium 99m-sestamibi scintigraphy in hyperparathyroidism Assumpta Caix&s, MD, Lluis Bern& MD, Antonio Herntidez, MD, PhD, Francisco Javier TCbar, MD, PhD, Paz Madariaga, MD, Onofre Vegazo, MD, Angel Luis Bittini, MD, PhD, Basilio Moreno, MD, PhD, Eduardo Faure, MD, Dolores Ab&, MD, PhD, Joan Piera, MD, PhD, Jose Maria Rodriguez, MD, Jordi Farrerons, MD, PhD. nr~d Manuel Puig-Domingo, MD, PhD, Barcelona,

Marcia,

Afadrid:

and

Zaragoza,

PhD,

Spain

Background.

Until now, preoperative parathyoid imaging has been considered unnecessary because currently available techniques do ,not provide an? better results than an espeti surgeon. W conducted a multicenter prospective study ezjaluating the calLability of technetium 99m sestamibi scintigraphy in the preoperative identification. qfpathologic glands. Methods. Ninetythree patients with h?~pel~a.ratfl~roidism, seven of them reoperative cases, were studied. In addition, 20 age-matched normocalcemic control subjects were also studied. Results.Surgical confirmation of scintigrafihic images was obta.ined in 91 of 93 cases (sen.sitivit-)r, 97.8%). In all reo . p era t’zve cases (n = 7), in all cases of ectopic glands (whether operated or not; n = 6), a,nd in all patients with a sin.gle-gland disease (n = 70), topograph.ic identification of the disease (n = 23), involvement of more tha,n patliologic gland wa.s correct in 100 O1 /‘a . In multiple-gland one gland was visualized in only 61 % of the patients; h.owever, in 91% of patients, at least one gla,nd was localized. Surgical success-defined as postoperative normocalcemia-with. this approach was lOO(%. All scans of normocalcemic control subjects -were ,rzegative. Of 31 pa.tients in whom a multinodular goiter coexisted, seven jn-esen ted a signiJicant radionuclide background at 120 nun utes ’ scan. False-positive images -were found together with those correspondin~g to the path.ologic glands in only three cases. Conclusions.99’nTc-sestamibi is a highly reliable, sensitive, and specific technique for imaging of pathologic glands in h$rerparathLyroidi& especiali$ in sillgle-gland disease. It may be considered as a. f-trst 1’zne sin ,’ gl-pe rote d uie w h en a preopelative topographic diagnosis is required. (Suigery 1997:121:535-41.) From Hospital de Sant Pau, Autonomous la ;inixaca, Mzcrcia, Hospital Gegorio Zaragoza, Spaill

University of Barcelona, Barcelona, Hospital Virgen Maamridn, Madrid, and Hospital Chico de Za,.agosa,

SI~RGICAL LOCALIZ.-\~‘ION OF pathologic glands in patients suffering from hyperpar-athyroidism is highly successful in experienced teams, surgical failure has been reported in LIP to S% of patients in some important series. ‘-’ -1 substantial effort in parathyroid imaging has thus been undertaken in the last decade to obmin a highly reliable sensitive, and specific technique to identifjl the affected gland or glands before operation. This is especially important in ectopic pathologic parathyoid glands, which are present in LIP to 10%

Ak~HO~~H

Accepted

for publication

Reprint rquests: d’Endocrinologia .bmni hIa Claret, Copyight

0 1997

0039.GOGO;‘Y7.;‘$5.00

Nor.

5. 1996

Manuel Puig-Domingo, i Nutricib, Hospital de la Santa 167. Barcelona 08005, Spain. by ­-Year + 0

11/56;79065

Book,

Inc.

MD. Creu

PhD. Serwi i Salt Pm, Pare

de

of patients in some series,~“’ and in which a surgical failure after a first cervical exploration makes difficult a second intervention and also increases personal and economic costs. Substantial evidence of the use of parath!roid imagina by “g”Tc-sestamibi scintigraphjr has appeared in rec&t j.ears.‘- lg Comparisons with other imaging procedures in these studies have almost always shown better performance bv ggmTc-sestamibi o\-er other techniques, including ultrasonography, magnetic resonance imaging, computed tomography (CT) scan, and 201Tl/T~ substraction scintigraphy (TI,/‘Tc) .‘. lo. 15.“2 ” However, even with this information, different considerations indicating potential weaknesses of “““Tc-sestamibi imaging have been raised,‘? such as distortion imaging caused by a coexisting multinodular goiter and thyroid adenoma, a relatively small number of patients in early SURGERY

535

536

caixtis

et al.

Fig. 1. A, “gmTc-sestamibi scan of a eutopic enlarged parath)Toid gland: the persisting image at 120 minutes was topographically identified as lower right and surgically confirmed. B, the image obtained for ectopic enlarged gland located at anterior mediasrinum. series, the real sensitivity and specificity in multiple enlarged glands, and the lack of information in normal subjects, suggesting that this technique may nor be sufficiently reliable for universal use in preoperative diagnosis of hyperparathyroidism. The aim of our study was to prospectively compare a large series of patients with different forms of hyperparathyroidism wilth a control population in an attempt to define the real possibilities of “gmTc-sestamibi scintigraphy in the management of such patients. SUBJECTS

AND

METHODS

Patient selection. After informed consent was obtained, 93 adult patients diagnosed with hyFerparathp roidism at four Spanish university hospitals, all reference centers for endocrine surgery, were included in the study. Hyperparathyroidism, either primary or secondary, was diagnosed according to clinical and biologic data, including hyperrension, nephrolitiasis, bone pain, digestive symptoms, and sustained hypercalcemia, together with supranormal intact parathormone (normal value, 15 to 60 pg/ml, Magic-Lite PTH; Ciba-Corning Diagnostic Corp, hledfield, MA). Patient characteristics. Seventy-two of the 93 patients studied were women and 21 were men, all with a mean

age of 55.1 + 14.‘i years. Primary hyperparathyroidism was diagnosed in 79 patients, and hyperparathyroidism was a result of kidney failure in the rest. In most patients (86 of 93) this was the first diagnosis; in 7 patients, previous operation had been unsuccessful. Two patients had type I multiple endocrine neoplasia, and another had a type II multiple endocrine neoplasia family history. The mean preoperative serum calcium level was 2.97 -C 0.30 mmol,/L (normalrange, 2.14 to 2.54mmol/ L), the mean serum phosphate level was 0.89 + 0.61 mmol/L (normal range, 0.85 to 1.33 mmol/L), and mean intact parathormone was 392.65 + 444.73 rig/L (normal range, 15 to 60 ng/‘L). Control population. To study the specificity of the technique and after giving informed consent, 20 postmenopausal women with a mean age of 56.5 t 11.0 years attending the gynecology and obstetrics department at one of the institutions were also included in the study. Calcium and phosphorus levels, as well as general biochemistry and hematology, were all normal in these individuals. Study design. All consecutive patients with the diagnosis of hyperparathyroidism in the participating hos-

Fig. 2. A, Scan shows an early image in which a heterogeneous thyroidal phase is washed out at 120 minutes, allowing identification of two persisting hot spots that corresponded to inferior enlarged glands. B, Substantial background is present at 120 minutes because of coexistence of multinodular goiter; however, persisting spot at superior left lobe was interpreted as abnormal parathpoid gland and was subsequentl! surgically identified as single-gland enlargement. pitals between June 1993 and October 1995 were included in the study. ,2fter informed Consent was obtained, gg”Tc-sestamibi scintigraphp was performed in all patients. In some patients another imaging technique (ultrasonography and/or CT) was also performed. All patients were treated surgically on the basis of clinical and biologic data according to the National Institutes of Health conference consensus criteria.‘3 Neck or mediastinal surgery, or both, was performed, and operative findings were compared with the localization diagnosis established by scintigraphic images of the pathologic pamthyroid gland or glands. In primal? intewentions in which gammagraphy indicated a cervical localization, careful inspection and recognition of eutopic normal glands were performed. For primary surgery in which an ectopic location was established before operation, either in primary diagnosis or in reoperatice cases, the same procedure was followed, in the interest of identifying normal eutopic glands. Surgical success was defined as the normalization of postoperative serum calcium concentrations.

Radionuclide localization. Planar images of the neck and upper portion of the chest were obtained in the anterior \iew, 15 and 120 minutes after the injection of 370 (in 29 patients) or 740 MBq (in 64 patients) of g9mTcsestamibi, which correspond respectively to the thyroid and parathyroid phases of the scanning. Each image was acquired with a preset time mode of 10 minutes by using a large field-of-view scintillation camera (Siemens Orbiter II; Siemens) with a low-energy, high-resolution parallel hole collimator. Unique images were interpreted as single-gland disease, whereas more than one positive image was considered to correspond to multiple-gland disease. Careful imaging examination of individuals with a coexisting multinodular goiter was carried out to indicate whether the final image was distorted b! the late retaining capacity of the goiter. Other imaging methods. Ultrasonographic images were performed with a high-resolution ultrasonograph (Toshiba; Sonolayer SSA-27OA) and CT scans were done with a Toshiba 900. Surgical procedures. All patients underwent surgical neck exploration with standardized identification of all

535

Caixtis

su rgely

et al. May

Table I. Correlation findings

of ggmTc-sestamibi

localization

of pathologic

No. of enlarged

glands

1

2

3

4

Total

Type of disease

Prilnary HP (n. = 693 First diagnosis* Recurrences? Secondal? HP (12= 1j Kidney failure Ptimay HP (n = 7) First diagnosis Recurrences Secondary HP (II = 1) Kidne\T failure Primary HP ( n = 0 j Secondary HP (12= 2) Kidney failure

parathyroid

Complete identification

64;

glands with surgical

Incomplete identification

1997

and pathologic

False$ositive re&ts

62

0 0

28 0

0

0

0

0 1

211 0

41

1

0

1s

0

0

0

0

2

0

1

1

0

Primal?; HP (1~= 2) First diagnosis Second? HP (II = 11 j Kidney failure

2

9

0

n=93

75

18

3s

HF’, Hypeqnrathyoidism. *One patienr with multiple endocrine neoplasia (MEN) 1 and one with MEN 2.1 were included. tone patient with MEN 1 sas included. IThree patients presented bith ectnpic gland enlargement. BComesponded to accompaqing imayes in relation LO rhwoid retained radionuclide. I ITwo patients showed a negative s<-an: thus these were rhe onk instances considered false negative. IIn four patients the smallest enlarged gland did not show a positive scan

parathyroid glands, regardless of the number detected by scintigraphy. If a solitary or double gland enlargement was found, removal of the pathologic gland or glands was performed. For diffuse pathologic gland involvement, a subtotal parathyroidectomy was carried out and the remnant tissue was marked with a metallic clip, leaving a fragment equal in size to a normal parathyroid gland and always from the most normal parathyroid gland. When mediastinal surgery was required, a transcenical approach was performed forjuxtathymic parathyroids and median sternotomy for ectopic glands located in the lower or posterior mediastinum. Statistical analysis. All data are expressed as mean -C standard deviation. For each imaging technique, sensitivity was defined as the ratio of true-positive results to the sum of true-positive plus false-negative results. Specificiwwas defined as the ratio of true-negative results to the sum of true-negative plus false-positive results. RESULTS Positive scans were obtained in all but two patients (sensitivity, 9$.8%). The negative cases were in two women, 83 and 63 years old, each pi-esenting with un-

operated primary hyFerparathyoidism caused by two small enlarged glands. All reoperative cases (?z= 7, three of them ectopic glands) were correctly identified. In 70 patients in whom final diagnoses of single-gland enlargement were made, a positive scan was obtained (Table I). In two patients, false-positive images were obtained in addition to the positivity of the enlarged gland, causing the misdiagnosis of single-gland involvement (Table II). In 23 patients the final diagnosis was multiple-gland disease because more than one gland was enlarged at surgery. In this group, ““Tc-sestamibi scintiscan showed more than one positive gland in 14 of 23 patients. In the remaining patients the scintiscan showed completely negative scans in two of them, discussed before, and in seven patients only one positive gland was visualized, corresponding to the largest one. Together, these nine cases were considered false negative for multiple-gland disease because none or only one gland could be visualized (Table II). In the 1-l patients in whom the diagnosis of multiple-gland disease was correctly performed by scintigraphy, not all the glands could be visualized, because of a total of 50 affected glands, 38 (76%) were positive at scintigraphy. The weight of the negative glands was much lower than that of the positive ones (0.73 + 0.6 gm versus 5.21 t 7.3 gm).

Caixcis

Table

II. Sensitivity

of “g’nTc-sestamibi

in the identification

of enlarged

parathyroid

Correct

Incorrect

TJ$e of disease Prima? HP First diagnosis Recurrence Secondary HP Kidney failure Total Primary HP First diagnosis Recurrence Secondal? HP Kidney failure Total

Single (72 = 70)

Total (n = 93)

@t 6::

2 1

64 7

0 68 (97%)

11 14 (61%)

11 82 (88%)

MUltipb"

611 0

28 0 0 2 (3%)

8 0

3 9 (39%) ar pathologic

539

glands

(n, = 23)

HP. Hyperpaarhyoidism. *Diagnosis of multiple-gland disease was obtained in those patients in whom at least two glands were enlarged considered con-ect when morr than one gland showed a positive image. tone patient wirh muldple endocrine neoplasia (MEN) 1 and one wirh MEN 2~4 were included. IOne padent with MEN 1 was included. .$False-positive image from thyroid gland caused en-m~eous diagnosis. I ITwo CBFCS showed completelynegative scan.

All ectopic glands (,n.= 6, three reoperative cases) were localized with a single scintigraphic procedure (Fig. 1). Goiter was present in 31 of the 93 patients. In 24 of these 31 patients, at the 12@minute scan, sestamibi was already washed out from the goitrous thyroid gland (Fig. 2). Therefore the minimal background could not have been misleading in the final interpretation. In the seven other patients a substantial background was present at 120 minutes, but the parathyroid image was sufficiently clear for a correct topographic diagnosis in four. In the remaining three patients correct identification of pathologic glands was still possible, but superimposed images of nodular goiter confilsed the real number of pathologic parathyroid glands (Fig. 2). Two of these three glands corresponded to a single-gland enlargement although the scan showed a double image, and in the third gland a quadruple scan was observed even though only two glands were really abnormal. As confirmed by surgery, no normal parathyroid gave a positive scan. Specificity was therefore 97%. Sensiti&y and specificity were unchanged by the use of the radionuclide at low or high doses (370 versus 740 MBq) . Scintiscan was negative in all 20 normocalcemic postmenopausal women who were included as control subjects. In reference to the other imaging procedures, the most used was ultrasonography in 51 cases and CT scan in 33. Sensitivities for these techniques were 40.5% and 48.5%, respectively, whereas specificities were 93% and 94%.

al.

glands

Enlarged parath)roid Identification

et

examination.

3 11 (12%j Scintigraphic

identification

n-as

DISCUSSION Although intraoperative identification of abnormal parathyroid glands is accepted as highly sensitive and specific in the hands of experienced surgeons,‘, ‘2 24 an effort toward obtaining a reliable imaging procedure that may help in the preoperative localization of pathologic glands has been made in the last decade. Although CT scan, ultrasonography, and MRl have shown a high variability in the rates of false-positive and false-negative results, ranging from 30% to 90% depending on the series, 15, 18.25-2y the use of gg”Tc-sestamibi scintigraphy has offered consistently good results.@! “3 ” Parathyroid imaging with this radionuclide was first described by Coakley et a1.30 in 1989. Since then, other studies have indicated that the sensitivity and specificity of this procedure are around 90% in most studies. However, it has been claimed that most reports included a small number of patients, which may lead to a bias effect of early publications. In our experience, which includes more than 90 patients evaluated with the same protocol in different institutions, high sensitivity and specificit) were obtained. The sensitivity of 100% in cases with a single-gland enlargement stands out. ggmTc-sestamibi scintigraphy was able to differentiate between singleand multiple-gland involvement in almost 90% of patients (Table II). Among our patients a single-gland enlargement as small as 75 mg was correctly identified, thus indicating the powerful efficiency of this technique. However, when more than one gland was involved, the larger gland tended to trap all the radionuelide, leading to an absence of image in the smaller glands. This would explain the difference in sensitivity

540

Caixcts

et al.

when comparing single and multiple disease, 97% versus 61%. Comparing the results of patients with primaq and secondary hyperparathyroidism, we observed that most of the failures in detecting more than one enlarged gland occurred in patients with primary hyperparathyroidism. One possible explanation could be the number of glands involved, because all the patients with primary hyperparathyroidism and multiple-gland disease had two enlarged glands at the most. By contrast, most patients with secondary hyperparathyroidism had more than two enlarged glands, which increased the odds that ggmTc-sestamibi will be taken up by the largest ones. This finding leads us to encourage surgeons to explore and identify the four parathyroid glands-even in the presence of a single positive gland-in the scans of patients with primary hyperparathyroidism. On the other hand, when false-positive results are considered, the main problem is the presence of multinodular goiter, which is know~l to retain the radiotracer for a much longer period of time than a normal thyroid and may give misleading images. Scan interpretation in seven of the 31 patients with goiter was difficult, and in three of them the diagnosis was in fact incorrect. A longer washing time with attainment of images at 180 or 240 minutes after administration of ggmTc-sestamibi mav eliminate this problem in such individuals. Specificity of ggmTc-sestamibi scintigraphy was notable, because no single normal gland showed a positive scan. This is also the first study reporting data on a control population; not one among the normocalcemic individuals presented a positive image. All ectopic cases, both reoperative and previously unoperated, were correctly identified, thus indicating the usefulness of this technique in noncervical disease. X case of double-gland enlargement or multiple-gland disease, with a large eutopic abnormal gland, may possibly decrease the radionuclide uptake of a smaller ectopic pathologic gland located, for example, in the mediastinum and thus pass unnoticed. Fortunately, this is a rare combination that we have as yet not observed, despite extensive experience as reference centers for endocrine surgery. Of a total of six cases of ectopic gland involvement, three patients were operated on again; in the other three patients the use of ggmTc-sestamibi permitted primarily a curative mediastinal operation, which would not have been considered without this information.31 This raises the question of whether using ggmT~sestamibi scintigraphy is indicated before the first parathyroid operation. Although the prevalence of ectopic cases is generally below lO%, it is worth recalling that avoiding reoperation is obviously desirable for all patients. Nevertheless, although it was beyond the scope of our investigation, a detailed cost-benefit study would be interesting, taking into account that we did not find

differences in results when the high and low doses of radionuclide were compared, thus implying the possibility of making the procedure much cheaper. In conclusion, what seems consistent from our data and those of previous reports is that if a single imaging technique is required in hyperparathyoid disease, this must be ggmTc-sestamibi scintigraphy, both in reoperative and unoperated cases. This is clear when comparisons with other techniques are made in terms of both sensitivity and specificity. However, although g3mTc-sestamibi is quite accurate for patients with single-gland enlargement, it is not so reliable for patients with multiple-gland involvement. This implies that imaging support in the preoperative evaluation of hyperparathp roidism still does not replace the necessity of an experienced surgeon. It may be very helpful, however, even for experienced surgeons. REFERENCES 1. Rudberg

C, Akerstr6m

ation for primary 1986;99:64351. 2. Russell

CF, Edis

experience of surgeT

G, Palmer

M, et al. Late

hyperparathyoidism AJ. Surgeq

in 441

for primq

with 500 consecutive in the asymptomatic

KG, Fraker management

of operSurgery

hyperparathyroidism:

cases and evaluation of the role patient. Br J Surg 1982;69:2447.

3. Levin KE, Clark OH. The reasons erations. Arch Surg 1989;124:911-5. 4. Billingsley operative

results patients.

for failure

DL, DoppmanJI., of undescendent

in parat&oid

op

et al. Localization and parath>Toid adenomas

in patients with persistent primaT hyperparathyroidism. Surgeq 1994;116:982-90. 5. Weber CJ, Vansant J, ,-Uazraki N, et al. \ialue of ggmtechnetiumsestamibi Surgeq

“%odine imaging 1993,114:1011-8.

6. Prinz R\, Lonchyna coscopic excision Surge?

MJ, Kettle imaging

localization

33:313-K 8. Taillefer calization

\‘, Carnaile of enlarged

B, Wurtz mediastinal

parathyroid

surgery.

A, Proye parathyoid

Ch. Thoraglands.

1994;116:99P1005.

7. O’Doheq ParathlToid tive

in reoperative

and

AG, Wells P, Collins REC, with ggm technetium-sestamibi: tissue

uptake

studies.

R, Boucher I: Ponin C, Lambert of parathyroid adenotnas in

parathyroidism using a single with gg’“technetium-sestamibi 1992;3.3:1801-7.

J Nucl

Coakley .“IJ. preoperaMed

1992;

R. Detection patients xvith

radionuclide imaging (double phase study).

and lch!lxr-

procedure J Nucl Med

9. Wei JP, Burke GJ, Mansberg AR. Prospective evaluation of the efficacy of “g”‘technetium-sestamibi and ?odine radionuclide imaging of abnormal parathyoid glands. Surgery 1992;112: 1111-i. 10. i\‘eber

CJ, Vansant

J, Alarraki

sestamibi iodine 123 imaging Surgery 1993;114:1011-S. 11. ThulC P, Thakore B VansantJ,

N, et al. Value

of technetium

in reoperatil-e

parathyoid

McGari~

I,\:, IVeber

99msurgev.

C. Phillips

LS.

Preoperative localization of parathyroid tissue with ggmtechnetium-sestambi lz31 substraction scanning. J Clin Endocrinol hlet?b ‘ 1994,:8:77-82. 12. Casas AT, Burke GJ, Mansberger AR, It’ei JP. Impact of “““technetium-sestamibi localization on operative time and success of operations for primary hyperparathyoidism. .Im Surg 1994 60:12-7. 13. Halvorson DJ, Burke GJ, Mansberger AR, Wei JP. Use of tech-

Caixcis et al.

netium

Tc-99n-sestamibi

and

preoperative localization mary hyperparathyoidism. 14. \$‘eifiV, normal

Burke GJ, hlansberger parath!Toid glands

disease using combination mibi radionuclide scans. 15. Geatti

0, Shapiro

iodine

123 radionuclide

scan

of abnormal parathyoid glands South Med J 1994;87:3369. AR. Preoperative in patients with ggmTc-pertechnetate

.Inn

B, Orsolon

Surg

imaging of ah hyperparathyoid and gg’“Tc-sesta-

1994;219:568-73.

PG, et al. Localization

roid enlargement: isobu~lisonitrinile

experience with and ~“‘Trhallium

phy and

tomographs.

computed

for

in pri-

technetium-99m scintigraphy,

Eur J Nucl

hIed

methow ultrasonogra-

before surgeIT? J Clin Endocrinol A, Berni L, Piera J, et al. LTtility

t@aphy evaluation

as a first-line imaging of h!perparath~roidislm.

1994;21:15-22.

1995:.13:525-30. 18. Thompson GB, Rlulan with ence.

Clin

BP, Grant

technerium-99msestibi: Surge17 1994:116:96673.

19. Johnston

LB, Carroll

ath>-oid gland using sestamibi

MJ, Britton

localization radionuclide

in the preoperative Endocrinol (Oxf,

CS, et al. Parathyroid an initial

institutional

KE. et al. The

accuracy

in primav h)Ferparathwoidism imaging. J Clin Endocrinol

imaging

Prospective radionuclide

scan

wrsus

high-resolution

Metab

ultrasonography

preoperative localization of abnormal parathyroid glands tients with preciously unoperated primary h>perparathyoidism. .kn J Surg 1993;166:369-73. 21. Rodriguez

JM,

Tezelman

S, Sipel-stein

JP. for

in pa-

AE, et al. Localization

Diagnosis

Dub QY. Endocrinol

and

hy?er-

using technetium-ses 1995;80:7-10.

management

of asymptomatic

consensus development Med 1991;114:593-7.

Prirnaq hyperparathyroidism: Metab Clin North

RP, Graham

hyxr-

LD,

Brock

WB,

confera surgical 1989;18:701-

.Irn Russell

%I.

CostwE

fectiveness of preoperative localization studies in primary hyperparathvroidism disease. Ann Surg 1994;219:582-6. 26. Sim6n I, Simd R, Mesa J, AguadG S, Boada L, Sureda DG. C&mmagrafia de sustracci6n de tecnecio-99m frente

don cloruro de talio-201 y pertecnetato a la ultrasonografia de alta resoluci6n

la localizaci6n de las gltidulas tiroidismo primario. hIed Clin CB.

parathwoidism. 28. Miller~DL,

of par-

GJ, Sathyanarayana, Mansberger -AR, Wei comparison of ggmtechnetium-sestamibi/‘iodine-123

preoperative localization J Clin Endocrinol hletab

Conference.

27. Higgins

experi-

1996;8 1:3x-552. 20. Casas &IT, Burke

23. NIH

14. 25. Roe SM, Bums

Metab 1995;80:302-i. of 99m-Tc-sestamibi scin-

procedure

parathyoidism: tamibi scanning.

24. Clark OH, perspective.

16. Hind@ E, Mel2iere D, Simon D, Perlemuter L, Galle P. Prima? hvperparathyoidism: is trcnetium-99m.sestamibiiiodine-123 substraction scanning the best procedure to locate enlarged glands 17. Caix%

procedures in patients with persistent or recurrent pxathyoidism. Arch Surg 199+129:570-5. 22. Mitchell BB Kinder B, Cornelius E, Stewart .AF. Prima?

primary hyperparathyroidism: ence statement. .Inn Intern

of parathy-

541

of magnetic

Radio1 Doppman

parath!Toid Radiology 29. McInqx

Role

RC, Kumpe

resonance

Clin North JL, Shawker

adenomas 1987;162:133-7.

graphic ablation 129:499-505. 30. Coakley AJ. Kettle

paratiroides en (Barcj 1992;99:774-7.

in patients DA, Liecht;

for

imaging

who have

undergone

RD. Reexploratioll

CP, O’Doherty

Arch

tylisoninile

in the localization Med

1996;37:631-3.

hyper-

of ectopic

of surgq.

and

angio-

Surg

1994;

MJ. Collins

“‘“Tc-sestamibi, a new agent for parathwoid imaging. Cornmun 1989;10:791-&. 31. BernP L, &ix& A, Piera J, et al. Technetium-99m-methox7isobu-1 Nucl

in

Am 1993;31:1017-28. TH, et al. Localization

h~perparadyroidism.

AG, Wells

en

el hiperpara-

parathyroid

Nucl

REX. Med

adenoma.