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Meta-Analysis
. 2018 Mar 15;3(3):CD012080.
doi: 10.1002/14651858.CD012080.pub2.

Non-invasive diagnostic tests for Helicobacter pylori infection

Lawrence Mj Best  1 , Yemisi Takwoingi, Sulman Siddique, Abiram Selladurai, Akash Gandhi, Benjamin Low, Mohammad Yaghoobi, Kurinchi Selvan Gurusamy
Affiliations
Meta-Analysis

Non-invasive diagnostic tests for Helicobacter pylori infection

Lawrence Mj Best et al. Cochrane Database Syst Rev. .

Abstract

Background: Helicobacter pylori (H pylori) infection has been implicated in a number of malignancies and non-malignant conditions including peptic ulcers, non-ulcer dyspepsia, recurrent peptic ulcer bleeding, unexplained iron deficiency anaemia, idiopathic thrombocytopaenia purpura, and colorectal adenomas. The confirmatory diagnosis of H pylori is by endoscopic biopsy, followed by histopathological examination using haemotoxylin and eosin (H & E) stain or special stains such as Giemsa stain and Warthin-Starry stain. Special stains are more accurate than H & E stain. There is significant uncertainty about the diagnostic accuracy of non-invasive tests for diagnosis of H pylori.

Objectives: To compare the diagnostic accuracy of urea breath test, serology, and stool antigen test, used alone or in combination, for diagnosis of H pylori infection in symptomatic and asymptomatic people, so that eradication therapy for H pylori can be started.

Search methods: We searched MEDLINE, Embase, the Science Citation Index and the National Institute for Health Research Health Technology Assessment Database on 4 March 2016. We screened references in the included studies to identify additional studies. We also conducted citation searches of relevant studies, most recently on 4 December 2016. We did not restrict studies by language or publication status, or whether data were collected prospectively or retrospectively.

Selection criteria: We included diagnostic accuracy studies that evaluated at least one of the index tests (urea breath test using isotopes such as 13C or 14C, serology and stool antigen test) against the reference standard (histopathological examination using H & E stain, special stains or immunohistochemical stain) in people suspected of having H pylori infection.

Data collection and analysis: Two review authors independently screened the references to identify relevant studies and independently extracted data. We assessed the methodological quality of studies using the QUADAS-2 tool. We performed meta-analysis by using the hierarchical summary receiver operating characteristic (HSROC) model to estimate and compare SROC curves. Where appropriate, we used bivariate or univariate logistic regression models to estimate summary sensitivities and specificities.

Main results: We included 101 studies involving 11,003 participants, of which 5839 participants (53.1%) had H pylori infection. The prevalence of H pylori infection in the studies ranged from 15.2% to 94.7%, with a median prevalence of 53.7% (interquartile range 42.0% to 66.5%). Most of the studies (57%) included participants with dyspepsia and 53 studies excluded participants who recently had proton pump inhibitors or antibiotics.There was at least an unclear risk of bias or unclear applicability concern for each study.Of the 101 studies, 15 compared the accuracy of two index tests and two studies compared the accuracy of three index tests. Thirty-four studies (4242 participants) evaluated serology; 29 studies (2988 participants) evaluated stool antigen test; 34 studies (3139 participants) evaluated urea breath test-13C; 21 studies (1810 participants) evaluated urea breath test-14C; and two studies (127 participants) evaluated urea breath test but did not report the isotope used. The thresholds used to define test positivity and the staining techniques used for histopathological examination (reference standard) varied between studies. Due to sparse data for each threshold reported, it was not possible to identify the best threshold for each test.Using data from 99 studies in an indirect test comparison, there was statistical evidence of a difference in diagnostic accuracy between urea breath test-13C, urea breath test-14C, serology and stool antigen test (P = 0.024). The diagnostic odds ratios for urea breath test-13C, urea breath test-14C, serology, and stool antigen test were 153 (95% confidence interval (CI) 73.7 to 316), 105 (95% CI 74.0 to 150), 47.4 (95% CI 25.5 to 88.1) and 45.1 (95% CI 24.2 to 84.1). The sensitivity (95% CI) estimated at a fixed specificity of 0.90 (median from studies across the four tests), was 0.94 (95% CI 0.89 to 0.97) for urea breath test-13C, 0.92 (95% CI 0.89 to 0.94) for urea breath test-14C, 0.84 (95% CI 0.74 to 0.91) for serology, and 0.83 (95% CI 0.73 to 0.90) for stool antigen test. This implies that on average, given a specificity of 0.90 and prevalence of 53.7% (median specificity and prevalence in the studies), out of 1000 people tested for H pylori infection, there will be 46 false positives (people without H pylori infection who will be diagnosed as having H pylori infection). In this hypothetical cohort, urea breath test-13C, urea breath test-14C, serology, and stool antigen test will give 30 (95% CI 15 to 58), 42 (95% CI 30 to 58), 86 (95% CI 50 to 140), and 89 (95% CI 52 to 146) false negatives respectively (people with H pylori infection for whom the diagnosis of H pylori will be missed).Direct comparisons were based on few head-to-head studies. The ratios of diagnostic odds ratios (DORs) were 0.68 (95% CI 0.12 to 3.70; P = 0.56) for urea breath test-13C versus serology (seven studies), and 0.88 (95% CI 0.14 to 5.56; P = 0.84) for urea breath test-13C versus stool antigen test (seven studies). The 95% CIs of these estimates overlap with those of the ratios of DORs from the indirect comparison. Data were limited or unavailable for meta-analysis of other direct comparisons.

Authors' conclusions: In people without a history of gastrectomy and those who have not recently had antibiotics or proton ,pump inhibitors, urea breath tests had high diagnostic accuracy while serology and stool antigen tests were less accurate for diagnosis of Helicobacter pylori infection.This is based on an indirect test comparison (with potential for bias due to confounding), as evidence from direct comparisons was limited or unavailable. The thresholds used for these tests were highly variable and we were unable to identify specific thresholds that might be useful in clinical practice.We need further comparative studies of high methodological quality to obtain more reliable evidence of relative accuracy between the tests. Such studies should be conducted prospectively in a representative spectrum of participants and clearly reported to ensure low risk of bias. Most importantly, studies should prespecify and clearly report thresholds used, and should avoid inappropriate exclusions.

PubMed Disclaimer

Conflict of interest statement

This report is independent research funded by the National Institute for Health Research (NIHR Cochrane Programme Grants, 13/89/03 ‐ Evidence‐based diagnosis and management of upper digestive, hepato‐biliary, and pancreatic disorders). The views expressed in this publication are those of the author(s) and not necessarily those of the NHS, the National Institute for Health Research or the Department of Health.

LB: none known.

SS: none known.

AS: none known.

AG: none known.

BL: none known.

MY: is an Editor with the Cochrane Upper GI and Pancreatic Diseases (UGPD) Review Group. However, other UGPD Editors were responsible for the editorial processing of this review.

KS: none known.

YT: none known.

Figures

1
1
Clinical pathway
2
2
Study flow diagram.
3
3
Risk of bias and applicability concerns graph: review authors' judgements about each domain presented as percentages across included studies. For each domain, the numbers shown on the bar represent the number of studies that were scored as high, unclear or low in terms of risk of bias or applicability concern.
4
4
Forest plot of urea breath test‐13C.FN = false negative; FP = false positive; TN = true negative; TP = true positive. The forest plot shows an estimate of sensitivity and specificity from each study and the threshold used. Studies are sorted by threshold, sensitivity and specificity. For threshold, the number of minutes in brackets is the time after administration of urea.
5
5
Forest plot of urea breath test‐13C at commonly reported thresholds. FN = false negative; FP = false positive; TN = true negative; TP = true positive. Thresholds are shown in brackets and the number of minutes in brackets is the time after administration of urea.
6
6
Forest plot of urea breath test‐14C. FN = false negative; FP = false positive; TN = true negative; TP = true positive. The forest plot shows an estimate of sensitivity and specificity from each study and the threshold used. Studies are sorted by threshold, sensitivity and specificity. For threshold, the number of minutes in brackets is the time after administration of urea.
7
7
Forest plot of serology. FN = false negative; FP = false positive; SD = standard deviation; TN = true negative; TP = true positive. The forest plot shows an estimate of sensitivity and specificity from each study and the threshold used. Studies are sorted by threshold, sensitivity and specificity. Other threshold is staining of a 120kDa protein (CagA) gel band and/or at least two of five proteins between 28–33 kDa.
8
8
Forest plot of stool antigen test. FN = false negative; FP = false positive; TN = true negative; TP = true positive; WL = wavelength. The forest plot shows an estimate of sensitivity and specificity from each study and the threshold used. Studies are sorted by threshold, sensitivity and specificity.
9
9
Summary ROC plot of non‐invasive tests for H pylori infection. The SROC curves for the four tests are parallel. The curve for each test is drawn within the range of estimates of specificity from the studies included for the test.
10
10
Summary ROC plot of direct comparisons of urea breath test‐13C and serology. Each summary curve was drawn restricted to the range of specificities for each test. The size of each symbol was scaled according to the precision of sensitivity and specificity in the study. A dotted line joins the pair of points for the two tests from each study.
11
11
Summary ROC plot of direct comparisons of urea breath test‐13C and stool antigen test. Each summary curve was drawn restricted to the range of specificities for each test. The size of each symbol was scaled according to the precision of sensitivity and specificity in the study. A dotted line joins the pair of points for the two tests from each study.
12
12
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each study included for urea breath test‐13C
13
13
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each study included for urea breath test‐14C.
14
14
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each study included for serology
15
15
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each study included for the stool antigen test
1
1. Test
Urea breath test‐13C.
2
2. Test
Urea breath test‐14C.
3
3. Test
Urea breath test ‐ Unknown isotope.
4
4. Test
Serology.
5
5. Test
Stool antigen test.
6
6. Test
Urea breath test‐13C (delta over baseline > 3% (20 minutes)).
7
7. Test
Urea breath test‐13C (delta over baseline > 3% (30 minutes)).
8
8. Test
Urea breath test‐13C (delta over baseline > 3.5% (30 minutes)).
9
9. Test
Urea breath test‐13C (delta over baseline > 4% (10 minutes)).
10
10. Test
Urea breath test‐13C (delta over baseline > 4% (20 minutes)).
11
11. Test
Urea breath test‐13C (delta over baseline > 4% (30 minutes)).
12
12. Test
Urea breath test‐13C (delta over baseline > 4.5% (30 minutes)).
13
13. Test
Urea breath test‐13C (delta over baseline > 5% (30 minutes)).
14
14. Test
Urea breath test‐14C (counts per minute > 50).
15
15. Test
Urea breath test‐14C (disintegrations per minute > 200).
16
16. Test
Serology > 7 units/ml.
17
17. Test
Serology ≥300 units.
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    1. Jekarl DW, An YJ, Lee S, Lee J, Kim Y, Park YJ, et al. Evaluation of a newly developed rapid stool antigen test using an immunochromatographic assay to detect Helicobacter pylori. Japanese Journal of Infectious Diseases 2013;66(1):60‐4. - PubMed
Jensen 1998 {published data only}
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Jordaan 2008 {published data only}
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Kamel 2011 {published data only}
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Kuloglu 2008 {published data only}
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Lahner 2004 {published data only}
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Lee 1998 {published data only}
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Logan 1991a {published data only}
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Lombardo 2003 {published data only}
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Lottspeich 2007 {published data only}
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Luthra 1998 {published data only}
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Mana 2001a {published data only}
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Mansour‐Ghanaei 2011 {published data only}
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Misawa 1998 {published data only}
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Mohammadian 2007 {published data only}
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Monteiro 2001a {published data only}
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Morales 1995 {published data only}
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Noguera 1998 {published data only}
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Novis 1991 {published data only}
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Ogata 2001 {published data only}
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Ozturk 2003 {published data only}
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Peitz 2001 {published data only}
    1. Peitz U, Baumann M, Tillenburg B, Borsch G, Stolte M, Malfertheiner P, et al. Insufficient validity of a rapid blood test for diagnosis of Helicobacter pylori infection. Medizinische Klinik 2001;96(12):703‐7. - PubMed
Peura 1996 {published data only}
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Puspok 1999 {published data only}
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Qadeer 2009 {published data only}
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Rafeey 2007 {published data only}
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Rathbone 1986 {published data only}
    1. Rathbone BJ, Wyatt J, Tompkins D, Heatley RV, Losowsky MS. Diagnostic IgG ELISA for gastric campylobacter‐pyloridis infection using serum samples. Gut 1986;27(5):A607.
Safe 1993 {published data only}
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Salles‐Montaudon 2002 {published data only}
    1. Salles‐Montaudon N, Dertheil S, Broutet N, Gras N, Monteiro L, Mascarel A, et al. Detecting Helicobacter pylori infection in hospitalized frail older patients: The challenge. Journal of the American Geriatrics Society 2002;50(10):1674‐80. - PubMed
Schilling 2001 {published data only}
    1. Schilling D, Jakobs R, Peitz U, Sugilla M, Stolte M, Riemann JF, et al. The diagnostic accuracy of (13)C0urea breath test in diagnosis of Helicobacter pylori (hp) infection in patients with partial gastric resection due to peptic ulcer disease. Gastroenterology 1999;116(4 suppl):A304. - PubMed
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Scuderi 2000 {published data only}
    1. Scuderi G, Celi D, Romagnolo M, Lupi A, Alecci L, Dramissino I, et al. Helicobacter pylori: Use of a stool antigen detection test and a six‐day triple therapy [2]. Digestive and Liver Disease 2000;32(1):71‐3. - PubMed
Segamwenge 2014 {published data only}
    1. Segamwenge IL, Kagimu M, Ocama P, Opio K. The utility of the Helicobacter pylori stool antigen test in managing dyspepsia: An experience from a low resource setting. African Health Sciences 2014;14(4):829‐34. - PMC - PubMed
Selcukcan 2011 {published data only}
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Sharbatdaran 2013 {published data only}
    1. Sharbatdaran M, Kashifard M, Shefaee S, Siadati S, Jahed B, Asgari S. Comparison of stool antigen test with gastric biopsy for the detection of Helicobacter pylori infection. Pakistan Journal of Medical Sciences 2013;29(1):68‐71. - PMC - PubMed
Sheu 1998a {published data only}
    1. Sheu BS, Lee SC, Lin PW, Chang YC, Yang SB, Lin XZ. Diagnostic efficacy of carbon 13 urea breath test to detect H. pylori in patients after gastrectomy. Gut 1998;43(Suppl 2):A57.
Sheu 1998b {published data only}
    1. Sheu BS, Lee SC, Lin PW, Chang YC, Yang SB, Lin XZ. Diagnostic efficacy of carbon 13 urea breath test to detect H. pylori in patients after gastrectomy. Gut 1998;43(Suppl 2):A57.
Shin 2009 {published data only}
    1. Shin CM, Kim N, Lee HS, Lee HE, Lee SH, Park YS, et al. Validation of diagnostic tests for Helicobacter pylori with regard to grade of atrophic gastritis and/or intestinal metaplasia. Helicobacter 2009;14(6):512‐9. - PubMed
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Surveyor 1989 {published data only}
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Thobani 1995 {published data only}
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Tiwari 2014 {published data only}
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Vandenplas 1992 {published data only}
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Villalobos 1992 {published data only}
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Yoshimura 2001 {published data only}
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References to studies awaiting assessment

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