Ultrasonography findings in diabetes and diabetes gastroparesis: A meta-analysis

Marcellus Simadibrata; Amanda Pitarini Utari; Alvita Dewi Siswoyo; Elsha Stephanie Anastasia; Trifonia Pingkan Siregar; Dyah Purnamasari

doi:10.12688/f1000research.128672.1

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Systematic Review

Ultrasonography findings in diabetes and diabetes gastroparesis: A meta-analysis

[version 1; peer review: 1 not approved]

Marcellus Simadibrata^1,2, Amanda Pitarini Utari ^1,2, Alvita Dewi Siswoyo^1,3, Elsha Stephanie Anastasia², Trifonia Pingkan Siregar^1,3, Dyah Purnamasari^1,4

Marcellus Simadibrata^1,2, Amanda Pitarini Utari ^1,2, [...] Alvita Dewi Siswoyo^1,3, Elsha Stephanie Anastasia², Trifonia Pingkan Siregar^1,3, Dyah Purnamasari^1,4

PUBLISHED 31 Aug 2023

Author details Author details

¹ University of Indonesia, Jakarta Pusat, DKI Jakarta, 10430, Indonesia
² Department of Gastroenterology, National General Hospital Dr. Cipto Mangunkusumo, University of Indonesia, Jakarta Pusat, DKI Jakarta, 10430, Indonesia
³ Department of Radiology, University of Indonesia, Jakarta Pusat, DKI Jakarta, 10430, Indonesia
⁴ Department of Endocrinology, National General Hospital Dr. Cipto Mangunkusumo, University of Indonesia, Jakarta Pusat, DKI Jakarta, 10430, Indonesia

Marcellus Simadibrata
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Amanda Pitarini Utari
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Alvita Dewi Siswoyo
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Elsha Stephanie Anastasia
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Trifonia Pingkan Siregar
Roles: Resources, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

Dyah Purnamasari
Roles: Resources, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

OPEN PEER REVIEW

REVIEWER STATUS

Abstract

Background: The gold standard for diagnosis of diabetes gastroparesis (DG) is with gastric emptying scintigraphy (GES) examination. However, GES is not available in every healthcare center worldwide and the examination cost is rather expensive, unlike ultrasonography (USG) examination. This study aims to evaluate gastric changes monitored with USG in diabetes mellitus (DM) and DG.
Methods: We performed searches from Google Scholar, PubMed, Science Direct, Proquest, and Scopus in April 30 – May 6, 2022. Random-effect approach on outcomes, standardized mean-difference (SMD) and 95%-confidence interval (CI) was assessed.
Results: Compared to healthy control; (1) Antral cross-sectional area (CSA) in DM is bigger in fasting (SMD=1.25cm²; 95%CI, 0.79 to 1.71, I2=81%, P<0.05) and postprandial (SMD=3.70 cm2; 95%CI, 1.45 to 5.34, I2=85%, P<0.05). (2) Gastric emptying time (GET) is longer with DG (SMD=75.44min; 95%CI, 31.61 to 119.27, I2=97%) and in DM (SMD=35.54min; 95% CI, 11.49 to 59.60, I2=94%). (3) Gastric half-emptying time (GE50) were found to be longer in DM (SMD=20.73 min; 95%CI, 14.69 to 26.77, I2=60%, P<0.05) and DG (SMD=7.46min; 95%CI, 5.06 to 9.86, I2=68.2%, P<0.05). (4) Smaller gastric emptying rate (GER) in DG (SMD=-31.95%; 95%CI, -42.22% to -21.69%, I2=84%, P<0.05) and DM (SMD=-16.14%; 95%CI, -30.88% to -1.39%, I2=78%, P<0.05). (5) Less antral contraction in DG (SMD=-1.47; 95%CI, -2.61 to -0.33, I2=82%, P<0.05).
Conclusions: Patients with DM and DG have wider antral CSA, longer GET and GE50, reduced GER and reducing antral contraction. USG is useful for assessing gastric emptying in DM and DG.
PROSPERO registration: CRD42022328695 (10/05/2022)

Keywords

Meta-Analysis, Diabetes Gastroparesis, Diabetes Mellitus, Ultrasonography

Corresponding author: Amanda Pitarini Utari

Competing interests: No competing interests were disclosed.

Grant information: The authors received funding for this research from Research and Community Service Information Base of Indonesia (Badan Informasi Penelitian dan Pengabdian Kepada Masyarakat Indonesia – BIMA Indonesia). Nomor: NKB-793/UN2.RST/HKP.05.00/2022 The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2023 Simadibrata M et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: Simadibrata M, Utari AP, Siswoyo AD et al. Ultrasonography findings in diabetes and diabetes gastroparesis: A meta-analysis [version 1; peer review: 1 not approved]. F1000Research 2023, 12:1066 (https://doi.org/10.12688/f1000research.128672.1) First published: 31 Aug 2023, 12:1066 (https://doi.org/10.12688/f1000research.128672.1) Latest published: 31 Aug 2023, 12:1066 (https://doi.org/10.12688/f1000research.128672.1)

Introduction

Gastric symptoms of diabetes are often a long-standing complication of uncontrolled diabetes mellitus (DM) which highly affect the patient's quality of life.¹^,² Delayed gastric emptying (DGE) without obstruction in diabetes gastroparesis (DG) is caused by disorder in the neuromuscular function of the stomach which can be a result of various processes: idiopathic, DM-associated gastroparesis, or as an adverse effect of medical intervention such as surgical gastric resection.³^,⁴ Diabetic gastroparesis is shown by gastrointestinal symptoms such as nausea, vomiting, postprandial fullness, bloating, and early satiety.⁴^,⁵ Hyperglycemia, oxidative stress, neuropathy, and inflammation in diabetic patients are associated with the pathophysiology of DG.³^,⁵

A study in general practice from the United Kingdom revealed that the prevalence of gastroparesis per 100,000 persons was 13.8 in 2016. DM is the second most common etiology after idiopathic.⁶ Different from that record, a study in the United States in 2018 found DM as the primary cause of gastroparesis, with as high as 57.4% of the patients having DM. The overall number is also higher, reaching 267.7 per 100,000 persons, although the prevalence of patients with definite delayed emptying reported from scintigraphy is lower, with only 21.5 per 100,000 persons.⁷ It is estimated that the prevalence of this disorder to be 9.6 per 100,000 person in men and 37.8 per 100.000 in women.⁸ Depression and anxiety are common in patients with gastroparesis; thus, their quality of life is significantly impaired.⁵^,⁹ Aside from the quality of life, evaluation of delayed emptying is also essential to analyze absorption and consequently regulation of blood glucose in DM.¹^,⁵

The gold standard for diagnosis of DG is with gastric emptying scintigraphy (GES) examination.⁴ However, the application of this method is still limited in many countries due to the limited availability of examination equipment, relatively expensive cost, and long hours of the examination.¹⁰^,¹¹ Radiation exposure is also a concern in itself.¹² Other recommended alternatives such as 13C-octanoic acid breath test, wireless motility capsules, and electrogastrography (EGG) are even less available. In contrast, ultrasonography (USG) is readily available in most hospitals worldwide. USG examination is a non-invasive, affordable, and relatively easy-to-perform test. It can measure emptying time, intra-gastric volume, and antral cross-sectional area (CSA).⁸ It is also known to be used by anesthesiologists to determine the volume and content of the stomach for perioperative point-of-care tests.¹³^–¹⁵ The broad availability, safety from radiation exposure, and affordable tools could make ultrasound a suitable candidate for an alternative gastric emptying examination¹⁶^–¹⁸ and its accuracy compared to the gold standard needs further investigation. The potential USG use on DG screening remains a question. The objective of this study is to¹ evaluate USG findings of gastric changes found in DM and DG. ²

Methods

This meta-analysis was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA)-2020 guideline.¹⁹^,⁶⁴ Prior to this publication, the study protocol had already been registered to the PROSPERO database (CRD42022328695 (10/05/2022)).²⁰

Search strategy

Literature search was conducted during period April 30 – May 6, 2022 by comprehensive search in Google scholar, PubMed, Science Direct, ProQuest, and Scopus by authors. The search words for each database platform were based on Medical Subject Heading (MeSH) terms combined with Boolean operator (AND/OR) with keyword: (“gastroparesis”[MeSH Terms] OR “gastroparesis”[All Fields]) AND (“diabetes mellitus”[MeSH Terms] OR (“diabetes”[All Fields] AND “mellitus”[All Fields]) OR “diabetes mellitus”[All Fields] OR “diabetes”[All Fields]) AND (“diagnostic imaging”[Subheading] OR (“diagnostic”[All Fields] AND “imaging”[All Fields]) OR “diagnostic imaging”[All Fields] OR “ultrasonography”[All Fields] OR “ultrasonography”[MeSH Terms]) (PUBMED), (Diabetic Gastroparesis AND Ultrasonography OR USG OR US) in Google Scholar, Science Direct, ProQuest, Scopus, and Diabetes Gastroparesis in clinical trial registries (i.e clinicaltrial.gov, ISRCTN, European Clinical Trial Registry) (see Extended data for the full list of clinical trial registries⁶⁴).

Study selection

The studies gathered from the search were screened by the authors. Duplicates were removed using Mendeley Reference Manager after a manual crosscheck. Reviewers independently screened the studies based on the eligibility criteria: observational (cross-sectional, case-control, and cohort) and interventional studies, included patients with both Type 1 (T1D) and Type 2 Diabetes (T2D), assessed comparison of gastric antral area on fasting and postprandial state, gastric emptying time, gastric half emptying time, antral contraction rate. Exclusion criteria were: review articles, duplicates, protocols or guidelines, irrelevant articles, case series, case reports, and non-human studies. The study selection process from searching, screening, and selection is elaborated further in the PRISMA diagram (Figure 1).

Figure 1. Search strategy following the PRISMA 2020 flow diagram for new systematic reviews.¹⁹

Data extraction

Reviewers extracted the data separately with a standardized format and reviewed. Any differences and disagreements were resolved through discussion among authors until an agreement was reached. Standardized formats for data extraction were as follows: author name, publication year, country, study design, sample size, age, duration of diabetes, examination methods, outcomes, and quality assessment.

Quality assessment

All authors performed quality assessment. The study was assessed with the Study Quality Assessment Tool from the National Institute of Health (NIH) for case-control, cohort, and cross-sectional studies.²¹ Quality assessments for cross-over studies were assessed based on Cochrane Systematic Reviews.²² The outcome of the quality assessment was assigned as poor, fair, and good based on the overall rating from each question. Differences were resolved through discussion among authors until an agreement was reached. This article included all studies from all ranges of quality (poor, moderate, and good). Quality assessments are shown in Table 1.

Table 1. Quality assessment.

Quality assessment
Case control	Quality assessment
Bian et al. (2011)	Good
Brogna et al. (1999)	Fair
Chiu et al. (2014)	Good
Cotroneo et al. (1991)	Poor (Abstract-only Article)
Darwiche et al. (1999)	Good
Darwiche et al. (2001)	Good
Darwiche et al. (2014)	Good
Dorlars et al. (2008)	Good
Gao et al. (2000)	Poor (Abstract-only Article)
Garg et al. (2020)	Good
Hermann et al. (1998)	Good
Kawagishi et al. (1944)	Good
Moldovan et al. (2005)	Good
Pfaffenbach et al. (1994)	Fair
Shen et al. (2014)	Good
Sogabe et al. (2005)	Fair
Sogabe et al. (2008)	Good
Taher et al. (2016)	Good
Undeland et al. (1996)	Fair
Undeland et al. (1997)	Good
Undeland et al. (1998)	Good
Vogelberg et al. (1985)	Fair
Vogelberg et al. (1986)	Fair
Vogelberg et al. (1988)	Fair
Wu et al. (2014)	Poor (Abstract-only Article)

Operational definitions

The calculations for each operational definition were as follows. Cross-sectional area is defined as total gastric cross-sectional area evaluated during ultrasonography assessment with multiple method (i.e. anteroposterior diameter × craniocaudal diameter × π)/4²³). Preprandial/fasting antral is defined as the measurement of antral area pre-meal or after fasting time, while postprandial is measured post-meal.²⁴ Gastric emptying time is described as the time after the meal until the time gastric returns to its original measurement.²⁵ Gastric half-emptying time (GE50) is the time post-meal until only 50% of gastric content is left.²⁶ The motility index is calculated by mean amplitude × frequency of contraction.²⁷

Data synthesis and analysis

The primary outcomes of this study were to analyze the effect of gastric changes in diabetic and DG patients found in ultrasound examination. This study's gastric changes consisted of antral area CSA, GET, GE50, GER (%), and antral contraction. Dersimonian-Laird method was used for tau estimation. Inverse variance was used for pooling of SMD of continuous outcome. P-value of <0.05 is the cutoff for study to be considered statistically significant.

I² and Q statistics were used to assess heterogeneity. High heterogeneity was defined as I>50% and/or P-value <0.1. Random-effect analysis was used for estimating the effect size regardless of the I² value. Leave-one-out sensitivity analysis was conducted to evaluate each study's influence on the pooled results. Potential bias in publications was assessed via Begg's funnel plot. This study used a subgroup analysis based on group population in the study design. Sensitivity analysis was used to ensure the robustness of the result. All statistical analyses were performed using Review Manager ver. 5.4 (The Cochrane Collaboration).

Results

The search strategy described in Figure 1 resulted in 136 articles from database screening, four studies from manual screening, and three from citation screening. After evaluation of titles and abstracts, 43 articles were selected for full-text evaluation. The review yielded 25 case-control studies. Article appraisal graded 18 articles as good, four as fair, and two as poor (Extended data¸supplemenent 1⁶⁴). All studies were included in the study to minimize the risk of publication bias.

All studies reported gastric changes found in people with diabetes with various degrees. The gastric antral area, emptying time, and antral contractility were found to be worse in DM and DG populations. Changes in antral contraction were found to be insignificant in diabetes but less in the DG population. With a total of 25 studies included, 715 samples of DM were included in this study. Further result are elaborated in Table 2.

Table 2. Characteristics of the included study and the quality assessment.

Study	Year	Country	Study design	Sample size		DM Type	Age (years) Mean±SD/Median		Diabetes duration (years)	Outcomes	Quality assesment
Study	Year	Country	Study design	Diabetes (M/F)	Control (M/F)	DM Type	Diabetes	Control	Mean±SD	Outcomes	Quality assesment
Bian et al.	2011	China	Case-Control	71 (39/32)	30 (12/18)	T2	68.2±6.8	68.1±6.3	11.1±5.2	GET1/2, Tlag, GET60, GET120, Stomach CSA	Good
Brogna et al.	1990	Italy	Case-Control	14 (9/5)	10 (6/4)	T1	42±10	39±9	13±2	FET, GE50	Fair
Chiu et al.	2014	Taiwan	Case-Control	11 (9/2)	11 (9/2)	T2	58±2	51±5	11.1±5.6	Antral & Fundus CSA, Antral Contraction.	Good
Cotroneo et al.	1991	Italy	Case-Control	18	10	T2	NS	NS	NS	GET	Poor (Abstract-only)
Darwiche et al.	1999	Sweden	Case-Control	14 (6/8)	19 (8/11)	T1	55±9	37±18	34±10	Antral CSA, GET	Good
Darwiche et al.	2001	Sweden	Case-Control	20 (11/9)	10 (5/5)	T1	55±10.75	54±17	30.5±12.26	GER	Good
Darwiche et al.	2014	UAE	Case-Control	31 (25/6)	10 (8/2)	T1&T2	52±12	54±14	15±9	Antral CSA, GER,	Good
Dorlars et al.	2008	Germany	Case-Control	48 (29/19)	50 (26/24)	T1&T2	54.8	51	NS	GET	Good
Gao et al.	2000	China	Case-Control	20	22	T2	NS	NS	NS	GET50	Poor (Abstract-only)
Garg et al.	2020	India	Case-Control	53 (24/29)	50 (20/30)	T1&T2	56.55±8.95	44.06±13.99	6.6	CSA, GV	Good
Hermann et al.	1998	Germany	Case-Control	22 (9/13)	30 (14/16)	T1	37.75±12	36	18.1±7.83	GET, enantiomer availability	Good
Kawagishi et al.	1994	Japan	Case-Control	32 (17/15)	10 (5/5)	T1&T2	55.8	53.8	14	Antral contraction, velocity of flow	Good
Moldovan et al.	2005	Romania	Case-Control	36 (17/19)	20 (10/10)	T1&T2	T1&T2: 48.9±7.3 & 59.9±7.6	52.6±10.1	NS	Antral CSA, GET	Good
Pfaffenbach et al.	1994	Germany	Case-Control	20 (10/10)	20 (10/10)	T2	65.7±10.1	Range (23-71)	15±11.5	GET	Good
Shen et al.	2014	China	Case-Control	36 (19/17)	92 (52/40)	T2	46.5±8.6	44.7±8.5	NS	GET	Good
Sogabe et al.	2005	Japan	Case-Control	30 (16/14)	N/A	T1&T2	60.6±12.1	NA	16.6±11.6	Frequency of contraction, motility index, GE	Fair
Sogabe et al.	2008	Japan	Case-Control	18 (6/12)	13 (7/6)	T1&T2	61.6±11.4	50.3 6.5	16.3±8.8	Contraction frequency, motility index, GE	Good
Taher et al.	2016	Bangladesh	Case-Control	45 (16/29)	45 (15/30)	T2	52.64±8.59	48.13±10.68	13.16±5.64	Antral Area	Good
Undeland et al.	1996	Norway	Case-Control	42 (15/27)	23 (14/9)	T1	33.5	44.7	7.7	Antral CSA	Fair
Undeland et al.	1997	Norway	Case-Control	14 (5/9)	18 (9/9)	T1	36.4	31	20.3±9.6	Antral CSA, Vagal Tone, PP volume	Good
Undeland et al.	1998	Norway	Case-Control	20 (10/10)	20 (10/10)	T1	35.3±7.6	34.7±10.7	NS	Antral area, proximal area, proximal diameter	Good
Vogelberg et al.	1985	Germany	Case-Control	24 (7/17)	11 (7/4)	T1	38±17	29±14	15.6±9.7	Antral CSA, GE50	Fair
Vogelberg et al.	1986	Germany	Case-Control	32 (18/14)	12 (8/4)	T1	50±17	42±17	16.1±6.9	Frequency, intensity, velocity	Good
Vogelberg et al.	1988	Germany	Case-Control	10 (3/7)	5 (2/3)	T1	47.5±17.7	46±19	19.0±10.7	Antral area, frequency, intensity, velocity	Good
Wu et al.	2014	China	Case-Control	35	35	NS	NS	NS	NS	GER, ET	Poor

Primary outcomes

Summary meta-analysis results presented as forest plots are shown in Table 3.

Table 3. Summary of meta-analysis’ plots.

Outcomes	Group (n=population)	No of studies	Standardized mean difference (95%CI)	I² (%)	P-value
Pre Prandial gastric antral cross-sectional area	DM (315) vs HC (240)	11	1.25 cm² (0.79 to 1.71)	81	P<0.001
Post prandial gastric antral cross-sectional area	DM (191) vs HC (166)	8	3.70 cm² (1.45 to 5.34)	85	P<0.005
Gastric emptying time (GET)	DM (129) vs HC (130)	5	35.54 min (11.49 min to 59.60 min)	94	P<0.001
Gastric emptying time (GET)	DG (52) vs HC (75)	3	75.44 min (31.61 min to 119.27 min)	97	P<0.001
Gastric half emptying time (GE50)	DM (49) vs HC (32)	3	20.73 min (14.69 to 26.77)	60	P<0.001
Gastric half emptying time (GE50)	DG (56) VS HC (114)	2	7.46 min (5.06 to 9.86 min)	68.2	P<0.001
Gastric emptying rate (GER)	DG (115) VS HC (81)	3	-31.95% (-42.22% to -21.69%)	84	P=0.01
Gastric emptying rate (GER)	DM (33) VS HC (39)	5	-16.14% (-30.88% to -1.39%)	78	P<0.001
Antral contraction	DM (28) VS HC (22)	3	0.09 (-0.18 to 0.36)	0	P=0.01
Antral contraction	DG (85) VS HC (53)	6	-1.47 (-2.61 to -0.33)	82	P<0.001

Antral cross-sectional area

The standardized mean difference (SMD) of antral CSA in pre- and post-prandial showed that antral CSA (cm²) in diabetic patients were significantly bigger both in preprandial (SMD=1.25 cm² (95%CI, 0.79 cm² to 1.71 cm²), I²=81%, P<0.05) and postprandial (SMD=3.70 cm² (95%CI, 1.45 cm² to 5.34 cm²), I²=85%, P<0.05). Leave-one-out sensitivity analysis in the preprandial subgroup showed that heterogeneity was reduced when the study by Darwiche et al., 2014 was omitted from the analysis (I²=70%, P<0.05) with the direction of effect remaining unchanged. In the postprandial subgroup, heterogeneity was reduced following the removal of studies by Darwiche et al., 2014 (SMD=1.06 cm² (95%CI, 0.7 cm² to 1.42 cm²), I²=65%, P<0.05) and Taher et al., 2016 (SMD=1.26 cm² (95%CI, 0.71 cm² to 1.8 cm²), I²=76%, P<0.05), however, the direction of effect remains Figure 2.

Figure 2. Antral cross-sectional area.

Gastric emptying time (GET)

The SMD of gastric emptying time (GET) in DM and DG revealed that GET (min) were significantly longer in both the DM and DG subgroups. Furthermore, a longer emptying time in DG (SMD=75.44 min (95%CI, 31.61 min to 119.27 min), I²=97%) was found compared to DM (SMD=35.54 min (95%CI, 11.49 min to 59.60 min), I²=94%). Leave-one-out sensitivity analysis in both subgroups showed no significant reduction in heterogeneity if each study was removed Figure 3.

Figure 3. Gastric emptying time.

Gastric half emptying time (GE50)

The SMD of GE50 in DM showed that GE50 were significantly longer in both DM and DG subgroups. A bigger time difference to HC was found in DM (SMD=20.73 min (95%CI, 14.69 min to 26.77 min), I²=60%, P<0.05) compared to DG (SMD=7.46 min (95%CI, 5.06 min to 9.86 min), I²=68.2%, P<0.05). Leave-one-out sensitivity analysis in the DM subgroup showed that heterogeneity was reduced (I²=44%, P<0.05) when the study by Brogna et al., 1990 (SMD=18.34 min (95%CI, 11.73 min to 24.94 min)) was removed from the analysis. No changes of direction were found in leave-one-out sensitivity analysis Figure 4.

Figure 4. Gastric half-emptying time.

Gastric emptying rate (GER)

The pooled result of SMD of gastric emptying rate (GER) in DM and DG were smaller in both subgroups compared to the control. Overall, DG subgroups had smaller GER (SMD=-31.95% (95%CI, -42.22% to -21.69%), I²=84%, P < 0.05) than DM (SMD=-16.14% (95%CI, -30.88% - -1.39%), I²=78%, P<0.05). Leave-one-out sensitivity analysis in the DM subgroup revealed that heterogeneity was reduced when the study by Darwiche et al., 1999 was removed (I²=0%, P=0.9). In the DG subgroup, sensitivity analysis showed no significant reduction in heterogeneity if each study was removed. No changes of direction were found in leave-one-out sensitivity analysis Figure 5.

Figure 5. Gastric emptying rate.

Antral contraction

The frequency of antral contraction in diabetic patients were found similar to HC (SMD=0.09 (95%CI, -0.18 to 0.36), I²=0%, P=0.49), but significantly less in DG (SMD=-1.47 (95%CI, -2.61 to -0.33), I²=82%, P<0.05). Leave-one-out sensitivity showed that heterogeneity reduced when the study by Kawagishi et al., 1994 (SMD=-1.97 (95%CI, -2.93 to -1.00), I=42%, P=0.16) or Sogabe et al., 2005 (SMD=-1.12 (95%CI, -2.18 to -0.07) I²=64%, P ≤ 0.05) was removed from the analysis. The direction of effect remains unchanged in both treatments Figure 6.

Figure 6. Antral contraction.

Publication bias

Begg’s funnel plot inspection for asymmetry to assess the publication bias in this study indicate possible publication bias in outcomes of antral area and GE50, the rest of the outcomes (GET, GER, and antral contraction) were found symmetrical, hence minimal risk of publication bias were found in the variables Figure 7.

Figure 7. Publication bias assessment funnel plot of (A) antral area (B) gastric emptying time (GET) (C) gastric half-emptying time (GE50) (D) gastric emptying rate (GER) (E) antral contraction.

DM: Diabetes Melitus, DG. Diabetes Gastroparesis.

Discussion

Diabetes with and without gastroparesis results in changes in gastric physiological conditions that can be examined via ultrasonography. In our study, 11 case-controls demonstrated changes in gastric antral CSA,¹⁷^,²³^–²⁶^,²⁸^–³³ indicating there is a possible structural change leading to a wider antral area (SMD 1.25 cm² in fasting state and 3.70 cm² in postprandial) compared to the HC. Total GET¹⁶^,¹⁸^,³⁰^,³⁴^–³⁷ and GE50¹²^,²⁶^,³⁴^,³⁸^,³⁹ were also assessed, and all studies reported longer emptying time in DM and DG groups (SMD to healthy control of GET in DG at 75.44-min, DM st 35.54-min; GE50 15.75-min in DM and 7.46-min in DG; and reduced GER SMD -31.95% in DG and -16.14% in DM). Reduced gastric motility¹⁷^,²⁷^,⁴⁰^–⁴² was also found in DG (SMD to control at -1.47 contraction).

Antral area and antral dilation were found to be wider in both fasting and postprandial states than HC in our study. Undeland et al. (1996)³¹ reported the loss of parasympathetic innervation presented by the loss of vagal tone and the finding of wider fasting and postprandial antral area. Further study by the same author³³ reported that loss of vagal tone is associated with the antral area and intragastric meal distribution. The mechanism might be related to vagal nerve function to stimulate gastric acid secretion to prepare the stomach for digestion. In DM and DG, acid secretion was found to be lower⁴³ with slower emptying of gastric juice,²⁹ which may be resulted from vagal neuropathy.³¹^,³³ Autonomic neuropathy due to vagal impairment also causes loss of gastric tone³²; consequently, wider dilation before and after the food filling can be seen in DM.

Prolonged emptying time in DM is often associated with two mechanisms; hyperglycemic condition and the presence of autonomic neuropathy.⁵ The first mechanism is a hyperglycemic condition. Moldovan et al. (2005)³⁰ discovered that HbA1c level and fasting glucose are highly significant with DGE. Maheshwari et al. (2021)⁴⁴ stated the prevalence of DGE to be around 30–50% in DM patients. In acute hyperglycemia, disturbance of the physiologic gastric emptying phase is associated with prolonged gastric emptying. Gastric emptying of solids is divided into two phases; the lag phase (movement of meals from the fundus to antrum) and the post-lag phase (the process of meal passing the pylorus), which involves actions of the pyloric, antral, and proximal gastric section. Conditions of hyperglycemia can stimulate pyloric contraction, disrupt antral wave, and reduce proximal gastric tone, causing a longer lag phase and slower post-lag emptying rate.⁴⁵ Chronic hyperglycemia can also cause prolonged gastric emptying. In the normal state, blood glucose and incretin secretion depend on carbohydrate exposure in the small intestines. However, constant hyperglycemia in poorly controlled DM can induce glucagon like peptide-1 (GLP1) and gastric inhibitory polypeptide (GIP) production, which stimulate insulin production, resulting in a constantly high level of GLP1.⁴⁶ GLP1 slows gastric emptying rate.⁴⁷^,⁴⁸ Furthermore, the hormonal by-product from incretin secretion, amylin, induces vagal response and further decreases the gastric emptying rate in both DM and DG population.⁴⁹ Therefore, both acute and chronic conditions may lead to prolonged gastric emptying in DM.

The second mechanism that often-prolonged gastric emptying shown in DM is neuropathy.⁵ The gastric area receives innervation from celiac ganglia and vagal nerve, which regulate gastric motility.⁵⁰ Diabetes causes neuropathy that reduces antral contraction, causing less contraction and resulting in slower food digestion in the stomach and, eventually, longer emptying time.⁵ A study by Kawagishi et al.⁴⁰ and Vogelberg et al.³⁸^,⁴¹ finds that autonomic neuropathy is associated with reduced antral contraction. The prevalence of neuropathy in DM with DGE from the studies varies, ranging from 39%–75%, indicating a possible correlation to DGE. Seven studies²⁵^,³⁰^,³³^,⁴⁰^,⁵¹^,⁵² found a significant relation in DGE to autonomic neuropathy (AN) in DM. However, Pfaffenbach et al. (1994)³⁶ and Zhou et al. (2019)⁵³ found no significant difference in DGE in DM with AN or without AN. These findings are congruent to the theory of prolonged GET due to neuropathy.

Gastric half emptying time in diabetic patients showed an interesting result. The finding showed SMD to HC of 15.75-min in DM and 7.46-min in DG, with longer GE50 in DM, contrary to the definition of DG itself, which is an established diagnosis after findings of definite prolonged gastric emptying with the absence of structural obstruction.⁵⁴ The longer GE50 in DM is because studies included in the meta-analysis in DG used a liquid test-meal,¹²^,³⁹ while all samples in DM were measured with a solid test-meal, which requires a longer time to digest.²⁶^,³⁴^,³⁸ Therefore, a slower half-emptying time was found in the solid meal test in DM compared to liquid test in DG populations.

The method for ultrasonography assessment of gastric emptying varies across all studies. To the best of our knowledge, a protocol for gastric emptying measurement has not yet been established, especially in DG. The fasting time varies for every study, with the shortest overnight fasting (6~8 hours)³¹^,³³ and the longest at 16 hours.³⁴ The meal sets to evaluate postprandial gastric changes in both liquid and solid meal test were also very diverse. Various liquid meals were used in the liquid meal test, including water,⁵¹ consommé,²⁷^,⁴² meat soup,¹^,²⁶^,³¹^,³² soluble dietary fiber liquid,⁵⁵ and commercial meal soup.¹^,³³ For meal test, a variation on solid meal test includes World Instant Gastrointestinal Ultrasound Contrast,¹²^,⁵⁶ test meal with different calorie content (280–650kcal),³⁰^,³⁵^,³⁶^,³⁸^,⁴¹^,⁵⁷ rice pudding,¹⁵^,²⁸^,²⁹^,⁵²^,⁵⁸ minced beef meat,¹⁰ gastro-enteric ultrasound developer meal,³⁷ and semi-solid paste.⁵⁹ An established protocol for meal-set and fasting time is necessary to reduce the risk of bias in the gastric emptying study.

Routine use of ultrasonography for gastric emptying has multiple benefits. A study by Stevens et al. (2011)¹⁰ analyzed the difference in gastric emptying measurement using 2D-USG compared to the 3D-USG method and found no significant correlation in results from both examination methods. However, 3D-USG was found to be superior due to its significance and relatively good agreement limit when compared to the previous gold standard GES.⁶⁰ Two studies²⁸^,³⁶ analyzed the inter-observer and intra-observer variability in USG to assess the reproducibility of USG and found the inter-observer standard measurement of error (SME) around 0.3%–10.9% and intra-observer SME around 3.6%–9.5%, indicating a good reproducibility for USG. GES and USG comparison shows a good correlation with a limit of agreement within 2SD¹⁵ and no significant difference on result.¹⁰^,¹² Bian et al. (2011)²⁵ compared the octane breath test to USG and found a significantly similar result on variables. Another study by Jūngling et al. (2001)⁵¹ used USG as the standard method to assess oatmeal test sensitivity and specificity. All results showed a favorable tendency on USG use for gastric emptying measurement except for one study by Maheshwari et al. (2021),⁴⁴ which found poor concordance in gastric evaluation compared to endoscopy to examine residual gastric volume. However, the poor correlation needs further investigation as it might be resulted from other factors (i.e., poor measurement technique, suboptimal positioning, clinician's expertise, etc.).⁴⁴ The capability of USG to assess real-time emptying and the gastric area remains superior for USG compared to GES.²⁸^,²⁹ Furthermore, Zhou et al. (2001),⁶¹ Murray (2005),⁵⁷ and Vogelberg (1988)¹⁷ also highlight the possible use of USG to monitor gastric improvement after ghrelin, metoclopramide, and cisapride medication. Therefore, the use of USG in GES requires a standardized clinical trial or more extensive study to evaluate the extent of function and possible use of USG in gastric emptying assessment.

Abdominal symptoms were mostly complained by the patient with DM and DG with DGE. Chiu et al. (2014)²⁶ reported that GI symptoms score in DM postprandial decrease less than HC. The top three most complained symptoms were abdominal distension (36.1%–54.7% prevalence),²³^,²⁶^,³⁰ postprandial fullness (19.4%–54.7%),²³^,³⁰ and dysphagia (38.9%).³⁰ The food process in the stomach is complex and requires coordinated actions of all stomach regions. Starting from reservoir function of the fundus, peristaltic mix in the antrum, and lastly, gastric pylorus as the gate filters before the chyme enters duodenum.² Other structures were also involved in the food process, including smooth muscles, vascular system, enteric and extrinsic autonomic nerve, and the interstitial cells of Cajal.⁶² In diabetic patients, changes in gastric anatomy,²⁵^,²⁶ supporting structures⁵¹^,⁵⁶^,⁶² (i.e., autonomic innervation, vascular system),⁶² impaired gastric content distribution,³³ immunological changes,⁶³ and systemic conditions (i.e., hyperglycemic state, hormone production)⁴⁰ were found. These changes disrupt the physiological process of gastric digestion, leading to alteration of emptying time to the complaint of gastric symptoms.⁶² Delays in gastric emptying in DM itself is a spectrum of gastric change, leading to gastroparesis.

There are some limitations in our study. We found that there are very limited data for ultrasonography measurement in a certain population (i.e., patient with marked gas retention, markedly obese due to inability to assess USG results objectively); some studies excluded obese²⁷^,⁴² patients for better representation of the general population. Therefore, further evaluation of ultrasonography measurement in this population is needed. We included postprandial data for every various meal set for each study. A standardized protocol in solid or liquid food packages to evaluate gastric emptying must be established to ensure a correct assessment. Long examination hours for USG (range from 30 minute³⁸ – 8 hours⁵³) might not be viable for every situation. Therefore a further study to evaluate shorter analysis, or a standardized time for USG assessment is advised. We also acknowledge that there are potential publication bias in our study based on the Begg’s funnel plot assessment. Aside from the limitations, to the best of our knowledge, this is the first meta-analysis that evaluates the ultrasonography findings in DM and DG that includes various study designs with no language exclusion and included studies from all countries worldwide.

Conclusion

In conclusion, DM and DG could affect gastric anatomic and physiologic function, which results in prolonged emptying time and gastric symptoms. Wider antral area, longer gastric emptying time, longer half-emptying time, reduced gastric emptying rate, and less antral contraction were found in both populations. This study supports the use of ultrasonography for screening and diagnostic methods to treatment monitoring for DGE. However, these findings were based on observational studies, in which nonuniform definitions exist for several outcomes. Therefore, randomized controlled trials are advised for future studies.

Data availability

Underlying data

All data underlying the results are available as part of the article and no additional source data are required

Extended data

Open Science Framework: Ultrasonography Findings in Diabetes and Diabetes Gastroparesis: A meta-analysis. https://doi.org/10.17605/OSF.IO/YQ4XN.⁶⁴

This project contains the following extended data:

- Suppl 1 Literature Search.docx (Literature search methodology, Boolean keywords, and list of databases)
- Suppl 2 Quality Assessment.xlsx (Quality assessment of the included studies)
- Suppl 3 Forest Plot for all outcomes.docx (Meta-analysis forest plots for all outcomes)
- Suppl 4 Begg’s Funnel Plot for all outcome.docx (Begg’s funnel plot assessment for evaluation of risk of bias of the included studies)
- Database search.xlsx (Raw datavase search result)

Reporting guidelines

Open Science Framework: PRISMA checklist for ‘Ultrasonography findings in diabetes and diabetes gastroparesis: A meta-analysis’. https://doi.org/10.17605/OSF.IO/YQ4XN.⁶⁴

Data are available under the terms of the Creative Commons Zero “No rights reserved” data waiver (CC0 1.0 Public domain dedication).

Acknowledgments

The authors would like to thank the division of Gastroenterology, Department of Internal Medicine, Central General Hospital Cipto Mangunkusumo and Staffs of Faculty of Medicine, Universitas Indonesia for the support throughout the writing process. We thank our colleagues, Humaira Jasmeen and Livia Assyifa Rachman who provided insight and useful suggestions.

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¹ University of Indonesia, Jakarta Pusat, DKI Jakarta, 10430, Indonesia
² Department of Gastroenterology, National General Hospital Dr. Cipto Mangunkusumo, University of Indonesia, Jakarta Pusat, DKI Jakarta, 10430, Indonesia
³ Department of Radiology, University of Indonesia, Jakarta Pusat, DKI Jakarta, 10430, Indonesia
⁴ Department of Endocrinology, National General Hospital Dr. Cipto Mangunkusumo, University of Indonesia, Jakarta Pusat, DKI Jakarta, 10430, Indonesia

Marcellus Simadibrata
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Amanda Pitarini Utari
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Alvita Dewi Siswoyo
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Elsha Stephanie Anastasia
Roles: Conceptualization, Formal Analysis, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Trifonia Pingkan Siregar
Roles: Resources, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

Dyah Purnamasari
Roles: Resources, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

Competing interests

No competing interests were disclosed.

Grant information

The authors received funding for this research from Research and Community Service Information Base of Indonesia (Badan Informasi Penelitian dan Pengabdian Kepada Masyarakat Indonesia – BIMA Indonesia). Nomor: NKB-793/UN2.RST/HKP.05.00/2022 The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Simadibrata M, Utari AP, Siswoyo AD et al. Ultrasonography findings in diabetes and diabetes gastroparesis: A meta-analysis [version 1; peer review: 1 not approved]. F1000Research 2023, 12:1066 (https://doi.org/10.12688/f1000research.128672.1)

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Michael Camilleri, Mayo Clinic Minnesota, Rochester, Minnesota, USA

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This is an interesting attempt to evaluate the potential role of ultrasonography in evaluating gastric motor functions in patients with diabetes and those with diabetic gastroparesis. A meta analysis was performed, and the studies included were reported to be at ... Continue reading

This is an interesting attempt to evaluate the potential role of ultrasonography in evaluating gastric motor functions in patients with diabetes and those with diabetic gastroparesis. A meta analysis was performed, and the studies included were reported to be at some risk of bias, and some of the studies actually included were abstract which presumably would not have sufficient information to appraise methodology.

MAJOR COMMENTS
1. The use of ultrasonography assesses the emptying of predominantly liquid meals, and the relevance of liquid or homogenized food to gastric emptying in patients with diabetes and particularly those with diabetic gastroparesis is unclear. Specifically the literature has documented extensively that the problem in patients with diabetic gastroparesis pertains to the emptying of solids not liquids or homogenized food

2. while the measurement of antral cross-sectional area is likely to be accurate, it is unclear whether this represents an evaluation of the accommodation response of the stomach, or whether it is a reflection of impairment of gastric emptying; ultrasonography is also unable to appraise the proximal portion of the stomach because of interference by the ribcage and therefore another important component of motor function of the stomach can not be assessed

3. while ultrasonography can certainly measure wall motion and contractions of the stomach, and these appeared to be diminished in patients with diabetic gastroparesis, the degree of wall motion as not been correlated with the amplitude of contractions or the treat duration force that is associated with the wall motion and therefore the method does not allow for further evaluation of the quantitative motor function of the antrum of the stomach which is critically important for trituration of solid food and emptying.

In summary while ultrasonography does identify findings in diabetes and gastroparesis that may differentiate gastric function from healthy controlled, it is insufficiently quantitative from the perspective of the important emptying of solids, as well as the impact of the measured antral contractions on either trituration or propulsion of food from the stomach

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

I cannot comment. A qualified statistician is required.
Are the conclusions drawn adequately supported by the results presented in the review?

Partly
If this is a Living Systematic Review, is the ‘living’ method appropriate and is the search schedule clearly defined and justified? (‘Living Systematic Review’ or a variation of this term should be included in the title.)

Not applicable

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: gastroenterology; motility

I confirm that I have read this submission and believe that I have an appropriate level of expertise to state that I do not consider it to be of an acceptable scientific standard, for reasons outlined above.

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Michael Camilleri, Mayo Clinic Minnesota, Rochester, USA

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11 Aug 2025 | for Version 1

Michael Camilleri, Mayo Clinic Minnesota, Rochester, Minnesota, USA

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Not Approved

This is an interesting attempt to evaluate the potential role of ultrasonography in evaluating gastric motor functions in patients with diabetes and those with diabetic gastroparesis. A meta analysis was performed, and the studies included were reported to be at some risk of bias, and some of the studies actually included were abstract which presumably would not have sufficient information to appraise methodology.

MAJOR COMMENTS
1. The use of ultrasonography assesses the emptying of predominantly liquid meals, and the relevance of liquid or homogenized food to gastric emptying in patients with diabetes and particularly those with diabetic gastroparesis is unclear. Specifically the literature has documented extensively that the problem in patients with diabetic gastroparesis pertains to the emptying of solids not liquids or homogenized food

2. while the measurement of antral cross-sectional area is likely to be accurate, it is unclear whether this represents an evaluation of the accommodation response of the stomach, or whether it is a reflection of impairment of gastric emptying; ultrasonography is also unable to appraise the proximal portion of the stomach because of interference by the ribcage and therefore another important component of motor function of the stomach can not be assessed

3. while ultrasonography can certainly measure wall motion and contractions of the stomach, and these appeared to be diminished in patients with diabetic gastroparesis, the degree of wall motion as not been correlated with the amplitude of contractions or the treat duration force that is associated with the wall motion and therefore the method does not allow for further evaluation of the quantitative motor function of the antrum of the stomach which is critically important for trituration of solid food and emptying.

In summary while ultrasonography does identify findings in diabetes and gastroparesis that may differentiate gastric function from healthy controlled, it is insufficiently quantitative from the perspective of the important emptying of solids, as well as the impact of the measured antral contractions on either trituration or propulsion of food from the stomach

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

I cannot comment. A qualified statistician is required.
Are the conclusions drawn adequately supported by the results presented in the review?

Partly
If this is a Living Systematic Review, is the ‘living’ method appropriate and is the search schedule clearly defined and justified? (‘Living Systematic Review’ or a variation of this term should be included in the title.)

Not applicable

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

gastroenterology; motility

I confirm that I have read this submission and believe that I have an appropriate level of expertise to state that I do not consider it to be of an acceptable scientific standard, for reasons outlined above.

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Ultrasonography findings in diabetes and diabetes gastroparesis: A meta-analysis

Abstract

Keywords

Introduction

Methods

Search strategy

Study selection

Figure 1. Search strategy following the PRISMA 2020 flow diagram for new systematic reviews.19

Data extraction

Quality assessment

Table 1. Quality assessment.

Operational definitions

Data synthesis and analysis

Results

Table 2. Characteristics of the included study and the quality assessment.

Primary outcomes

Table 3. Summary of meta-analysis’ plots.

Figure 2. Antral cross-sectional area.

Figure 3. Gastric emptying time.

Figure 4. Gastric half-emptying time.

Figure 5. Gastric emptying rate.

Figure 6. Antral contraction.

Publication bias

Figure 7. Publication bias assessment funnel plot of (A) antral area (B) gastric emptying time (GET) (C) gastric half-emptying time (GE50) (D) gastric emptying rate (GER) (E) antral contraction.

Discussion

Conclusion

Data availability

Underlying data

Extended data

Reporting guidelines

Acknowledgments

References

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Figure 1. Search strategy following the PRISMA 2020 flow diagram for new systematic reviews.¹⁹