Content uploaded by Stine Storsrud
Author content
All content in this area was uploaded by Stine Storsrud on Sep 26, 2014
Content may be subject to copyright.
nature publishing group ORIGINAL CONTRIBUTIONS
STOMACH
1
© 2014 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY
see related editorial on page x
INTRODUCTION
Gastroparesis is de ned as delayed gastric emptying in the absence
of an obstruction to out ow from the stomach ( 1 ), and is a well-
known complication to diabetes mellitus (DM) and occur in both
DM type1 and 2 ( 2,3 ). Diabetic gastroparesis is o en associated
with at least one of following factors: gastrointestinal (GI) symp-
toms, nutrition di culties and / or poor glycemic control including
postprandial hypoglycemia ( 3,4 ). e prevalence of gastroparesis
in patients with DM is uncertain, but is suggested to be present
in 30 – 65 % of outpatients with long standing DM ( 2,3 ). In clinical
practice, the presence of gastroparesis is o en under-recognized,
and therefore its clinical consequences are sometimes not man-
aged in an optimal manner ( 5 ). e pathogenesis of this disabling
condition is probably complex and still not well understood
( 6 ), but it is associated with the presence of diabetic autonomic
neuropathy ( 7 ).
In patients with diabetic gastroparesis it is of importance to opti-
mize the metabolic control, because hyperglycemia per se inhibit
gastric emptying, which may further deteriorate glycemic con-
trol ( 8 ). Coordination of exogenous insulin action with nutrient
delivery to intestine is crucial, as poor coordination may lead to
unstable plasma glucose levels, hyperglycemia and hypoglycemia,
which may result in poor glycemic control ( 9 ). In patients with
delayed gastric emptying the coordination of insulin and nutrient
A Small Particle Size Diet Reduces Upper
Gastrointestinal Symptoms in Patients With Diabetic
Gastroparesis: A Randomized Controlled Trial
Eva A . Olausson , RD, PhD
1 , Stine St ö rsrud , RD, PhD
1 , H å kan Grundin , Ph Mag
2 , Mats Isaksson , PhD
2 , Stig Attvall , MD, PhD
1 and
Magnus Simr é n , MD, PhD
1
OBJECTIVES: Gastroparesis is a well-known complication to diabetes mellitus (DM). Dietary advice is considered
to be of importance to reduce gastrointestinal (GI) symptoms in patients with diabetic gastroparesis,
but no randomized controlled trials exist. Our aim was to compare GI symptoms in insulin treated
DM subjects with gastroparesis eating a diet with small particle size ( “ intervention diet ” ) with the
recommended diet for DM ( “ control diet ” ).
METHODS: 56 subjects with insulin treated DM and gastroparesis were randomized to the intervention diet or
the control diet. The patients received dietary advice by a dietitian at 7 occasions during 20 weeks.
GI symptom severity, nutrient intake and glycemic control were measured before and after the inter-
vention.
RESULTS: A signifi cantly greater reduction of the severity of the key gastroparetic symptoms — nausea / vomiting
( P = 0.01), postprandial fullness ( P = 0.02) and bloating ( P = 0.006) — were seen in patients who
received the intervention diet compared with the control diet, and this was also true for regurgitation /
heartburn ( P = 0.02), but not for abdominal pain. Anxiety was reduced after the intervention diet, but
not after the control diet, whereas no effect on depression or quality of life was noted in any of the
groups. A higher fat intake in the intervention group was noted, but otherwise no differences in body
weight, HbA1c or nutrient intake were seen.
CONCLUSIONS: A small particle diet improves the key symptoms of gastroparesis in patients with diabetes mellitus.
(ClinicalTrials.gov NCT01557296)
Am J Gastroenterol advance online publication, 14 January 2014; doi: 10.1038/ajg.2013.453
1 Department of Internal Medicine and Clinical Nutrition, Institute of Medicine, Sahlgrenska, Academy, University of Gothenburg , Gothenburg , Sweden ;
2 Department of Radiation Physics, Institute of Clinical Science, Sahlgrenska Academy, University of Gothenburg , Gothenburg , Sweden . Correspondence:
Magnus Simr é n, MD, PhD , Department of Internal Medicine & Clinical Nutrition, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg , 41345
Gothenburg , Sweden . E-mail: magnus.simren@medicine.gu.se
Received 15 August 2013; accepted 19 November 2013
The American Journal of GASTROENTEROLOGY VOLUME 104 | XXX 2012 www.amjgastro.com
2
STOMACH
Olausson et al.
delivery to the small intestine is problematic. Based on the well-
known importance of achieving a good metabolic control to pre-
vent diabetic complications ( 10 ), improving the predictability of
this coordination seems important.
Patients with diabetic gastroparesis o en su er from a wide
array of predominantly, but not exclusively, upper GI symptoms.
Of these, abdominal pain ( 11 ), bloating ( 2 ), postprandial fullness
( 2,12 ), early satiety, nausea and vomiting ( 11 ) occur most fre-
quently. e presence of these symptoms contributes to the fact
that many patients with gastroparesis have diets de cient in calo-
ries, vitamins, and minerals ( 8,13 ). e combination of severe GI
symptom, poor metabolic control and nutritional di culties also
impairs the quality of life in these patients ( 14 ). Moreover, patients
with diabetic gastroparesis have been found to require more
healthcare than other groups of patients with DM ( 15 ).
e management of patients with diabetic gastroparesis includes
attempts to improve gastric emptying, relieve GI symptoms, and
improve glycemic control and the nutritional state. e pharma-
cologic treatment options include mainly the use of prokinetic and
antiemetic drugs. e rst choice of treatment in patients with dia-
betic gastroparesis is most o en dietary advice. However, to the
best of our knowledge there are no randomized controlled trials
assessing the e ect of dietary interventions in diabetic gastropare-
sis. Current dietary recommendations for patients with gas-
troparesis include suggestions derived from an empirical approach
that compensate for the impairment of gastric emptying by con-
suming foods that are low in fat and ber, as it is well established
that these nutrients delay gastric emptying ( 16 ). To maintain the
energy intake at an acceptable level the recommendation suggests
small, frequent meals ( 17,18 ). In a previous study we compared
the gastric emptying rate with two di erent meals based on the
same caloric content and food composition, but with di erences
in particle size between the meals. e gastric emptying rate of a
meal with large particle size was clearly di erent between patients
with diabetic gastroparesis and healthy control subjects, whereas
the emptying rate of a meal with small particle size was more simi-
lar (no signi cant di erence) between subjects with diabetes and
gastroparesis and healthy subjects ( 19 ).
erefore, the aim of this study was to compare the e ects of a die-
tary intervention recommending meals with small particle size with
the standard dietary recommendations to patients with DM ( 20 ),
in insulin treated diabetic subjects with gastroparesis. Our primary
goal was to improve GI symptoms associated with gastroparesis,
and the secondary goal to assess e ects on body weight, nutritional
intake, metabolic control, mental health and quality of life.
METHODS
Subjects
For participation in this 20-weeks parallel group, dietary interven-
tion trial, we evaluated patients with insulin treated DM between
18 and 70 years, and with a clinical suspicion of gastroparesis,
based on the presence of upper GI symptoms and / or unsta-
ble plasma glucose. In order to be included, the patients had to
demonstrate delayed gastric scintigraphic emptying (see below),
and no evidence of mechanical obstruction, i.e. ful lling the de -
nition of gastroparesis. e subject should be able to understand
verbal and written information and complete questionnaires in
Swedish. Exclusion criteria were: previous GI surgery except
appendectomy, severe psychiatric disease, sequelae a er cerebrov-
ascular disease, serum creatinine > 150 μ mol / l, and untreated dis-
ease with a potential impact on gastric emptying or GI symptoms.
In order to exclude mechanical obstruction or another GI expla-
nation behind the upper GI symptoms, all patients had to have
been investigated with upper GI endoscopy within one year prior
to inclusion in the study. Clinical characteristics of the subjects
were obtained from chart review.
is study was approved by the Regional Ethical Review Board
at the University of Gothenburg, Gothenburg, Sweden. Each par-
ticipant was verbally informed about the study and was given writ-
ten information, and prior to any study related procedure they
gave written informed consent.
Gastric scintigraphy
e gastric emptying rate was measured with gastric scintigraphy
according to a nationwide standard method ( 21,22 ). Reference
values for solid gastric emptying have been established in a study
of 160 healthy subjects (69 males, 91 females), and for men the
normal range for retention of the radioactivity in the stomach at
120 min a er the nished meal (R
120 ) is 0 – 51 % , for women < 50
years old, 9 – 66 % , and for women > 50 years old 0 – 55 % ( 22 ). As
hyperglycemia per se delays gastric emptying ( 23 ), plasma glucose
at the beginning of the gastric scintigraphy had to be ≤ 10 mmol / l.
Questionnaires
Severity of GI symptoms. e subjects were asked to complete
the validated questionnaire, Patient Assessment of Gastrointesti-
nal Disorders-Symptom Severity Index (PAGI-SYM) to assess GI
symptom severity during the preceding 2 weeks ( 24 ). e 20-item
PAGI-SYM includes 6 subscales: nausea / vomiting, fullness / early
satiety, bloating, upper abdominal pain, lower abdominal pain
and heartburn / regurgitation analyzed on a 6-point Likert scale
ranging from 0 (no symptoms), 1 (very mild), 2 (mild), 3 (moder-
ate), 4 (severe) to 5 (very severe symptoms). is instrument has
undergone thorough validation procedures and has been found
to be construct valid, reliable and responsive to changes in pa-
tients with upper GI disorders ( 25 ) and has been found to be con-
struct valid and reliable in gastroparesis ( 24 ). Furthermore, a sub-
set of this scale, the nine-item Gastroparesis Cardinal Symptom
Index (GCSI) consisting of the three subscales nausea / vomiting,
fullness / early satiety and bloating, has been validated in patients
with gastroparesis ( 26,27 ).
Anxiety and depression. e severity of anxiety and depression
were determined with the self-reporting questionnaire, Hospital
Anxiety and Depression Scale (HADS) ( 28 ). e HADS contains
14 items, 7 items on depression and 7 items on anxiety. Patients
score to the extend they agree with each statement on a 4-point
scale, ranging from 0 to 3. Cut o points for severity in each do-
main are scores: 0 – 7 = normal; 8 – 10 = mild; 11 – 14 = moderate;
© 2014 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY
3
STOMACH
A Small Particle Size Diet in Diabetic Gastroparesis
and 15 – 21 = severe. A score of 8 or above is considered abnormal.
e HADS questionnaire has been reported to have good valid-
ity in diabetic subjects ( 29 ). Factor structure, discriminant validity
and internal consistency were studied in a review paper, and the
authors found that the sensitivity and speci city for detecting
anxiety and depression were 0.80 ( 30 ).
Quality of life. e quality of life was determined with the widely used
generic questionnaire the 36-item Short-Form Health Survey (SF-36)
( 31,32 ). e Swedish translation has also been thoroughly validated
( 33 ). SF-36 consists of eight di erent domains, and these can be sum-
marized in a physical component summary (PCS): physical function-
ing, role physical, bodily pain and general health; and a mental com-
ponent summary (MCS): vitality, social functioning, role emotional
and mental health. e highest possible score is 100, where no limita-
tions or disabilities are reported, and the lowest score possible is zero,
where the greatest degree of limitation or disability is reported.
Dietary intake, nutrition and glycemic control
A dietitian (EO) trained all the subjects in completing a 4-day
food diary at home. Dietary recordings were performed during
one day during the weekend and 3 days during weekdays. e
amount of all food and beverages were recorded in weight and
household measures. e dietitian interviewed each subject and
any ambiguities were resolved upon return of the food records.
e same dietitian calculated the nutrient content in all dietary
records from the Database Swedish National Food Composition
Tables, 11th of April 2007 (National Food Agency, Uppsala, Swe-
den) using the computer program Dietist XP version 3.2, (Diet
and Nutrition Data, Bromma, Sweden). For this study, the caloric
content (kcal), and the amount of protein, fat, carbohydrates and
ber (all in grams) were used.
Body weight was recorded in underwear clothing and without
shoes to the nearest 0.1 kg on calibrated, electronic scales (Serial
no 11087, system 31, Advanced weighing Co Ltd, New Haven, East
Sussex, BN9 0DU, UK). Height was measured in standing position
to the nearest 0.5 cm. Body mass index (BMI) was calculated as
weight (kg) divided by height squared (m
2 ) (kg / m 2 ).
Blood samples were collected for the analyses of glycosylated
hemoglobin (HbA1c). e analyses were conducted at an
accredited reference laboratory (Clinical Chemistry laboratory,
Sahlgrenska University Hospital, Gothenburg, Sweden) accord-
ing to the ISO / IEC 15 189 Standard for Medical Laboratories.
HbA1c were converted to the Diabetes Control and Complica-
tions Trial (DCCT), standard levels using the formula: HbA1c
(DCCT) = (0.923 × HbA1c (MonoS) + 1.345; R 2 = 0.998) ( 34 ).
Study design
Subjects with insulin treated DM and suspected gastroparesis
were asked if they were willing to participate in this study. If a
diagnosis of diabetic gastroparesis was con rmed with scintig-
raphy, and the patient agreed to participate in the study, he / she
was further evaluated at the randomization visit where a dietitian
(EO) instructed the subject how to complete the questionnaires;
PAGI-SYM, HADS and SF36 and how to complete 4-days dietary
food record — the food record was completed at home, the other
questionnaires were completed at the hospital at baseline. At the
same occasion body weight, height and a blood sample for the
analysis of HbA1c were taken. If the patient met all the inclusion
criteria, and had no exclusion criteria, he / she was randomized
to one of the two dietary treatment groups (see below) by draw-
ing envelopes. Moreover, the patient was also randomized to be
treated by one of two dietitians (EO or SS). During the study, each
patient received dietary advice from the same dietitian at seven
outpatient visits (each lasting approximately 45 – 60 min) during
20 weeks. Both dietitians followed the same written instructions
on how to give dietary advice to the patients in the two treatment
groups (see Appendices ). e time interval between the rst three
visits was 2 weeks, between visits 4 – 7 the interval was 3 weeks,
and the nal visit (visit 8) occurred 4 weeks a er visit 7, i.e. 20
weeks a er the randomization visit.
Before the nal visit, the patients had completed the ques-
tionnaires PAGI-SYM, HADS, SF36 and a 4-days dietary record
at home, and these were collected by one dietitian (EO). At this
visit the body weight, height, gastric emptying and blood sample,
HbA1c, were measured again.
Diets
e patients were randomized to receive dietary advice, which
di ered regarding the particle size of the food (for more detailed
information, see Appendices ). Otherwise the nutritional compo-
sition in the two dietary treatment groups was the same. Except
recommending the fat content to be reduced to 25 – 30 % of total
energy and the ber content to 15 gram / 1,000 kcal, in order to
be in line with the earlier study ( 19 ) and with the current rec-
ommendations for patients with gastroparesis ( 16 ), the diet was
in accordance with the recommended diet in diabetes ( 20 ). Both
groups were advised to have the same meal scheme; breakfast,
snack, lunch, snack, dinner and evening snack, and received die-
tary counseling on 7 occasions.
Intervention diet. is group received advice to eat foods with
small particle size or food items that could easily be processed into
small particle size ( Appendix 1 ). A characteristic feature of the in-
tervention diet was that “ the food should be easy to mash with a
fork into small particle size, e.g. mealy potatoes ” . erefore, this
diet excludes foods with the following characteristics: foods with
husks / peels (e.g. corn, peas, tomato, sprouts, onions, cabbage),
membranes (e.g. orange, lemons and grapefruit), stringy foods
(e.g. rhubarb, asparagus, leeks, stalks of broccoli and cauli ower),
seeds and grains (e.g. nuts and almonds, bread with whole grains),
compact, poorly digestible particles (such as pasta, rice, grated veg-
etables, meat, raw vegetable salad and cheese slices) and white fresh
bread. However, if e.g. corn, peas and onion have been mixed in a
food processor to a similar consistency as mashed potato, these
were allowed in the intervention diet, and food items like almonds
and nuts could be included if they had been ground into our.
Control diet. is group received advice to eat the food usually
recommended for patients with diabetes ( 20 ), and allowed foods
The American Journal of GASTROENTEROLOGY VOLUME 104 | XXX 2012 www.amjgastro.com
4
STOMACH
Olausson et al.
with large particle size and the food items should have a low
glycemic index ( 35 ) ( Appendix 2 ). Examples of food items with
large particle size are whole meat, seafood, cheese slices, almonds
and nuts. Examples of foods with low glycemic index are pasta,
rice, grated vegetables, raw vegetable salad, wok vegetables, fresh
fruit and bread with whole grain and / or sourdough. is diet
does not contain foods with small particle size, e.g. milkshakes,
berry and fruit compote, mashed potato, smooth soups and
mashed turnips.
Data analysis and statistics
e patients were randomized into two groups, one who received
advice to eat the intervention diet with food with small particle
size, and a group who were advised to eat the control diet, i.e. the
diet with large particle size and similar to the standard diet recom-
mended for diabetes, but adapted for patients with gastroparesis.
ese two groups were then used for within- and between-group
comparisons. SPSS version 18.0 for Windows (SPSS, Inc.,
Chicago, IL) was used for statistical analyses. We performed the
analyses on an intention-to-treat population, i.e. all patients who
were randomized were included in the analyses. In case of pre-
mature drop-out, missing data were imputed from the previous
assessment using the last observation carried forward technique,
and included in the analysis. e changes at the last visit relative to
baseline in the three PAGI-SYM subscales that constitute the Gas-
troparesis Cardinal Symptom Index (GCSI), i.e. nausea / vomiting,
fullness / early satiety and bloating, were our primary outcome
variables (between-groups comparisons), as these are considered
to be the key GI symptoms of gastroparesis. Changes in the other
PAGI-SYM domains, gastric emptying ( % retention at 120 min),
quality of life (SF-36), psychological symptom severity (HADS),
body weight, nutritional intake and glycemic control (HbA1c)
were secondary outcome variables. A sample size calculation
was performed, and in order to be able to detect a di erence in
the change of our primary outcome variables of 0.8 between the
treatment groups with 80 % power at α = 0.05, assuming a SD of 1,
at least 50 subjects with evaluable data were needed. Besides the
between-group comparisons of changes in the outcome variables,
we also performed within-group comparisons of the same varia-
bles. Moreover the associations between gastric emptying data and
change in symptoms were measured in the two treatment groups.
e demographic characteristics of the patients are presented
as mean ± s.d. and median (range), and were compared between
the groups using the Mann-Whitney U test. e outcome vari-
ables at baseline and a er the treatment period in the two groups
are shown as mean ± s.d. and for the majority of parameters
also as median (range). For comparisons within the groups the
Wilcoxon Signed Rank test was used, whereas comparisons
between the groups for outcome variables were made using
Analysis of Covariance (ANCOVA) adjusting for baseline val-
ues. Correlations were measured using Spearman ’ s rank correla-
tion coe cients. e between-group di erences in changes in the
outcome variables are shown as mean and 95 % CI. Two-tailed
P values < 0.05 were accepted as statistically signi cant. No correc-
tions for multiple comparisons were performed.
RESULTS
Patients
Diabetic patients with insulin treated diabetes and delayed gastric
emptying were recruited from hospital and primary care outpa-
tient clinics in the western region of Sweden during the period
of August 2007-August 2011. Eighty-three diabetic subjects with
insulin treated diabetes and suspected gastroparesis were asked to
participate in the study ( Figure 1 ). Eleven of these were not willing
to take part, leaving 72 subjects who were willing to be screened
for eligibility and to be investigated with gastric scintigraphy.
Normal gastric emptying was found in 14 subjects, and 2 patients
with gastroparesis declined to take part in the dietary interven-
tion part, leaving 56 subjects (36 women) who were randomized
to the treatment groups. irty-six of the randomized patients
had diabetes type 1 (22 intervention diet, 14 control, diet), eight-
een subjects had diabetes type 2 (5 intervention diet, 13 control
diet), one subject had Latent Autoimmune Diabetes in the Adult
(LADA) diabetes (intervention diet) and one subject had Maturity
Onset Diabetes in Young (MODY) diabetes (control diet), with a
signi cant di erence in the distribution of diabetes type 1 and 2
between the diet groups ( P = 0.02). Only one patient used a proki-
netic agent during the study, and the dose was unchanged. Demo-
graphic and clinical characteristics of the randomized patients are
presented in Table 1 , and no signi cant di erences between the
groups in any of these variables were detected.
During the treatment phase, one patient died of myocardial inf-
arction in the intervention group in the 20th week of the study,
and ve patients ended prematurely in the control group because
of worsening of existing upper GI symptoms ( n = 3), occurrence of
new GI symptoms ( n = 1 ; a er a visit to Africa) or without any spe-
ci c reason mentioned ( n = 1). ese missing data were imputed
from the previous assessment (baseline), using the last observa-
tion carried forward technique, and included in the analysis. All
patients who completed the trial expressed adherence with dietary
treatment (verbal reports as well as food diaries) and considered
the dietary changes to be feasible.
Gastrointestinal symptoms, anxiety, depression and quality of
life
All GI symptoms, except for upper abdominal pain, improved
signi cantly (lower PAGI-SYM scores) a er the intervention diet
( Figure 2a ), whereas none of the GI symptoms improved a er
the control diet ( Figure 2b ). e severity of the primary outcome
variables were all signi cantly more improved a er the inter-
vention diet than a er the control diet; nausea / vomiting ( − 0.56
( − 1.01 to − 0.11) (mean change di erence (95 % CI); P = 0.01),
fullness / early satiety ( − 0.61 ( − 1.14 to − 0.08); P = 0.02) and
bloating ( − 0.86 ( − 1.48 to − 0.25); P = 0.006). Also regurgitation /
heartburn was more improved a er the intervention diet than
a er the control diet ( − 0.51 ( − 0.94 to − 0.07); P = 0.02), whereas
no group di erences were noted for upper ( − 0.36 ( − 1.01 – 0.28);
P = 0.27) or lower abdominal pain ( − 0.50 ( − 1.15 – 0.14); P = 0.12).
e change in symptom severity did not di er between patients
with diabetes type 1 and 2 in any of the groups ( P = 0.37 – 0.95 for
the primary outcome variables).
© 2014 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY
5
STOMACH
A Small Particle Size Diet in Diabetic Gastroparesis
total intake of calories, ber, carbohydrates and protein remained
unchanged in both groups without any between-group di er-
ences. No major group di erences were noted for dietary patterns
or balance between intakes during meals or snacks (food diaries
and verbal reports). No di erences were seen between or within
the groups regarding body weight or metabolic control (HbA1c).
In both groups, gastric emptying ( % retention at 120 min) was
improved a er the treatment period relative to baseline, and this
change was signi cantly greater in the intervention group com-
pared with the control group ( Tab l e 2 ). However, the change in
gastric emptying rate at follow-up was not signi cantly associated
with the change in symptom severity measured by PAGI-SYM
(data not shown). Gastric emptying rate at baseline in the inter-
vention group tended to be negatively associated with the change
in symptoms a er treatment, which reached statistical signi cance
e severity of anxiety (HADS) was reduced in the intervention
diet group, but not in the control diet group a er the treatment
period. However, the between-group comparison of change in
anxiety score was not signi cant ( Table 2 ). Depression (HADS)
and quality of life (mental and physical component summary of
SF-36) remained unchanged in both groups and no between-group
di erences were noted ( Ta bl e 2 ).
Dietary intake, nutrition, gastric emptying and glycemic
control
e intake of fat changed signi cantly more in the intervention
group than in the control group, with a greater increase in the
intervention group at study completion ( Table 2 ). e fat intake
increased signi cantly in the intervention diet group, but not in
the control diet group, whereas within-group comparisons for
83 asked to participate in the study
11 not willing
to participate
2 with gastroparesis,
not willing to particpate
72 screened
14 normal gastric
emptying
56 randomized
28 control
5 drop-outs
↑ Gl
symptoms
(n=4)
No
specific
reason
(n=1)
•
•
28 intervention
1 death (MI)
27 completed the study
28 included in final analyses
23 completed the study
28 included in final analyses
Figure 1 . Flow chart demonstrating the number of patients in the different phases of the study.
Table 1 . Demographic and clinical characteristics of subjects with insulin-treated diabetes and gastroparesis presented as mean ± s.d. and
median (range)
Age, years
Duration of
diabetes,
years
Insulin-
treated,
years
Insulin / kg
body
weight, U Body weight, kg BMI, kg / m
2
S-creatinine
μ mol / l
GFR, ml /
min / 1.73 m
2
R
120
, % R
180
, %
Intervention
diet, n =28
51.5 ± 11.7 28.2 ± 14.8 23.7 ± 15.8 0.6 ± 0.3 77.9 ± 16.0 25.6 ± 4.7 82.2 ± 20.5 80.0 ± 18.8 77.1 ± 9.8 57.8 ± ± 16.4
51 (31 – 69) 28.0
(2.0 – 65.0)
28 (4 – 46) 0.5
(0.3 – 1.7)
74.6
(52.3 − 110.3)
25.0
(20.1 – 40.9)
76.5
(55 – 138)
82.5
(40 – 126)
79.5
(53 – 91)
61
(18 – 81)
Diabetes
diet, n =28
55.0 ± 11.4 23.6 ± 15.6
21.6 ± 17.4 0.7 ± 0.5 78.4 ± 15.8 27.7 ± 4.9 72.2 ± 12.3 82.7 ± 19.2 74.7 ± 12.9 59.9 ± 19.75
54.5
(27 – 69)
18.0
(2.0 – 64.0)
16 (1 – 63) 0.5
(0.2 – 2.2)
80.8
(54.6 − 114.4)
28.4
(18.4 – 36.0)
74.0
(54 – 100)
86 (48 – 128) 72.5
(55 – 94)
55.5
(31 – 91)
GFR, glomerular fi ltration rate; R
120 , retention of the radioactivity in the stomach 120 min after meal intake (gastric scintigraphy); R
180 =Retention of the radioactivity in the
stomach 180 min after meal intake (gastric scintigraphy).
The American Journal of GASTROENTEROLOGY VOLUME 104 | XXX 2012 www.amjgastro.com
6
STOMACH
Olausson et al.
only for upper abdominal pain (rho = − 0.39; P = 0.04), i.e. patients
with greater symptom improvement tended to have less severely
a ected gastric emptying at baseline, whereas no such associations
were noted in the control group (data not shown).
DISCUSSION
In the present study we have demonstrated in a randomized con-
trolled trial that a small particle size diet substantially improved
the upper GI symptoms considered to be the key symptoms
of gastroparesis — nausea / vomiting, postprandial fullness, early
satiety and bloating ( 2,6 ) — in patients with diabetic gastroparesis.
Moreover, there was also an e ect of this intervention diet on
other GI symptoms, but no major e ect could be detected on
nutrient intake or glycemic control a er 20 weeks on the small
particle diet relative to a diet normally recommended to patients
with DM.
Patients with diabetic gastroparesis o en complain of severe
upper GI symptoms and poor glycemic control. Moreover, the
severity of the upper GI symptoms is associated with reduced
quality of life ( 36 ), and may lead to inadequate nutrient intake
( 8,13 ). e treatment options are limited, but dietary modi ca-
tions are considered to be of great importance, despite the fact that
no randomized controlled trials exist. erefore, our study is of
clinical importance, as we were able to demonstrate that advising
patients with diabetic gastroparesis to eat a diet with small particle
size signi cantly improved upper GI symptoms, whereas no such
e ect was seen when patients were advised to eat a diet normally
recommended to patients with DM, modi ed based on dietary
recommendations for gastroparesis.
Traditionally, patients with gastroparesis are recommended to
eat small, low-fat, low- ber meals 4 – 5 times per day ( 16 ), based
on the fact that meal volume, and the content of calories, fat and
bre a ects gastric emptying ( 19,37 ). However, in a recently pub-
lished small experimental study, we demonstrated that a solid
meal with small particle size increased the gastric emptying rate in
patients with diabetic gastroparesis ( 19 ). Based on this nding, we
hypothesized that a diet with small particle size would improve GI
symptoms in diabetic gastroparesis, as GI symptom severity is
associated with the degree of gastric emptying, albeit modestly
( 21 ). is hypothesis could be con rmed in the present study,
which should have implications for dietary advice to patients with
diabetic gastroparesis in clinical practice.
e proximal stomach serves as reservoir for food and the
distal stomach as the grinder. A er food ingestion there is a neu-
rally mediated relaxation of the proximal stomach and when
the food enters the stomach the process of accommodation is
enhanced, which allows ingestion of food without generation of
discomfort ( 38 ). Solids are initially retained in the stomach and
undergo churning, while antral contractions propel particles
towards the closed pylorus. Food particles are emptied once their
size have been reduced to approximately 2 mm in diameter ( 37 ).
erefore, we focused our attention on food particle size when
we developed the intervention diet tested in this trial. Moreover,
as phase III of the migrating motor complex is of importance for
gastric emptying of larger particles ( 39 ), and absence of phase
III has been associated with gastroparesis, food items with large
particle size were excluded from the intervention diet ( 40 ).
erefore, based on physiology and pathophysiology of diabetic
gastroparesis, reducing particle size of the diet seems logical.
In our previous study we also demonstrated that a small par-
ticle size diet increased the late postprandial glycemic response
and reduced the postprandial blood glucose dip in patients with
diabetic gastroparesis ( 19 ). erefore, we also hypothesized that
treatment with a small particle size diet would improve the meta-
bolic control in patients with DM and gastroparesis. However, this
was not con rmed in the present study. A potential explanation for
this may be that the study duration of 20 weeks was not su cient
to alter the metabolic control. erefore, studies of longer duration
are needed to further evaluate the e ect of this diet on long-term
glycemic control. Moreover, no major e ect on dietary intake was
noted, nor on body weight, except for a tendency toward higher fat
0
**
**
**
*** *
N/V Fullness Bloating U abd pain L abd pain H/R
Baseline Follow-up
1
2
PAGI-SYM scores
3
4
5
0
N/V Fullness Bloating U abd pain L abd pain H/R
Baseline Follow-up
1
2
PAGI-SYM scores
3
4
5
Figure 2 . GI symptom severity, as measured with PAGI-SYM, at base-
line and after the dietary treatment period (20 weeks) in the group who
received advice to eat the intervention diet (small particle size) ( a ) and
the group who were instructed to follow the control diet ( b ). The between-
group comparisons demonstrated signifi cantly greater symptom improve-
ment in the intervention diet group than in the control group for the primary
outcome variables, nausea / vomiting ( P = 0.01) , fullness / early satiety
( P = 0.02) and bloating ( P = 0.006), and also for heartburn / regurgitation
( P = 0.02). * P < 0.05, * * P < 0.01, * * * P < 0.001 vs. baseline — within-group
comparisons. PAGI-SYM domains: N / V, nausea / vomiting; Fullness,
fullness / early satiety; U / L abd pain , Upper / Lower Abdominal Pain;
H / R, Heartburn / regurgitation.
© 2014 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY
7
STOMACH
A Small Particle Size Diet in Diabetic Gastroparesis
In patients with diabetes, the presence of GI symptoms is asso-
ciated with psychological distress and reduced quality of life
( 41,42 ). Improvement of GI symptoms in patients with diabetic
intake in the intervention group. Again, the study duration may
have been too short for subjects to change their diet substantially
to increase nutrient intake and weight.
Table 2 . Variable at baseline and at fi nished 20 weeks study period grouped in intervention and control group, mean ± s.d., median (range)
Intervention diet, n =28 Diabetes diet, n =28
Base line
mean ±
s.d. median
(range)
Finished study
mean ± s.d.
median (range)
Change mean ±
s.d. median
(range) P value
Base line
mean ± s.d.
median (range)
Finished
study mean ±
s.d. median
(range)
Change mean ±
s.d. median
(range)
P
value
P value
I / D diet
Differential
change mean,
95 % CI
Body weight,
kg
78.4 ± 16.3 77.9 ± 16.0 − 0.5 ± 3.6 NS 79.0 ± 15.6 78.5 ± 15.8
− 0.5 ± 2.2 NS 0.99 − 0.012
( − 1.6 to 1.6)
75.5
(54 to 112.4)
74.7
(52.3 to 110.3)
0.6
( − 13.9 to 3.9)
82.0
(54.5 to 111.0)
80.8
(54.6 to
114.4)
− 0.7
( − 5.0 to 3.8)
kcal 1,505 ± 462 1,585 ± 483.1 80 ± 385.0 NS 1,551 ± 423.1 1,454 ± 319 − 97 ± 417.9 NS 0.096 154 (28 to 336)
1,480
(840 to 2,893)
1,507
(771 to 3,058)
108
( − 555 to 921)
1,574
(897 to 2,893)
1,469
(708 to 2,153)
0
( − 1392 to 488)
Protein, g 65 ± 21.7 67 ± 17.9 1 ± 23.6 NS 69 ± 19.6 65 ± 14.0 − 5 ± 20.9 NS 0.38 5 ( − 6 to 15)
61
(33 to 127)
65 (41 to 118) 0
( − 63 to 55)
66 (39 to 127) 65 (39 to 92) 4
( − 83 to 25)
Fat, g 60 ± 25.8 67 ± 27.6 7 ± 21.9 NS 62 ± 23.9 57 ± 13.1 − 5 ± 22.6 NS 0.034 11 (1 to 20)
55
(31 to 142)
62 (28 to 162)
4
( − 58 to 49)
58 (29 to 142) 55 (27 to 82) 0
( − 70 to 24)
Carbohy-
drate, g
163 ± 48.9 166 ± 51.0 3 ± 48.3 NS 162 ± 44.8 149 ± 47.7 − 13 ± 50.0 NS 0.17 16 ( − 7 to 40)
160
(78 to 269)
166 (79 to 268) 3
( − 86 to 113)
153 (83 to 278) 141
(64 to 253)
2
( − 134 to 69)
Fiber, g 17 ± 6.3 16 ± 5.5 − 1 ± 6.7 NS 17 ± 6.2 17 ±
7.5 0 ± 6.0 NS 0.53 − 1 ( − 4 to 2)
15 (7 to 34) 15 (9 to 33) − 1
( − 21 to 11)
18 (7 to 33) 16 (7 to 38) 0
( − 13 to 12)
HbA1c, % 7.4 ± 0.8 7.4 ± 0.8 − 0.0 ± 0.5 NS 7.9 ± 1.2 7.8 ± 1.1 − 0.2 ± 0.6 NS 0.98 − 0.0
( − 0.3 to 0.3)
7.3
(5.6 to 9.2)
7.3 (5.2 to
9.01)
0.0
( − 1.2 to 0.9)
8.1 (5.4 to 9.8) 7.9
(5.7 to 10.5)
0.0
( − 1.3 to 0.7)
HADS, anxiety 7.8 ± 4.3 S 6.5 ± 4.7 − 1.3 ± 2.7 0.024 7.2 ± 4.6 6.4 ± 4.4 − 0.8 ± 3.4 NS 0.63 − 0.4
8.0 (0 to 18) 6.0 (0 to 21) − 2.0
( − 5.0 to 4.0)
7.0 (1 to 17) 6.5 (1 to 21) 0.0
( − 10.0 to 5.0)
HADS,
depression
6.3 ± 4.9 5.6 ± 5.4 − 0.6 ± 2.5 NS 6.6 ± 4.6 5.9 ± 4.8 − 0.7 ± 4.2 NS
0.99 − 0.0
( − 1.8 to 1.8)
4.5 (0 – 17) 3.5 (0 – 21) 0.5
( − 8.0 to 4.0)
5.0 (1 to 19) 5.0 (0 to 21) 0.0
( − 12.0 to 8.0)
SF-36: PCS 39.0 ± 11.4 40.2 ± 10.9 1.2 ± 8.0 NS 37.6 ± 12.0 35.5 ± 12.8 − 2.1 ± 9.2 NS 0.11 3.6 ( − 0.8 to 8.0)
39.2
(7.4 to 55.3)
39.4
(19.4 to 59.5)
0.9
( − 18.3 to 20.3)
37.4
(13.1 to 55.3)
32.9
(8.7 to 55.5)
− 1.2
( − 21.9 to 16.7)
SF-36: MCS 41.5 ± 15.9 43.8 ± 15.2 2.3 ± 15.0 NS 42.1 ± 13.3 41.5 ± 14.8 − 0.5 ± 10.9 NS 0.48 2.6 ( − 3.8 to 9.0)
39.9
(10.5 to 71.0)
47.3
(9.7 to 62.2)
2.8
( − 50.4 to 26.6)
46.8
(7.5 to 56.6)
42.0
(8.9 to 66.1)
0.6
( − 32.0 to 20.4
Gastric
retention at
2 h ( % )
77.1 ± 9.8 61.2 ± 14.5 15.3 ± 14.4 < 0.0001 74.7 ± 12.9 69.5 ± 14.5 5.2 ± 8.1 0.02 0.002 9.4 (3.7 to 15.0)
79.5
(53 to 91)
64 (36 to 87) 17
( − 10 to 44)
72.5 (55 to 94) 69.0
(41 to 93)
5.5
( − 6 to 26)
BMI, body mass index; HbA1c, glycosylated hemoglobin; HADS, Hospital Anxiety and Depression Scale; NS, nonsignifi cant; PAGI-SYM, Patient Assessment Of Upper
Gastrointestinal Symptom Severity Index; SF-36, the Short-Form Health Status Survey; PCS, physical component summary; MCS, mental component summary.
The variables change within the group and between the groups; mean, 95 % confi dence interval. P < 0.05.
The American Journal of GASTROENTEROLOGY VOLUME 104 | XXX 2012 www.amjgastro.com
8
STOMACH
Olausson et al.
gastroparesis therefore has the potential to reduce psychological
distress and improve quality of life. However, in our trial only a sig-
ni cant positive within-group e ect on anxiety in the group with
the small particle size diet was observed, but with no signi cant
between-group di erences. Moreover no e ects on depression or
quality of life measures were noted in any of the groups. Quality
of life in patients with DM is complex and certainly in uenced
by several factors ( 43 ), and so is probably psychological distress.
In our group of patients with diabetic gastroparesis, not only GI
symptoms severity has the potential to negatively in uence quality
of life, as diabetic gastroparesis is associated with other late dia-
betic complications ( 44 ). erefore, it may not be surprising that
we failed to nd a major e ect on psychological distress or quality
of life with our dietary intervention. e duration of the study may
also be too short to fully appreciate the e ect of a dietary change on
general well-being. Moreover, our study was powered to detect an
e ect on upper GI symptoms, and not on these measures. Future
studies with longer duration and larger sample size may be needed
in order to fully address the e ect of this dietary intervention on
quality of life and psychological distress.
ere are of course limitations with our study. e duration of
the study was 20 weeks, which for some of the parameters meas-
ured may be too short. Moreover, stratifying patients based on
their gastric emptying response to a small particle meal at base-
line could theoretically have enhanced our e ect on symptoms, i.e.
only include patients where small particle size meal clearly a ected
the emptying rate from the stomach. A tendency towards a bet-
ter symptomatic response to the small particle size diet in patients
with less severe delay in gastric emptying at baseline was indeed
observed, but this association was modest, and not of su cient
strength to be clinically useful to choose patients for this therapy.
Moreover, the gastric emptying rate, measured with standard gas-
tric scintigraphy, which improved somewhat in both groups at
follow-up, tended to improve more a er 20 weeks with the small
particle size diet than in the control group, but this was not related
to the improvement in symptoms. erefore, symptom improve-
ment is probably more related to the direct e ect of the meal,
rather than via a permanent e ect of the diet on gastric emptying /
motility. Another potential problem is recall bias when reporting
symptoms, as we asked for symptom severity during the preceding
two weeks rather than using a daily diary. Further, the patients we
included were seen at a secondary / tertiary care center and several
of them had severe diabetes with multiple complications, so these
ndings may not be generalized to a less severely a ected group of
patients with diabetes and gastroparesis. ere was also an imbal-
ance in the distribution of diabetes type 1 and 2 in the treatment
groups, but as the symptomatic response did not di er between
patients with diabetes type 1 and 2, this imbalance is unlikely to
explain the positive e ect of the small particle size diet.
To conclude, in this randomized, controlled trial, we have dem-
onstrated that a diet with small particle size improves the key upper
GI symptoms of gastroparesis in patients with diabetes mellitus. is
should be incorporated in dietary advice given to patients with diabetic
gastroparesis. However, the e ect of this diet on nutrient intake, glyc-
emic control and quality of life in the long term needs further studies.
ACKNOWLEDGMENTS
e authors would like to express their gratitude to Nils-Gunnar
Pehrsson and Mattias Molin, Statistical Consulting Group AB, SE-
413 19 Gothenburg for statistical advice.
CONFLICT OF INTEREST
Guarantor of the article: Magnus Simr é n, MD, PhD.
Speci c author contributions: E.A.O., S.A., and M.S. designed the
study. E.A.O. and S.S. gave dietary advice. M.I. and H.G. analyzed
the gastric scintigraphies. E.A.O. and M.S. analyzed the data. E.A.O.,
S.A. and M.S. dra ed the manuscript, E.A.O., S.A. and M.S. provided
funding for the study. All co-authors critically revised the manuscript.
Financial support: M.S. has received support from the Swed-
ish Medical Research Council (grants 13409, 21691 and 21692),
the Marianne and Marcus Wallenberg Foundation, the Centre for
Person-Centred Care (GPCC), Sahlgrenska Academy, University of
Gothenburg and by the Faculty of Medicine, University of Gothen-
burg. E.A.O. has received research support from Swedish Nutrition
Foundation, Lund, the V ä stra G ö taland Region, Sahlgrenska Univer-
sity Hospital Foundations, the Diabetes Association in Gothenburg
and sponsorship for the cuvettes for analysis of plasma glucose from
Hemocue AB, Ä ngelholm.
Potential competing interest: Magnus Simr é n has received unre-
stricted research grants from Danone, Arla Foods and AstraZeneca,
and served as a Consultant / Advisory Board member for Danone,
Novartis, Almirall, and Shire / Movetis. No other con icts of interest
relevant to this article were reported.
Study Highlights
WHAT IS CURRENT KNOWLEDGE
3 Gastroparesis is a well-known complication to diabetes
mellitus.
3 Dietary advice is considered to be of importance to reduce
gastrointestinal (GI) symptoms in patients with diabetic
gastroparesis, but no randomized controlled trials exist.
WHAT IS NEW HERE
3 A diet with small particle size improved the key gastroparet-
ic symptoms — nausea / vomiting, postprandial fullness and
bloating — in patients with diabetic gastroparesis.
3 No such effect was seen when patients were advised to eat
a diet normally recommended to patients with diabetes
mellitus (DM), modifi ed based on current dietary recom-
mendations for gastroparesis.
3 Patients with diabetic gastroparesis should be advised to
eat a diet with small particle size in order to improve upper
GI symptoms.
REFERENCES
1 . Abrahamsson H . Treatment options for patients with severe gastroparesis .
Gut 2007 ; 56 : 877 – 83 .
2 . J o n e s K L , R u s s o A , S t e v e n s J E et al. Predictors of delayed gastric emptying
in diabetes . Diabetes Care 2001 ; 24 : 1264 – 9 .
3 . M o l d o v a n C , D u m i t r a s c u D L , D e m i a n L et al. Gastroparesis in diabetes
mellitus: an ultrasonographic study . Rom J Gastroenterol 2005 ; 14 : 19 – 22 .
4 . Parkman HP , Fass R , Foxx-Orenstein AE . Treatment of patients with dia-
betic gastroparesis . Gastroenterol Hepatol (NY) 2010 ; 6 : 1 – 16 .
© 2014 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY
9
STOMACH
A Small Particle Size Diet in Diabetic Gastroparesis
2 5 . R e v i c k i D A , R e n t z A M , T a c k J et al. Responsiveness and interpretation of
a symptom severity index speci c to upper gastrointestinal disorders . Clin
Gastro-enterol Hepatol 2004 ; 2 : 769 – 77 .
2 6 . R e v i c k i D A , R e n t z A M , D u b o i s D et al. Development and validation of a
patient-assessed gastroparesis symptom severity measure: the Gastroparesis
Cardinal Symptom Index . Aliment Pharmacol er 2003 ; 18 : 141 – 50 .
2 7 . R e v i c k i D A , C a m i l l e r i M , K u o B et al. Evaluating symptom outcomes in
gastroparesis clinical trials: validity and responsiveness of the Gastroparesis
Cardinal Symptom Index-Daily Diary (GCSI-DD) . Neurogastroenterol
Motil 2012 ; 24 : 456 – 63 .
2 8 . Z i g m o n d A S , S n a i t h R P . e hospital anxiety and depression scale . Acta
Psychiatr Scand 1983 ; 67 : 361 – 70 .
2 9 . S n a i t h R P . e hospital anxiety and depression scale . Health Qual Life
Outcomes 2003 ; 1 : 29 .
3 0 . B j e l l a n d I , D a h l A A , H a u g T T et al. e validity of the hospital anxi-
ety and depression scale. An updated literature review . J Psychosom Res
2002 ; 52 : 69 – 77 .
3 1 . W a r e J E J r . , S n o w K K , K o s i n s k i M et al. Applications of SF-36. SF-36 Health
Survey: Manual and Interpretation Guide . e Health Institute, New Eng-
land Medical Center: Boston , 1993 .
3 2 . W a r e J E J r , K e l l e r S D , G a n d e k B et al. Evaluating translations of health sta-
tus questionnaires. Methods from the IQOLA project. International Quality
of Life Assessment . Int J Technol Assess Health Care 1995 ; 11 : 525 – 51 .
3 3 . S u l l i v a n M , K a r l s s o n J , W a r e J E J r . e Swedish SF-36 Health Survey--I.
Evaluation of data quality, scaling assumptions, reliability and construct
validity across general populations in Sweden . Soc Sci Med 1995 ; 41 :
1349 – 58 .
3 4 . H o e l z e l W , W e y k a m p C , J e p p s s o n J O et al. IFCC reference system for
measurement of hemoglobin A1c in human blood and the national
standardization schemes in the United States, Japan, and Sweden: a
method-comparison study . Clin Chem 2004 ; 50 : 166 – 74 .
35 . Truswell AS . Glycaemic index of foods . Eur J Clin Nutr 1992 ; 46 (Suppl 2) :
S91 – S101 .
3 6 . d e l a L o g e C , T r u d e a u E , M a r q u i s P et al. Cross-cultural development and
validation of a patient self-administered questionnaire to assess quality
of life in upper gastrointestinal disorders: the PAGI-QOL . Qual Life Res
2004 ; 13 : 1751 – 62 .
37 . Camilleri M . Integrated upper gastrointestinal response to food intake .
Gastroenterology 2006 ; 131 : 640 – 58 .
3 8 . J a h n b e r g T , A b r a h a m s s o n H , J a n s s o n G et al. Gastric relaxatory response to
feeding before and a er vagotomy . Scand J Gastroenterol 1977 ; 12 : 225 – 8 .
3 9 . C a s s i l l y D , K a n t o r S , K n i g h t L C et al. Gastric emptying of a non-digestible
solid: assessment with simultaneous SmartPill pH and pressure capsule,
antroduodenal manometry, gastric emptying scintigraphy . Neurogastroen-
terol Motil 2008 ; 20 : 311 – 9 .
4 0 . D e l o o s e E , J a n s s e n P , D e p o o r t e r e I et al. e migrating motor complex:
control mechanisms and its role in health and disease . Nat Rev Gastroen-
terol Hepatol 2012 ; 9 : 271 – 85 .
41 . Talley SJ , Bytzer P , Hammer J et al. Psychological distress is linked to
gastrointestinal symptoms in diabetes mellitus . Am J Gastroenterol
2001 ; 96 : 1033 – 8 .
42 . Talley NJ , Young L , Bytzer P et al. Impact of chronic gastrointestinal symp-
toms in diabetes mellitus on health-related quality of life . Am J Gastroen-
terol 2001 ; 96 : 71 – 6 .
43 . Speight J , Reaney MD , Barnard KD . Not all roads lead to Rome-a review
of quality of life measurement in adults with diabetes . Diabet Med
2009 ; 26 : 315 – 27 .
44 . Kofod-Andersen K , Tarnow L . Prevalence of gastroparesis-related symp-
toms in an unselected cohort of patients with Type 1 diabetes . J Diabetes
Comp-lications 2012 ; 26 : 89 – 93 .
5 . F a r m e r A D , K a d i r k a m a n a t h a n S S , A z i z Q . D i a b e t i c g a s t r o p a r e s i s :
pathophysiology, evaluation and management . Br J Hosp Med (Lond)
2012 ; 73 : 451 – 6 .
6 . K a s h y a p P , F a r r u g i a G . Diabetic gastro-paresis: what we have learned and
had to unlearn in the past 5 years . Gut 2010 ; 59 : 1716 – 26 .
7 . D a r w i c h e G , A l m e r L O , B j o r g e l l O et al. Delayed gastric emptying rate in
Type 1 diabetics with cardiac autonomic neuropathy . J Diabetes Complica-
tions 2001 ; 15 : 128 – 34 .
8 . Parkman HP , Yates KP , Hasler WL et al. Dietary intake and nutritional
de ciencies in patients with diabetic or idiopathic gastroparesis . Gastroen-
terology 2011 ; 141 : 486 – 98 , 498 e1-7 .
9 . Ohlsson B , Melander O , o r s s o n O et al. Oesophageal dysmotility, delayed
gastric emptying and autonomic neuropathy correlate to disturbed glucose
homeostasis . Diabetologia 2006 ; 49 : 2010 – 4 .
1 0 . e e ect of intensive treatment of diabetes on the development and pro-
gression of long-term complications in insulin-dependent diabetes mellitus.
e Diabetes Control and Complications Trial Research Group . N Engl J
Med 1993 ; 329 : 977 – 86 .
1 1 . C h e r i a n D , S a c h d e v a P , F i s h e r R S et al. Abdominal pain is a frequent symp-
tom of gastroparesis . Clin Gastroenterol Hepatol 2010 ; 8 : 676 – 81 .
12 . Faraj J , Melander O , Sundkvist G et al. Oesophageal dysmotility, delayed
gastric emptying and gastrointestinal symptoms in patients with diabetes
mellitus . Diabet Med 2007 ; 24 : 24 .
1 3 . O g o r e k C P , D a v i d s o n L , F i s h e r R S et al. Idiopathic gastroparesis is associ-
ated with a multiplicity of severe dietary de ciencies . Am J Gastroenterol
1991 ; 86 : 423 – 8 .
14 . Cherian D , Paladugu S , Pathikonda M et al. Fatigue: a prevalent symptom
in gastroparesis . Dig Dis Sci 2012 ; 57 : 2088 – 95 .
1 5 . H y e t t B , M a r t i n e z F J , G i l l B M et al. Delayed radionucleotide gastric empty-
ing studies predict morbidity in diabetics with symptoms of gastroparesis .
Gastro-enterology 2009 ; 137 : 445 – 52 .
1 6 . C a m i l l e r i M , P a r k m a n H P , S h a M A et al. Clinical guideline: management
of gastroparesis . Am J Gastroenterol 2013 ; 108 : 18 – 37 .
17 . Gentilcore D , Chaikomin R , Jones KL et al. E ects of fat on gastric empty-
ing of and the glycemic, insulin, and incretin responses to a carbohydrate
meal in type 2 diabetes . J Clin Endocrinol Metab 2006 ; 91 : 2062 – 7 .
18 . Holt S , Heading RC , Carter DC et al. E ect of gel bre on gastric emptying
and absorption of glucose and paracetamol . Lancet 1979 ; 1 : 636 – 9 .
1 9 . O l a u s s o n E A , A l p s t e n M , L a r s s o n A et al. Small particle size of a solid meal
increases gastric emptying and late postprandial glycaemic response in
diabetic subjects with gastroparesis . Diabetes Res Clin Pract 2008 ; 80 :
231 – 7 .
2 0 . M a n n J I , D e L e e u w I , H e r m a n s e n K et al. Evidence-based nutritional ap-
proaches to the treatment and prevention of diabetes mellitus . Nutr Metab
Cardiovasc Dis 2004 ; 14 : 373 – 94 .
2 1 . O l a u s s o n E A , B r o c k C , D r e w e s A M et al. Measurement of gastric emptying
by radiopaque markers in patients with diabetes: correlation with scin-
tigraphy and upper gastrointestinal symptoms . Neurogastroenterol Motil
2013 ; 25 : e224 – 32 .
2 2 . G r y b a c k P , H e r m a n s s o n G , L y r e n a s E et al. Nationwide standardisation
and evaluation of scintigraphic gastric emptying: reference values and
comparisons between subgroups in a multicentre trial . Eur J Nucl Med
2000 ; 27 : 647 – 55 .
2 3 . S c h v a r c z E , P a l m e r M , A m a n J et al. Physiological hyperglycemia slows
gastric emptying in normal subjects and patients with insulin-dependent
diabetes mellitus . Gastroenterology 1997 ; 113 : 60 – 6 .
24 . Rentz AM , Kahrilas P , Stanghellini V et al. Development and psychometric
evaluation of the patient assessment of upper gastrointestinal symptom se-
verity index (PAGI-SYM) in patients with upper gastrointestinal disorders .
Qual Life Res 2004 ; 13 : 1737 – 49 .
The American Journal of GASTROENTEROLOGY VOLUME 104 | XXX 2012 www.amjgastro.com
10
STOMACH
Olausson et al.
Table A1 . Intervention diet — small particle size food
Poorly digestible food Medium digestible food Easily digestible food
Vegetables and roots
Raw: carrots, turnip, parsnips Cooked: carrots, turnip, parsnips Mashed turnips, mixed beetroot pickled beet
Cooked caulifl ower and broccoli stem Cooked caulifl ower fl ower, broccoli fl ower
Asparagus stalk Asparagus tip
Green pea Green pea pur é e
Boiled corn (Cooked and mixed) corn pat é
Cooked beans (Cooked and mixed) beans pat é
Cooked brussels sprouts (Cooked and mixed) brussels sprout pat é
Raw and cooked cabbage
Raw, boiled, and fried mushrooms Mixed mushrooms Mushroom paste
Boiled and fried onion Fine mixed onion, dried powdered onion
Cooked leeks Mixed leeks
Rhubarb
Salad, cucumber, tomatoes Canned crushed tomatoes Tomato paste
Pepper Pepper without skin Mixed pepper
Avocado Mashed avocado
Fruit and berry
Fresh fruit Cooked and canned fruit or berry Puree of fruit or berry
Skin and membrane of citrus:
Orange, clementine, grapefruit
Pineapple Ripe pears without skin Ripe pears without skin, canned peach
Raspberries, strawberries Gooseberries
Blueberries, currant, and lingo berries Mixed: blueberries, currant and lingo berries
Blackberry, cloudberries
Green and green-yellow banana Yellow banana Yellow-brown banana
Netted melon Kiwi, soft gala melon Mixed kiwi, water melon
Mango, papaya
Nuts and Almonds
Fruits and almonds Flour of fruits and almonds
Potato
Fried potatoes, french potatoes Boiled potatoes, baked potatoes Mashed potatoes, pressed potatoes, creamed potatoes
Pasta and rice
Pasta
Parboiled rice and brown rice, non-parboiled rice
Bulgur, couscous, porridge
Bread
White fresh bread Wholegrain cereal fl our bread Brown crisp
Bread with seeds and whole grains Bread baked on coarse fl our Bread baked on whole meal fl our, rye crisp, rusks
Cheese
Fat cheese, ripened cheese Cottage cheese Processed cheese, spreadable cheese, quark
Eggs
Hard-boiled eggs, soft-boiled eggs Mashed-boiled eggs, french omelet
Pancakes
Scrambled eggs made in frying pan Scrambled eggs made in pot Baked omelet Swedish style, baked egg
Butter pudding
APPENDIX 1
Table A1 continued on following page
© 2014 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY
11
STOMACH
A Small Particle Size Diet in Diabetic Gastroparesis
Table A2 . Control diet — large particle size food
Dietary treatment
Beverages
Free intake of beverages containing < 0.5 g carbohydrates / 100 ml ready
to drink beverages
Preparations to choose
Raw or lightly cooked vegetables
Fresh fruit and berries
Foods providing good metabolic control
Bread made of whole grain and whole grain fl our
Rice and pasta rather than potatoes
Potatoes are allowed only in combination with raw or light cooked
vegetables
Pasta and rice with long-cooking rather than with short-cooking time
Combination of food items to improve glycemic index
Legumes
Food items to avoid
Mashed potatoes and mashed turnips
Other mashed or mixed foods
Breads made of fl our without grains and / or sourdough
Fruit or berry compote or cream
Canned vegetables
Porridge, corn fl akes and gruel
Smooth soup
Sweet drinks
Table A1 . Continued
Poorly digestible food Medium digestible food Easily digestible food
Meat
Whole meat Minced meat dishes Mixed minced dishes, sausage
Jellied veal
Extra thin slices of ham
Fish and seafood
Cured salmon, smoked salmon Baked salmon Baked fl atfi sh, boiled fi sh loaf dishes, fi sh pudding
Raw spiced salmon Baked mackerel baked cod fi sh Fish souffl é , fi sh balls, fi sh pate, fi sh gratin herring terrine
Shrimp, crab, clams, tails Mixed shrimp, crab, clams, tails
Cooking methods
Raw, wok Cooked, canned Puree, mixed, pate, timbale, sauces
Fried in a pan, deep fried, wok Roasted, baked Cooked
Coating with egg and breadcrumbs
Coating with breadcrumbs
Fat cooking methods Lean cooking methods
APPENDIX 2
