Assessment of Gastric EmptyingComparison of Solid Scintigraphic Emptying and Emptying

of Radiopaque Markers in Patients and Healthy Subjects

PER-OVE STOTZER, MD, PhD, MARTHA FJ ÈALLING, MD, PhD,

JAKOBINA GR ÂETARSD ÂOTTIR, PhD, and HASSE ABRAHAMSSON, MD, PHD

The gold standard for measuring gastric emptying is scintigraphy, eithe r with dige stible solidsor liquids. Unfortunate ly, this method is expensive and of limited availability. An alternativecould be to use radiopaque markers (ROMs). Our aim was to compare these two tests inhealthy volunte ers and in patients to see whether emptying of ROMs can substitute forscintigraphic solid emptying. We also intended to see if patients with small intestinal bacte rialovergrowth (SIBO) had delayed gastric emptying. Twenty healthy subje cts and 21 patients, 11with SIBO and 10 with insulin-de pendent diabe tes mellitus (IDDM), were include d. Astandard meal with a [

99mTc]MAA-labe led omelet and 20 ROMs was given. Scintigraphic

emptying and ROM emptying were followed simultane ously. Reference values for gastricemptying of ROMs were determined in 50 healthy subje cts. The scintigraphic method and theradiologic method correlated signi® cantly in healthy subje cts (P , 0.05) , and in patients (P ,0.001) , when comparing half-emptying time for both methods. Scintigraphic half-emptyingtime corre lated signi® cantly with emptying of ROMs after 6 hr. Six of 11 patients with SIBO(P , 0.02) and 7/10 patients with IDDM (P , 0.02) had delayed scintigraphic emptying ofsolids using the 95th percentile in the controls as the uppe r reference value . Gastric emptyingof ROMs was, similar to solid scintigraphic gastric emptying, slower in women than in men.In conclusion, scintigraphic emptying of solids and emptying of ROMs are close ly corre lated.The radiologic method can be used as a simple r and more readily available method. Womenhave slower gastric emptying of ROMs than men, which necessitate s separate referencevalues. A high proportion of patients with symptomatic IDDM and with SIBO have delayedgastric emptying.

KEY WORDS: bacte rial overgrowth; diabetes me llitus; gastric emptying; small intestine.

Disturbed gastric emptying plays a major role in many

diseases (1). The most common are severe functional

dyspepsia (2± 4) and diabe tes mellitus (5± 9), but in a

large group of patients the cause is unknown (1).

Symptoms associate d with de layed gastric emptying

are nausea, vomiting, abdominal discomfort, early

satiety, and abdominal pain (1, 9). In diabe tes melli-

tus, impaired gastric emptying can cause poor meta-

bolic control (5).

The most direct and perhaps the most physiologic

method for measuring gastric emptying is scintigra-

phy, assessed as liquid or solid emptying. Unfortu-

nate ly, this method is of limited availability. An alte r-

native method for measuring gastric emptying could

be to use indige stible radiopaque markers (ROMs).

This method is available in every hospital. However,

the reliability of this method has been disputed. Some

Manuscript receive d April 25, 1998; revised manuscript rece ivedSeptember 22, 1998; acce pted Novembe r 14, 1998.

From the Departments of Internal Medicine, Nuclear Medicine,and Radiation Physics, Sahlgrenska Unive rsity Hospital, GoÈ teborg,Sweden.

Address for reprint requests: Dr. P.-O. Stotzer, Departme nt ofInternal Medicine , Sahlgrenska Unive rsity Hospital, S-413 45GoÈ teborg, Sweden.

Digestive Diseases and Sciences, Vol. 44, No. 4 (April 1999), pp. 729 ± 734

729Digestive Diseases and Sciences, Vol. 44, No. 4 (April 1999)

0163-2116/99/0400-0729$16.00/0 Ñ 1999 Plenum Publishing Corporation

authors found no corre lation between scintigraphic

gastric emptying of solids and emptying of ROMs (3,

4, 7) while others found a good corre lation (2). One

report sugge sted a better corre lation between symp-

toms and disturbed gastric emptying in patients with

diabe tic autonomic neuropathy when comparing

ROM emptying with scintigraphy (8).

Small inte stinal bacterial overgrowth (SIBO) is a

disorde r known to be connected with disturbe d mo-

tility in the small bowel and the gastric antrum (10,

11) . It is not known whether de layed gastric emptying

is common in this disorder.

This study was done with the aim to see whether

ROM emptying can be used as an alternative to solid

scintigraphic emptying. For that purpose we com-

pared these two tests in healthy volunte ers and in two

different groups of patients, one where de layed gas-

tric emptying is known to be a common ® nding,

insulin dependent diabe tes mellitus (IDDM), and one

where motor disturbance s are common and delayed

gastric emptying could be suspected, SIBO. The sec-

ond aim was to see if patients with SIBO have an

increased frequency of de layed gastric emptying.

MATERIALS AND METHODS

The study was divided into three parts. Part 1 was per-formed to select a proper type of ROM for further tests. Inpart 2 reference values for ROM emptying were deter-mined. In part 3 we compared scintigraphic emptying ofsolids with emptying of ROMs in healthy subjects and inpatients.

The study was approved by the Ethical and Isotopecommittees at Sahlgrenska University Hospital. Each sub-ject had given informed consent.

Subjects. Ten healthy volunteers, mean age 31.7 years(range 26 ± 38), 5 men and 5 women, participated in thestudy to select ROMs for further studies. To establishreference values for normal ROM emptying another 50healthy subjects participated, mean age 37.2 years (range25± 57) , 17 men and 33 women. Twenty of the 50 subjects,mean age 39.8 years (range 26 ± 57), 4 men and 16 women,participated in the combined ROM emptying test and scin-tigraphic solid emptying test.

Patients. Eleven patients with SIBO, mean age 66.4 years(range 48 ± 85) , 4 men and 7 women, and 10 patients withIDDM, mean age 46.5 years (range 35± 59), 1 man and 9women, participated. None of the patients with SIBO hadsymptoms of dyspepsia. All patients with diabetes mellitushad at least one symptom suggestive of delayed gastricemptying (see Introduction). Patients with previous gastricor small intestinal operations were excluded.

Selection of ROMs. In this part the optimal size anddensity of ROMs were selected. Five different ROMs weretested: (1) density 1.13 g/cm

3, cubic with 3 mm side; (2)

density 1.13 g/cm3, cubic with 1.5 mm side; (3) density 1.27

g/cm3, cylindric with size 2 3 2 3 8 mm; (4) density 1.27

g/cm3, cubic with 2 mm side; and (5) density 1.27 g/cm

3,

cubic with 1 mm side. The ROMs were compared in pairs

always using the ROM with density of 1.13 g/cm3

and 3 mmside as one part in the pairs. Although no signi® cant differ-

ences between these ROMs were observed (see Results),

the two different ROMs with density of 1.13 g/cm3

were

further compared to scintigraphic solid emptying in 10healthy subjects.

Standard Meal. In all emptying tests the same standard

meal was given. The meal was ingested within 10 min andconsisted of an omelet and 150-ml of a soft drink. The totalenergy content was 380 kcal. The omelet was made fromtwo eggs, 100 ml milk, 15 g ¯ our, and 5 g margarine and wascooked in a microwave oven. Macroaggregated albumen[12± 15 MBq

99mTc-labeled (Pulmonate) Amersham Inter-

national plc, Little Chalfont, UK] was added to the studymeal to determine scintigraphic emptying. The albumenbinds to the protein during cooking (12).

Scintigraph ic Emptying. Examination was done in thesitting position. The gamma camera used was a GeneralElectric (400 AC/T) ® tted with a low-energy all-purposeparallel-hole collimator. The gamma camera was connectedto a GE Starcam computer system. Anterior and posteriorregistration was each performed for 60 sec. The geometricmean from the two registrations was calculated to correctfor anterior/posterior movements of the gastric contents(13) . Correction was also done for physical decay of theisotope. Registration was done immediately afte r complet-ing the mean and after 10, 20, 30, 60, 120, 180, and 240 min.Gastric retention at 120 min (T120) and half-emptying time(T50) were calculated. The T50 value was derived from thecalculated linear regression line for gastric emptying. Ref-erence values for solid gastric emptying were established ina larger study of 160 healthy subjects: Values are given as5th and 95th percentiles. For men, the T50 was 55± 109 min,and retention at 120 min was 0 ± 44% ; for women # 40 yr,T50 was 71± 156 and retention at 120 min was 9 ± 66% ; forwomen . 40 yr, T50 was 59 ± 125 min, and retention at 120min was 0 ± 52% (HellstroÈ m et al, in preparation).

Emptying of ROMs. Twenty cubic ROMs with a densityof 1.13 g/cm

3and 3 mm on a side, chosen from the selection

test, were given toge ther with the standard meal. Emptyingof ROMs was followed with ¯ uoroscopy hourly until allROMs were emptied or for a maximum of 6 hr. Total timefor ¯ uoroscopy was less than 2 min, and total radiation wasless than 1 mSv. Half-emptying time (T50) was approxi-mated to the time when at least half of the ROMs wereemptied. If half-emptying was not achieved during theexamination time, T50 was approximated to 360 min.

Diagnosis of Small Intestinal Bacterial Overgrowth . Fordiagnosing small intestinal bacterial overgrowth, we usedthe following diagnostic tools: culture of small bowel aspi-rate , hydrogen breath test with 50 g glucose, and the clinicalresponse to treatment with antibiotics. Criteria for positivetests were: (1) culture of small bowel aspirate containing. 10

5colonic type bacteria/ml, (2) hydrogen breath with an

increase of hydrogen concentration of more than 14 ppmover baseline recordings (14) , and (3) favorable response totreatment with antibiotics evaluated with a second hydro-gen breath test and a questionnaire including registration ofstool frequency and abdominal symptoms (abdominal pain,abdominal bloating and ¯ atulence) before and after treat-

STOTZER ET AL

730 Digestive Diseases and Sciences, Vol. 44, No. 4 (April 1999)

ment. Patients included ful® lled at least two of these threecriteria (11).

Statis tics. Results are presented as median values andpercentiles. For statistics Student’ s t test, Fisher’s exact test,linear regression, and the Mann-Whitney U test were used.

RESULTS

Comparison of Different ROMs. There were no

statistically signi® cant differences in emptying time

among the ® ve different markers, as illustrated by

data from the two ROMs that were compared to

scintigraphic solid emptying (Figure 1). However, a

slight trend towards faster emptying of the smalle r

and the lighte r ROMs was observed. On the other

hand, it was easie r to identify the larger ROMs on

¯ uoroscopy, although the only ones de ® nite ly dif® cult

to count were the ROMs measuring 1 mm on a side .

For furthe r evaluation, the cubic ROMs with a den-

sity of 1.13 g/cm3

and 3 mm on a side were chosen.

ROM Emptying in Healthy Con trols . All 17 men

emptied all 20 ROMs within 6 hr. The numbers of

ROMs remaining at 6 hr in women were 0 (0 ± 8)

(median, 5th and 95th percentiles) (Figure 2). Men

had emptied more ROMs than women at all time

points (P , 0.01, Student’ s t test).

Comparison Between ROM Emptyin g and Scintig-

raphy. Analysis of T50 with linear regression for the

two tests gave the following results: In the healthy

subje cts, r 5 0.468 (P , 0.05) ; in all patients, r 50.686 (P , 0.001) ; in patients with SIBO, r 5 0.543

(P 5 0.1) ; in patients with IDDM, r 5 0.79 (P , 0.01) ;

in patients and healthy subje cts taken together, r 50.564 (P , 0.0001) (Figure 3). Comparing the T50 for

emptying of ROMs with T50 at scintigraphy, a signif-

icant corre lation was obse rved in IDDM (P , 0.05) ,

all patients (P , 0.001) (Table 1), and in patients and

Fig 1. Mean emptying curve s of scintigraphic solid emptying of theomele t test meal and emptying of cubic ROMs with a density of

1.13 g/cm3

and sides of 1.5 and 3 mm. Solid emptying was signi® -cantly faster at 5 hr but not at 6 hr. There was no signi® cant

difference between emptying time of the two different ROM sizesat any time.

Fig 2. Reference values for gastric emptying of ROMs with a

density of 1.13 g/cm3

and 3 mm on a side in healthy subjects (17men and 33 women).

Fig 3. Relation between half-emptying time (T50) for solid empty-

ing and ROMs in patients and healthy subjects. T50 for ROMs withemptying time . 360 min is approximated to 360 min.

ASSESSMENT OF GASTRIC EMPTYING

731Digestive Diseases and Sciences, Vol. 44, No. 4 (April 1999)

healthy subjects together (P , 0.0001) , and there was

a tendency towards signi® cance in the SIBO group

(P 5 0.06) (Fisher’s exact test).

Comparison between the retention of ROMs after

6 hr and retention at 120 min (T120) for scintigraphy

gave similar results as comparing ROM emptying at 6

hr with T50 at scintigraphy.

Although signi® cantly corre lated, the emptying was

signi® cantly slower for the indige stible ROMs with

T120: 90% (interquartile range 0 ± 100) compared to

28.5% (interquartile range 0 ± 60) for dige stible solids.

Gastric Emptyin g in Patients. In the SIBO group

4/11 patients (36% ) had prolonge d gastric emptying

with both emptying tests, and two additional patients

had delayed scintigraphic emptying, ie, in total 6/11

(55% ), compared with the results in 160 controls.

Scintigraphic emptying was signi® cantly slower in pa-

tients with SIBO than in healthy subje cts (P , 0.05,

Mann-Whitne y test).

In the patients with IDDM, 6/10 (60% ) had pro-

longed gastric emptying in both tests and one addi-

tional patient had delayed scintigraphic emptying.

Comparison of emptying in IDDM with emptying in

healthy subje cts showed signi® cantly slower emptying

in IDDM (P , 0.02, Mann-Whitne y test).

Two of the three patients with de layed scinti-

graphic emptying and normal ROM emptying had T50

value s on scintigraphy slightly above normal (T50 5140 and 143 min, respective ly) . Both patients had

SIBO.

DISCUSSION

The present study demonstrate s a signi® cant cor-

relation between two types of gastric emptying: emp-

tying of nondige stible solids (ROMs) and emptying of

dige stible solids. The corre lation was present in

healthy volunte ers and in patients. In both groups the

emptying of ROMs was de layed compared to digest-

ible solids. Women had slower emptying of ROMs

than men. Three patients with de layed solid emptying

at scintigraphy had normal ROM emptying, but two

of these patients had only a mild dysfunction. Our

® ndings are consistent with some previous work (2, 8,

15) , although others did not obse rve any correlation

(3, 4, 7). Therefore , an absence of corre lation be-

tween solid emptying and emptying of ROMs was

thought to be due to de layed onse t of the migrating

motor complex (MMC) (4) as another cause of de-

layed ROM-emptying.

Based on animal experiments, ROMs were be-

lieved to empty in the inte rdigestive state during

antral phase III (16) . This has been used as an expla-

nation for the differences in emptying of solids and

indige stible solids in clinical studies (3, 4, 7, 8, 15) .

However, we have recently observed that gastric emp-

tying of ROMs of the size used in this study occurs

unre lated to gastric phase III of the migrating motor

complex (17) . Thus, it is more like ly that the differ-

ence in reported results depends on methodological

pitfalls. A close corre lation exists between the size of

the ROMs and emptying time both in dogs and hu-

mans. Furthe rmore, gastric emptying of nondige stible

solids is de layed but in linear correlation with emp-

tying of dige stible solids (18, 19) . In contrast, a size-

dependent relation was less clear when cylindric

ROMs were used (20) . However, with this shape the

emptying may be dif® cult to predict and depends

mostly on the orientation of the ROMs in the pylorus.

In a previous study (21) and in the present study (data

not shown) , the emptying rate was almost the same

for cylindric ROMs (8 3 2 3 2 mm) as for cubic

ROMs of 2-mm size. Therefore , ROMs seem to ori-

ent with the smalle st diame ter towards the pylorus,

and this diameter may determine the emptying rate.

Furthe rmore, there is also a close correlation be-

tween the density of ROMs and emptying time (18,

19) . In many previous reports the density of the

ROMs has not been described at all (4, 7, 8, 20) . In

the present study we have determined density, shape ,

and size and have carefully chosen the most suitable

ROMs. Moreover, it is important to determine cor-

rect emptying curves for healthy individuals for the

ROMs to be used in clinics. Since gastric emptying

time varies with the factors discussed above and de-

pends on the composition and caloric content of the

test meal (22± 25) , appropriate reference values have

to be determined whenever any of these factors is

change d. Furthermore , we have also shown that gas-

tric emptying of ROMs is slower in healthy women

than in men. This has previously been shown for

scintigraphic emptying of solids (26) . In a recent

study, a higher sensitivity for identifying de layed gas-

tric emptying was found with ROMs compared to

solid scintigraphic emptying (15) . However, the num-

TABLE 1. COMPARISON OF T50 FOR SCINTIGRAPHIC SOLID GASTRIC

EMPTYING AND GASTRIC EMPTYING OF ROMS FOR 21 PATIENTS

(IDDM, N 5 10 AND SIBO, N 5 11)*

Solid em ptying

ROMs

Norm al Delayed

Normal 8 0

De layed 3 10

*P , 0.001, Fisher’ s exact test.

STOTZER ET AL

732 Digestive Diseases and Sciences, Vol. 44, No. 4 (April 1999)

ber of healthy subje cts in this paper was small, and it

was not corrected for gender, eithe r for solid scinti-

graphic gastric emptying or for gastric emptying of

ROMs.

We have compared the T50 for scintigraphic emp-

tying with the T50 for ROMs and with the number of

ROMs retained at 6 hr. To evaluate whether gastric

emptying is de layed, it seems possible to obtain the

relevant information from one single plain abdominal

x-ray 6 hr after ingestion of the ROMs.

Both patients with IDDM and SIBO had signi® -

cantly delayed gastric emptying in both tests com-

pared to healthy subje cts. Concerning IDDM, this is

not unexpected and is compatible with previous ® nd-

ings in this group of patients (5± 9). The mechanisms

are not well understood but autonomic neuropathy as

well as metabolic factors, eg, hyperglycemia (5), may

contribute . To our knowle dge de layed gastric empty-

ing as a common dysfunction in SIBO has not been

described before . However, motility disorders in the

small bowe l are believed to play a major role in SIBO

(10, 11, 27, 28) . It is not clear whether our ® nding is

just due to a widespread motor disorde r or if de layed

gastric emptying per se can cause SIBO. Possible

mechanisms in the latter case could be a slower ¯ ow

of luminal contents through the juxtapyloral region

and decrease of acidity peaks in this region. It should

be emphasize d that the results concerning gastric

emptying in patients with SIBO are preliminary be-

cause of the limited number of patients participating.

In conclusion, solid gastric emptying measured with

scintigraphy and gastric emptying with ROMs are

distinctive processes but show a high degree of cor-

relation. ROM emptying is proposed as a simple ,

readily available method that can be used to select

patients for furthe r evaluation with scintigraphy. Gas-

tric emptying of ROMs as well as of digestible solids

is slower in women than in men, which necessitate s

gender-speci® c reference values. Patients with SIBO

and IDDM with symptoms have , in a high proportion,

de layed gastric emptying with both methods.

ACKNOWLEDGMENTS

This study was supported by the Swedish Medical Re-search Council (No. 8288), KommunfoÈ rbundet foÈ r VaÈ straGoÈ taland (FoU 56), Jansen-Cilag AB, Sweden, and by theFaculty of Medicine, GoÈ teborg University, Sweden.

REFERENCES

1. Minami H, McCallum RW: The physiology and pathophysiol-

ogy of gastric emptying in humans. Gastroente rology 86:1592±

1610, 1984

2. Bertrand J, Metman E-H, Danquechin Dorval E, Rouleau Ph,

D’Hueppe A, Itti R, Philippe L: EÂ tude du temps d’evacuation

gastrique de repas normaux au moyen de granules radio-

opaques. Applications cliniques et validation. Gastroente rol

Clin Biol 4:770 ± 776, 1980

3. Caballero-Plasencia AM, Muros-Navarro MC, Martin-Ruiz

JL, V ale nzue la-Barranco M, De Los Reyes-Garcia MC,

Vilchez-Joya R, Casado-Caballero FJ, Gil-Extremera B: Gas-

troparesis of digestible and indigestible solids in patients with

insulin-dependent diabetes mellitus or functional dyspepsia.

Dig Dis Sci 39:1409 ± 1415, 1994

4. Chang C-S, Chen G-H, Kao C-H, Wang S-J, Peng S-N, Poon

S-K, Huang C-K: Gastric clearance of radiopaque markers in

non-ulcer dyspepsia patients. Scand J Gastroente rol 31:136 ±

139, 1996

5. Farre ll FJ, Kee ffe EB: Diabetic gastropare sis. Dig Dis 13:291±

300, 1995

6. Fe ldman M, Smith HJ: Effect of cisapride on gastric emptying

of indigestible solids in patients with gastroparesis diabetico-

rum. A comparison with metoclopramide and placebo. Gastro-

enterology 92:171± 174, 1987

7. Tung C-F, Chang C-S, Chen G-H, Kao C-H, Wang S-J: Com-

prehensive gastric emptying study for type-II diabetes me llitus

dyspeptic patients. Scand J Gastroenterol 32:884 ± 887, 1997

8. Fe ldman M, Smith HJ, Simon TR: Gastric emptying of solid

radiopaque markers: Studies in healthy subjects and diabetic

patients. Gastroenterology 87:895± 902, 1984

9. Loo FD, Palme r DW, Soerge l KH, Kalb¯ eisch JH, Wood CM:

Gastric emptying in patients with diabetes mellitus. Gastroen-

terology 86:485± 494, 1984

10. Vantrappen G, Janssens J, He llemans J, Ghoos Y: The inter-

digestive motor complex of normal subjects and patients with

bacte rial overgrowth of the small intestine. J Clin Invest

59:1158 ± 1166, 1977

11. Stotzer P-O, BjoÈ rnsson EB, Abrahamsson H: Interdigestive

and postprandial motility in small intestinal bacte rial over-

growth. Scand J Gastroente rol 31:875± 880, 1996

12. GrybaÈ ck P, NaÈ slund E, HellstroÈ m PM, Jacobsson H, Backman

L: Gastric emptying of solids in humans: Improve d evaluation

by Kaplan-Me ier plots. Eur J Nucl Med 23:1562± 1567, 1996

13. Tothill P, McLoughlin GP, Heading RC: Techniques and er-

rors in scintigraphic measurements of gastric emptying. J Nucl

Med 19:256 ± 261, 1978

14. Kerlin P, Wong L: Breath hydrogen testing in bacte rial over-

growth of the small intestine. Gastroente rology 95:982± 988,

1988

15. Poitras P, Picard M, De ry R, GigueÁ re A, Morais J, Plourde V,

Boivin M: Evaluation of gastric emptying in clinical practice.

Dig Dis Sci 42:2183± 2189, 1997

16. Hinder RA, Ke lly KA: Canine gastric emptying of solids and

liquids. Am J Physiol 233(4):E335± E340, 1977

17. Stotzer P-O , Abrahamsson H: Gastric emptying of non-

digestible solids is not related to antral phase III. Neurogas-

troenterol Motil 10:101, 1998 (abstract)

18. Meyer JH, Dressman J, Fink A, Amidon G: Effect on size and

density on canine gastric emptying of non-digestible solids.

Gastroente rology 89:805± 813, 1985

19. Meyer JH, Eliashoff J, Porter-Fink V, Dressman J, Amidon

GL: Human postprandial gastric emptying of 1± 3 millimeter

spheres. Gastroente rology 94:1315± 1325, 1988

20. Meyer B, Beglinge r C, Neumaye r M, Stalder GA: Physical

ASSESSMENT OF GASTRIC EMPTYING

733Digestive Diseases and Sciences, Vol. 44, No. 4 (April 1999)

characteristics of indigestible solids affect emptying from the

fasting human stomach. Gut 30:1526 ± 1529, 1989

21. Smith HJ, Feldman M: In¯ uence of food and marker length on

gastric emptying of indigestible radiopaque marke rs in healthy

humans. Gastroente rology 91:1452± 1455, 1986

22. Meyer JH, Ohashi H, Jehn D, Thomson JB: Size of liver

particles emptied from the human stomach. Gastroenterology

80:1489 ± 1496, 1981

23. Holt S, Reid J, Taylor TV, Tothill P, Heading RC: Gastric

emptying of solids in man. Gut 23:292± 296, 1982

24. Lin HC, Eliashoff JD, Yo-Guo Gu, Meyer JH: Effect of meal

volume on gastric emptying. J Gastrointest Motil 4:157± 163,

1992

25. Davis SS, Hardy JG, Fara JW: Transit of pharmaceutical

dosage forms through the small intestine. Gut 27:886 ± 892,

1986

26. Hermansson G, Sivertsson R: Gender-re lated differences in

gastric emptying rate of solid meal. Dig Dis Sci 41:1994 ± 1998,

1996

27. Code CF, Schlegel JF: The gastrointestinal interdigestive

housekeeper: Motor corre lates of the interdigestive myoe lec-

tric complex of the dog. In Procee dings from the Fourth

International Symposium on Gastro-Intestinal Motility. Mitch-

ell Press Ltd., Vancouve r, Canada, 1973, pp 631± 634

28. Husebye E, Skar V, Hù ve rstad T, Iversen T, Melby K: Abnor-

mal intestinal motor patterns explain enteric colonization with

gram-negative bacilli in late radiation enteropathy. Gastroen-

terology 109:1078 ± 1089, 1995

STOTZER ET AL

734 Digestive Diseases and Sciences, Vol. 44, No. 4 (April 1999)