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    othilb et al., in 1978, docum ented that the m easurement by rectilinear scanning techniques of transit ofgastnicably administered radionuclides was m arkedlyinfluenced by the position of the detector probes and bythe direction of the imaging 1). They found that anteniorby acquired counts alone, com pared to anterior andposterior corrected geom etric m eans, significantly underestimated gastric emptying rates for solid and liquidm eals. Christian et al. later confirm ed these findingsemploying gamma camera techniques 2). Yet, most ofthe reported studies on gastric emptying employingradionuclides are performed from the anterior viewalone without any attem pt to correct for the changingdis tr ibution of the radionuclide within the stomach andconsequent alteration in marker attenuation 38).

    Several authors have also reported an apparent delay,or lag tim e in gastric em ptying im mediately followingmeal conclusion lasting for variable lengths of time 3,9,10 . The purpose ofthis investigation is to evaluatethe need for correction techniques in improving the

    Received Nov. 5, 1984; revis ion accepted June 25, 1985.Jo hn G . M oore , M D , M ed ic al S erv ice 1 1 lG ), VA M ed ic al C tr.,

    S alt L ak e C ity, U T 84 14 8.

    accuracy ofthe measurement ofgastric emptying ratesSpecifically, we wish to examine the influence of geometric mean correction on the appearance of an eardelay period in em ptying and the effect of correctioncurve shape .

    M AT ER IA LS A ND M ET HO DS

    SubjectsA to ta l o f 37 subjects were studied. All had d iscon tinu

    med ications o f any k ind fo r th ree days p rio r to te sting. Tw ere not allow ed to sm oke during perform ance of the em pin g stud y. In form ed co nsen t w as o btain ed follow in g a pp roby the InstitutionalReviewBoardsof the Universityofand the Veterans A dm inistration M edical Center and D evopment Commit tees .

    MealsA fter a 20-hr solid-food fast, each subject w as given a stadardized meal of 50, 300, or 900 g. The meals were of thfollowing composition:

    50 g. Twelve healthy m ale subjects m ean age 3 1 2yr; range 23-51; mean weight = 76.9 4.2 kg; ran

    The Journalof Nuclear Medicine206 Moore,Christian,ayloret al

    Gastric Emptying Measurements:Delayed and Complex EmptyingPatterns W ithout AppropriateC orrectionJo hn G . M oo re, P aul E . C hristian, A ndrew T. Taylor, and N aom i A bazrakiD epartm ent of M edicine and N uclear M edicine, Veterans Adm inistration M edical C enter; andth e U niv ersity o f U ta h Sc ho ol ofM ed icine, S alt L ake C ity, U tah

    Anteriorlyacquiredand geometricmean correctedgastric emptyingcurvesof solidsandliquid isotopic -labe led meals were compared in 37 sub jects g iven 6 1 meals of th reedifferent sizes. Anterior data alone consistently and significantly underestimated solid-phasegastricemptyingrateswith all meal sizeswhen comparedto geometricmeanacquireddata.However,with liquidsthere were only slightdifferencesbetweenanteriorandanteriorandposteriorgeom etricmea n correctede mp tying-rates.The difference probablyreflectsgreaterattenuationof the 140 key photonof 99@ Tcomparedto the 247 keV photonof111In.With anterior data alone, an apparent early delay in emptying of solids was presentwith a ll meal s izes and the resuftant empty ing curves were nonlinearin shape . Geometric

    mean correctionresuftedin the linearizationof the solid-phaseemptyingcurvesandessentiallyeliminatedthe apparentdelayin emptyingor lag phasenotedwith the anteriordataalone.Basedon our results,geometricmean correctiontechniquesare necessaryforaccurateas sessme ntof radioisotopic-labeledsolidm eals.

    J NucIMed 26:12061210 985

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    5 4.5 - 10 4.5 ) w ere g iv en 2 5 g of b eef stew an d 2 5 g o f o ran gejuice. M eal consumption time was less than I mm .

    300 g. Eight healthy male subjects mean age 3 1 2.5yr. range 23-51; m ean w eight = 80.9 2.5 kg; range 72.2 95.5 ) were g iven 150 g of bee f s tew and I50g ofo range ju ice.Each w as studied four tim es on different study days to yield atotal of 32 studies. M eal consumption time was less than 5mm.

    900 g .Seventeen hea lthy male s mean age = 31 .5 1.8 y r;

    range 24-51; mean weight 78.4 3.1 kg; range 53-107)w ere given 900 g m eals consisting of 200 g of beef stew, 200 gof a pp le sauc e, 5 0 g o f b read , 2 25 g o f w ho le m ilk an d 2 25 g o forangejuice. M eal consum ption tim e w as 10 m m or less.

    S OL ID P HA SE M A R KE R

    For each s tudy, 5 mCi of technetium-99m- 99mTc)labeledsulfur colloid w as injected into 2050g of canned liver pate Sells) and fried until crisp. From 36g of the fried pate containing @600Ci of99m lc) w as m ixed thoroughly w iththe beef stew prior to ingestion. The estimated radiationexposure to the 600 @ zCiose of99m Tc is 11 m rad for the totalbody and 144 m rad for the stom ach ii). L abeling efficiencyand stabil ity ofthe pate marker have been previously reported 1 2 .

    L IQ U ID PH A SE M A RK E R

    One hundred microcuries of indium-l i I @In)ie thylenetriam inepentaacetic acid D TPA) w as m ixed w ith the orangeju ice. In a ll studie s, the labe led orange ju ice was consumedafter the solid portion ofthe m eal and im mediately before thefirst gastric image. The estimated radiation exposurew iththis dose is 24 mrad for total body and 44 mrad for thesto ma ch 11).

    RADIOISOTOPIC COUNTING

    Im aging techniques and validation studies have been rep orte d 2 ,1 2). Im ag es w ere o bta in ed at 1 0 30m m in terv als,depending on m eal size beginning w ith the first im age takena t mea l conclusion 0 time). A 410 keV collimato r was used.Solid and liquid phases of gastric em ptying w ere recordedseparately by setting the pulse-height analyzer on the 140-keV photopeak of99mTcand the 247-keV photopeak ofIn.

    Subjects sat while eat ing and in between counting intervalsan d sto od fo r abd om in al im ag in g an d 4 06 0ec c ou nts. A99m Tc point source w as taped to the chest to allow accuratehorizontal and vertical repositioning of the subject betw eenim ages. T he point source w as m arked on a persistence oscilloscope to reposition the subject. Im ages and counts w ere obtam ed at fixed tim ing intervals until greater than 50 of thesolid m arker had em ptied. A t every tim ing interval, im agesw ere acquired in the anterior and posterior projection. T he I -m m interv al betw een reco rd in g the an terio r an d p osterio rcounts w as not believed to introduce any significant error inthe calcula tions . Technet ium-99m counts were correc ted fordownsca tte r in te rfe rence from n by subtracting a m easured dow nscatter fraction of the n counts from the 99m Tc

    c oun ts. T he 9 9m Tc d ata w ere co rrec te d fo r ra dio ac tiv e d eT he geom etric m ean of the anterior and posterior counts square root of the product) w as calculated. B ackgroundrec tio n w as no t p erfo rm ed sin ce th e o rally in ges te d rad iotre rdoes not measu rably leave the G I tract during the couthe study. T he counts observed at each im aging interval wnorm alized to a percentage of the counts obtained at theimage 0 time), which wasassigned a 100 value. The resuwere expressed as the percent of retention at each imag

    tim e for both the solid and liquid m arkers. T he em ptying htim es t,12: the time when 50 of the marker had emptied)w ere com puted by interpolation from the observed data.

    STATISTICAL ANALYSIS

    The means of the percent retention values and the tvalues for the anterior alone and geom etric mean data wcompared at the corresponding timing intervals for bm arkers. P aired tw o-tailed S tudents t-tests of significanwere employed.

    RESULTS

    Solid-phaseemptyingF igure 1, upper panel, show s the m ean retention values

    th e an terior a nd g eom etric m ea n c orre cted c urve s fo r all tmeal s izes .

    50 g m eals: The m ean percent retention values of tanteriorly acquired data w ere significantly p < 0.01 ) highthan the geom etric m ean values at all tim ing intervals.observed m ean t112 value was also significantly p < 0.0higher anterior m ean T,,2 = 41 .5 5.4 m m, geom etric m e1,/2 35.9 5.3 mm).

    300 g meals: The mean percent retention values of thanteriorly acquired data w ere significantly p < 0.001 ) hig

    than the geometric mean values at the 20-,40-, 60-, and 80-m m intervals. T he observed m ean T,12 vw as aL so significantly p < 0.001) higher anterior m ean t1= 83.4 3.5 mm; geometric mean mean T,12 60.3 4.4

    mm). g meals: The mean percent retention values of the

    anteriorly acquired data w as significantly p < 0.01) highat all tim ing intervals. The observed m ean T,12 valuelonger for the anterior data alone but it w as not significandifferent anterior m ean 11/2 = 115.1 9.3 m m; geom etrmean t@,2= 108.8 8.1 mm).

    Inspection of the anteriorly acquired em ptying curvesF igure 1 reveals an early delay in em ptying w ith all three msizes and is particularly m arked for the 300 g m eal in w hicactual increase in counts w as observed at the 20-m m interT he geom etric m ean corrected curves, in contrast, reveaapparent early delay in em ptying w ith any m eal size andlin eariz ation o f th e e mp ty in g cu rv es.

    Liquid-phaseemptyingFigure 1, low er panel, show s the m ean percent retenti

    values for the anterior and geom etric m ean corrected cufor all three m eal sizes.

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    50gMealsN=12 300gM.aIsN=32 9 gMeaIsN= 7

    Solid Solid Solid

    0

    F IG UR EMe anpercentreten tionvaluess.e.m .for solid upp erpan el)and liquid lowerpanel)labeledphases.Avalues 0- - -0) are compared to geometr ic mean-corrected values --)t a ll timing intervals . Asterstatist ically significant differences at the indicated timing intervals by paired t-test analysis see text for v

    Liquid Liquid Liquid

    Ti m e M i n ut e s

    50 g meals: The mean percent retention values of theanteriorly acquired data w ere significantly p < 0.05) higheronly at the 20- and 40-m m tim ing intervals. T he observed t,,,2was also slightly but significantly p < 0.05 > 0.02) higher anterior m ean T,,2 = 25.2 2.4 m m, m ean geom etric m eant,/2 = 23.9 3.6 m m).

    300 g m eals: The m ean percent retention values for theanterior and geom etric m ean data did not significantly differat any timing interval. The mean T,12 values were also notsignificantly different anterior mean T,12 26.1 1.8 mm;geometric mean m ean T,,2 = 25.1 1.4 m m).

    g m eals: T he an terio rly acq uired m ean p ercen t retention values w ere significantly p < 0.05) higher than the m eangeom etric m ean values at the 60-m m tim ing interval only.The observed mean T,,2 values were not s ignif icantly differen t anterior m ean T,,2 = 7 7.0 6 .3 m m; m ean g eo metricmean T,12 = 74.0 5.6 mm ; p > 0.05).

    The liquid curves do not dem onstrate a delay in earlyemptying and show no significant difference between the

    anterior and the geom etric m ean corrected curves. T he anor im age curves w ere slightly higher for all three m eal s

    DISCUSSION

    These findings support the o rig inal obse rvationTothib l e t ab., a nd expand those of C hristian et al.d ocu men ted su bstan tial ina ccuracies in so lid an d li

    m eal radioisotopic counting m easurem ents whenance was p laced on measu rements from a single deing position 1,2). B oth groups reported undenestimtion of solid phase emptying rates when anteridetection alone w as used as com pared to w hen bilatanterior and posterior correction was used. Otgroups, employing correction measurement techniqhave noted the sam e inaccuracies with single viewaging 9 ,10,13,14). T he appa rent e xplanation forincrease in anteriorly acquired counts is due to shi

    The Journal of Nuclear Medicine208 Moore,Christian,ayloret al

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    MealsizeTime

    mm)AveragepercentExtremeercentGeometricAnterior g)

    N mean datadatadifferencedifference

    9, 10 .Th ean ter ior lycq uiredm ptyin gurv esnFig.1 clearly show a delay in early emptying for all sophase 99mTc meals compared to the geometric mcorrected data; this delay is most apparent with the 3g m eal in w hich an actual increase in retention ofm arker w as recorded at the 20-m m counting in teThe apparent early delayed period o f empty ing a ldisappeared w ith geom etric m ean connection producina lin ea r e mp ty in g c urv e w ith a ll th re e m ea l s iz es. T hobservations are pertinent to the application of curfit ting formulas to grouped data . Recommendationcomplex curve-fitting fo rmulae have been made bbeast th ree g roups o f investigato rs who d id not emgeometr ic mean correction 1618).Their nonlincurve-fitting formulae were based , in part, on the nnitio n of a c onsistently o bserved ea rly delay in sphase empty ing. With geometric mean correctedin three reported studies performed on heal thy subjthe emptying curves for the groups most closely cformed to a linear fit, without evidence of a delayearly phase ofemptying 1 , 13, 19). However, even w

    connections, early delayed phases in em ptying in grouof hea lthy subjects a re desc ribed fo r which more cp lex curve fitting fo rmulae may be appropria te 9 ,We are unable to explain these discrepancies ingrouped data but suggest that differences betwestudies in subject selection, m eal w eight and com ption or meal timing and counting in tervals may accfor a part of it.

    In conclusion gast ric emptying studies of three mealsizes in 37 healthy subjects has show n that appropriconnect ion techniques are necessary to accura te lysure solid-phase gas tric emptying ra tes. With the hen gamma-ray ene rgy liquid -phase marker emptyhowever, these connections are probably not nece 14, 18 . The failure to em ploy correction techniquessol id-phase emptying curves has resul ted, in someies, in an apparent early delay period in em ptying anmislead ing non linea r empty ing curves . We do notdud e that such an early em ptyin g d elay period dodoes not exist but nather that an apparent early emin g d elay can be an tifa ctu ab by create d by n ot em plo yappropria te correction techniques. We do not sugthat previous sol id emptying studies employing antdataaloneareinva lidatedhereby.Providedhebimitat ions of anterior detection a lone are apprecia ted uncrab measurements will suffice for most clinical s tuw here gross differences in em ptying rates betwgroups of subjects are sought 3, 4, 8).

    50 12 35.9 5.0 41.5 5.4 15.60.030032 60.3 3.5 83.4 4.3 38.16.8900t15 108.88.1 115.19.3 5.79.1t

    Excluding two of 17 studies because of extrem elyrolongedextrapolatedanteriorlyacquiredemp tying-halfimes ine xcessf400mm).ft

    In single study within series.

    Timemm)AverageExtremeM ealsizeGeometricAnteriorpercentpercent g)Nm ean

    datadatadifferencedifference501223.93.625.2 .05.520.03003225.11.426.1 .84.065.69001774.05.677.06.34.125.0

    TABLE ISolid-PhaseEm ptying Half-Time s.e.m.

    ofthe labe led so lid food mass from a poste rio r to a moreanterior pos ition in the s tomach and towards the antenio r detecto r during mea l d igestion. In phantom studie s,in which the position ofthe labeled food mass within thestom ach w as sim ulated, a shift of as little as 2.54 cmcaused a 35 increase in the anterior count 2). In thesesam e stu dies, geom etric m ean connection p rovided ap oint-so urce sensitivity fo r 9 9m Tc o f 1.9 fo r d ep th sbetween 5 and 20 cm and 3.3 below 2.54 cm andabove 22.86 cm. These data are in agreement withsim ilar studies by Ferrant and C auw e 15), using thegeometric mean technique . The measurement requirestwo detectors pos itioned anteriorly and pos teriorly, asemployed by Tothill et ab., or may be obtained with asingle gam ma cam era w ith th e subject alternately notating to an anterior and posterior position at eachcounting in te rval a s was done in th is study.

    I t i s a pp ar en t f ro m F ig . 1 a n d Ta b le s 1 a nd 2 th at th eerror in anterior m easure ment a lone is consistently

    barge fo r so lid -phase empty ing, particula rly with thesm alle r m eal sizes, w hile the error prod uced in liquidphase emptying is much smalle r and apparent only withthe 50 and 900 g mea l sizes. The e ffect o f the geometricmean correction on liquid empty ing is le ss significan tfor two reasons: a ) the 247-keY gamma photon ofInhas a smalle r a ttenuation coe ffic ient in tissue; and b )the liquid marker emptie s a t a fa sten ra te than the so lidmarker.

    An early delay, or laghase, in gas tric emptying inhea lthy subjects has been reported by several groups 3 ,

    TABLE 2Liqu id-PhaseEm ptyin gHalf-Tim es.e.m .

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    14. Meyer JH, VanDeventer G, Graham LS, Ct al: Errand corrections with scin tigraphic measurement oftric em ptying of solid foods. J N ucl M ed 24:19721983

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    16. Barber D C, D uthie HL, Howlett PJ, et al: Princicom ponents: A new approach to the analysis of gastrempty ing. In Dynamic S tudie s with Rad io isotopesMedicine,Vienna,IAEA, 1975,pp 185-196

    17. E lashoff JD , R eedy Ti, M eyer iH : A nalysis of gasemptying data. Gastroenterology 83:13061312,1982

    18. Dugas M C, Schade RR, Lhotsky D, et al: Compariso

    of methods for analyzing gas tr ic iso tope emptying.J P hysiol 243:6237-6242, 198219. M oore iG , Tweedy C, C hristian PE , et al: E ffect of

    on gas tric empty ing of liquid -so lid mea ls in man .DisSci28:340344, 98 3

    TheJo urnalof NuclearMe dicin2 10 Moore,Christian,a yloretal


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