Non-invasive techniques for the diagnosis of Helicobacter pylori infection
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1 REVIEW Non-invasive techniques for the diagnosis of Helicobacter pylori infection L. Gatta, C. Ricci, A. Tampieri and D. Vaira Department of Internal Medicine and Gastroenterology, Nuove Patologie, Bologna, Italy Helicobacter pylori infection can be diagnosed by invasive techniques requiring endoscopy and biopsy (histologic examination, culture, polymerase chain reaction), and non-invasive techniques (serology, urea breath test, urine or blood, detection of H. pylori antigen in stool specimen). However, recent studies have demonstrated that a strategy of `testing and treating' for H. pylori in uninvestigated, young (<50 years), dyspeptic patients in primary care is safe and reduces the need for endoscopy. Indeed, a number of clinical guidelines recommend non-invasive testing in dyspeptic patients followed by treatment of H. pylori in primary care based on clinical and economic analyses. Several non-invasive tests are currently available on the market. The choice depends on the clinical circumstances, the likelihood ratio of positive and negative tests, the cost-effectiveness of the testing strategy, and, nally, the availability of the tests. Nevertheless, two non-invasive tests are commonly used: the urea breath test, and the stool antigen test. Keywords Helicobacter pylori, dyspepsie, diagnosis, non invasive tests Accepted 9 December 2002 Clin Microbiol Infect 2003; 9: 489±496 INTRODUCTION In 1983, a report was published of unidenti ed gastric bacteria [1]. Since the discovery of Helicobacter pylori, we have learned much about this pathogen. It is one of the most common causes of chronic infection in humans [2], causes peptic ulcer disease and chronic gastritis, and is also strongly associated with gastric malignancies: indeed, it has been classi ed as a Class I carcinogen [3]. H. pylori infection can be diagnosed by invasive techniques (i.e. requiring endoscopy and biopsy), and non-invasive techniques. Historically, the diagnosis of H. pylori infection has been based on histologic examination of biopsy samples taken during endoscopy, culture, and the rapid urease test. However, endoscopy is expensive, is unpleasant for patients, and carries a small but de nite risk of complications [4]. Thus, the use of Corresponding author and reprint requests: D. Vaira, Department of Internal Medicine and Gastroenterology, Nuove Patologie, Via Massarenti 9, 40138, Bologna, Italy Tel: Fax: vairadin@med.unibo.it non-invasive tests to diagnose H. pylori infection is becoming more frequent. Furthermore, several guidelines recommend the use of non-invasive tests as rst-line treatment in the management of dyspepsia [5±7]. There are several non-invasive tests for the diagnosis of H. pylori infection. Choosing the `right' non-invasive test is not easy, and several aspects need to be considered: sensitivity, speci city, and the post-test probability of having or not having the infection following a positive or negative result [8]. We also have to look carefully at the clinical situation, i.e. pre-test probability of the infection in our population, the age of the patients, their present complaints, and past medical history. Finally, we have to consider economic evaluations that assess the costs and the consequences of the alternative strategies for the detection and/or management of H. pylori infection. There are two different types of non-invasive test: direct and indirect (Figure 1). The direct tests look for direct evidence of the presence of H. pylori. The stool test assesses the presence of bacterial antigens in stool. Indirect tests assess the presence of the infection by evaluating indirect evidence such as the presence of antibodies to H. pylori, or the amount of labeled CO 2 in the breath, an expression of the urease activity of the bacterium. ß 2003 Copyright by the European Society of Clinical Microbiology and Infectious Diseases
2 490 Clinical Microbiology and Infection, Volume 9 Number 6, June 2003 Figure 1 Non-invasive tests. NON-INVASIVE INDIRECT TECHNIQUES Immunologic tests Serologic tests The serologic tests are based on the detection of speci c anti-h. pylori IgG antibodies in the patient's serum. Serology was the rst non-invasive technique, even though, in principle, it has limitations. The most important is that we are not able to distinguish between active infection and a previous `contact'. Antibody levels persist in the blood for long periods of time, and as more and more patients with H. pylori infection are treated, persistent antibodies will lead to false-positive results. A meta-analysis of 21 studies with commercially available ELISA serology kits reported overall sensitivity and speci city of 85% and 79%, respectively [9]. Furthermore, the Medical Devices Agency of Great Britain evaluated a large number of ELISA tests [10]. Five hundred and eighty-eight samples of sera were assessed with 16 different tests. The overall accuracy of the assays averaged 78% (range 68±82%)for all sera. Thus, the accuracy of these tests is no longer adequate to justify their use on clinical or economic grounds. However, there are other elds in which serology can be useful, such as: large epidemiologic surveys, studies on age at acquisition of the infection, and assessment of detection of antibodies against the two important proteins CagA and VacA using different techniques (ELISA, recombinant immunoblot assay, Western blot)for research purpose. CagA and VacA are two important pathologic markers. The former is a 120-kDa protein with high immunogenic power, and its gene (caga)is located in the pathogenicity island (PAI)of the chromosome of H. pylori. Individuals infected with CagA-positive strains of H. pylori have a more severe in ammatory reaction, a greater degree of gastric atrophy and intestinal metaplasia, and a higher incidence of duodenal ulcer and intestinal-type gastric cancer [11]. The vacuolating toxin (VacA)is an 87-kDa protein, and its gene is situated a signi cant distance from the PAI. However, it is secreted by Helicobacter strains, that contain the PAI. It is activated at low ph, is resistant to acid and pepsin, causes vacuolation in cell culture in vitro, and damages mouse gastric epithelium in vivo [12]. A comparison of two anti-caga ELISA tests (HeloriCTX, Eurospital It)showed sensitivity and speci city of 100% and 76%, and 90% and 94%, respectively [13]. Western blotting has been developed into commercial test kits; in recent studies, Helico-blot 2.0 and Recombinant Immunoblot Assay Strip (RIBA)showed good sensitivity and speci city [14]. Near patient tests Near patient tests were developed to provide rapid diagnosis of H. pylori infection in clinics or physicians' of ces. They are technically simple to perform, and most of them currently use one-step tools on a drop of whole blood, while others require separation of serum, which diminishes their usefulness as near patient kits. Nevertheless, general remarks can be made about these tests. The most accurate `blood test' detects serum antibodies from clotted blood taken at venesection. Fingerprick test results can vary when there is dif culty in obtaining a drop of blood. Squeezing the nger can change the hematocrit by mixing tissue uid with the blood sample, changing the concentration of antibody in the serum. Whole blood tests are
3 Gatta et al Non-invasive techniques for diagnosis of H. pylori infection 491 in uenced by chylomicrons, which may affect the permeability of the blood plasma through the various membranes used in diagnostic tests. Recent evidence accumulated from 3805 patients in eight studies performed in 1999±2000 suggests that these tests have considerably lower sensitivity and speci city than originally assumed. The mean sensitivity (weighted for number of patients studied)was 71.1%, and the speci city was 87.6% [15]. Tests on saliva and urine Some studies have looked at saliva and urine as possible non-invasive samples in which to detect antibodies to H. pylori. However, results with the salivary assay have been disappointing (sensitivity 81%, speci city 73%)[16]. Regarding urine, there has been a study reporting sensitivity and speci- city of 86% and 91% in 132 patients [17]. However, these data have not been con rmed by a multicenter European trial using the same urine assay in a large population, where sensitivity and speci city of 89% and 69%, respectively, were reported [18]. Urease activity-based tests Urea breath test H. pylori is a strong urease producer. This enzyme splits urea into ammonia and CO 2. The test is based on this. Patients ingest urea labeled with either 13 Cor 14 C, and the labeled urea comes into contact with the mucosa and diffuses through the mucus towards the H. pylori and the mucosal blood supply. Urea hydrolysis occurring within the mucous layer produces ammonia and labeled CO 2. This is close to the epithelial blood supply, and, because of the concentration gradient, within a few minutes the labeled CO 2 will appear in the breath. Several doses of 14 C-labeled urea have been used in clinical studies, ranging from 37 kbq (1 mci)to 185 kbq (5 mci). Labeled urea is usually given to the patient with a test meal, to delay gastric emptying. After ingestion of the urea, breath samples are collected for up to 20 min by the patient exhaling into a CO 2 -trapping agent (hyamine). The radioactivity of each sample is measured by a scintillation counter, and the results are expressed as a percentage of the administered dose, adjusted for endogenous CO 2 production, or directly as counts/min. The sensitivity and speci city of the test are about 97% and 95%, respectively. However, the 14 C-urea breath test is reported to be unreliable in assessing patients who have had gastric surgery, and in patients who have been receiving proton pump inhibitors or ranitidine [19]. Recently, a new device for 14 C-urea breath testing has been described [20]. It uses a at breath card, which is able to adsorb exhaled CO 2 via chemical bonding. This card is then read using a small analyzer with a slot into which the card is put. This type of device might became a genuine `near patient test', where 14 C-urea breath testing is allowed, since it is easy to perform and has the advantage of being cheaper than 13 C-urea breath testing. However, concern with 14 C usually arises because of its long half-life, and the amount of radiation. Munster et al. reported that approximately 90% of the 14 C from a urea breath test is eliminated as CO 2 in the breath or urine after 3 days; the amount of isotope retained in the body is negligible [21]. Furthermore, the cumulative lifetime radiation exposure from this test has been calculated to be not more than 0.3 mrem/mci, which is considered to be equal to the background radiation that a person is exposed to in 1 day [22]. For this reason, the 1-mCi 14 C dose has been permitted, without restriction, for general use in the USA (Nuclear Radioactive Drug Committee, USA, us10fcr Radioactive drug), while in Europe the 14 C-urea breath test cannot yet be used with children and women of childbearing age. The 13 C-urea breath test is identical to the 14 C-urea breath test, except that 13 C is a non-radioactive isotope of 12 C, and its detection requires a mass spectrometer rather than a scintillation counter. Because 13 C is a naturally occurring isotope, it is measured as a ratio of 12 C, which is the most abundant isotope [23,24]. The 13 C-urea breath test is based on a simple principle: in the presence of H. pylori, isotopically labeled urea is rapidly hydrolyzed by the bacteria's urease, and the released CO 2 exhaled in the expired breath. Since its rst description by Graham et al. [25], who used 350 mg of 13 C-urea, this test has been extensively modi ed, including variations in the dose of labeled urea, sampling time, test meal, and cutoff values. These modi cations have been designed to reduce the duration of the test, improve its accuracy, or reduce the amount of the expensive substrate ( 13 C)used in the test. Tests employing a dose of 75 mg of 13 C-urea have proved to be as accurate as those using higher amounts, and are less expensive. This dose has been increasingly adopted in research studies, as
4 492 Clinical Microbiology and Infection, Volume 9 Number 6, June 2003 well as in most of the commercially available diagnostic kits [26]. Conventional urea breath test protocols use a test meal to delay gastric emptying and to allow time for an even distribution of the 13 C throughout the stomach. However, there is evidence that absence of a test meal does not affect accuracy [27]. Another area in which improvements in the conventional breath test have been possible is the duration of the test. Many breath test protocols require a baseline sample and another sample obtained 30 min after ingestion of the 13 C. Recently, a new type of urea breath test has been described that uses a tablet formulation of 13 C-urea, which allows breath sampling to be performed as early as 10 min after ingestion of the tablet with excellent accuracy [28,29]. Furthermore, the advantage of supplying the urea solution in a tablet is that interference from ureaseproducing bacteria in the oropharynx, which may cause false-positive results in earlier breath test protocols, is avoided [30,31]. Analysis of the results from studies in which the tests were evaluated against an accepted standard con rms their accuracy. In 3643 patients studied in 1999±2000, the weighted means for the sensitivity and speci- city of the urea breath test were 94.7% and 95.7%, respectively [15]. Serum bicarbonate The assessment of 13 C-bicarbonate from serum samples after oral ingestion of 13 C urea is not practicable for a urea breath test [32]. However, it was recently reported to have good accuracy in the post-treatment setting. Ammonia vapor Recently, a new device for assessing the presence of H. pylori infection has been described. It uses the urease activity of the bacterium, but in a different way (Figure 2). Urea is split into ammonia and CO 2. If the gastric ph is suf ciently high (ph > 9.25), ammonia gas can be detected in the breath [33]. The theoretical advantages of this test are important. It does not require any type of urea, because the test uses the physiologic amount of the urea present in the stomach. Furthermore, to raise the ph in the stomach, all that is needed is a glass of sparkling water and a little magnesium. At present, we only have preliminary results from 10 patients, but more studies are required on a method that might dramatically change the cost of the diagnosis. Figure 2 Detection of ammonia vapor in the mouth. NON-INVASIVE DIRECT TECHNIQUES Stool antigen test Over the last few years, an enzyme immunoassay (EIA)that detects the presence of H. pylori antigen in stool specimens has become available, and has undergone testing for the initial diagnosis of H. pylori infection and for the con rmation of eradication after treatment (Figure 3). A polyclonal anti- H. pylori capture antibody absorbed to microwells is the most widely used [34] test, but a monoclonal antibody test has been recently described. The polyclonal antibody test has been extensively evaluated in the diagnosis of H. pylori infection before therapy. In studies performed during 1999 and the rst 6 months of 2001, 3419 patients were evaluated, and the weighted means for sensitivity and speci city were 93.2% and 93.2%, respectively [15]. These studies suggest that the test is comparable to the urea breath test for the initial detection of H. pylori infection. Consequently, the European Helicobacter Pylori study group has recommended the use of the urea breath test or stool testing in the initial diagnosis of H. pylori infection. There has been some variability in the results reported by different investigators in the post-therapy setting. Some of these differences may be due to the standard used for comparisons. In the studies performed during 1999 and the rst 6 months of 2001, which used standards as recommended by the working party of the European H. pylori study group, 332 patients were evaluated. The weighted mean sensitivity and speci city of the polyclonal test were 92.1% and 87.6%, respectively. However, in the studies performed during the same period, which used only the urea breath test as a comparator, 790 patients were evaluated,
5 Gatta et al Non-invasive techniques for diagnosis of H. pylori infection 493 Figure 3 Stool antigen test: how does it work? with weighted mean sensitivity and speci city of 88.8% and 87.3% being reported [15]. Although more studies in the post-therapy setting are necessary, the European Helicobacter study group (Maastricht 2000)has suggested that the polyclonal stool test may be an alternative to breath testing after treatment [5]. In addition, a recent study showed the reliability of the polyclonal test in identifying patients still infected as early as 14 days after the end of the treatment (Table 1) [35]. For monoclonal antibodies, only two full articles have been published. The rst, in a pretreatment setting, found a sensitivity and speci city of 96.3% and 88.5%, respectively, in 53 Table 1 Early follow-up with the polyclonal stool test Day a Probability that the patients still have H. pylori infection at day 35 Probability that the patients will be free of H. pylori infection at day 35 patients, while the second, in a post-treatment setting, assessed sensitivity and speci city as 88.6% and 94.7% in 178 patients [36,37]. However, despite the encouraging results, more studies need to be performed on the monoclonal test. CONCLUSIONS Non-invasive tests are becoming more and more important in the clinical management of the dyspeptic patient. Indeed, a number of clinical guidelines recommend non-invasive testing in dyspeptic patients, followed by treatment of H. pylori in primary care: the Maastricht II European Consensus, the European Society for Primary Care Gastroenterology, and the American Gastroenterological Association [5±7]. All recommend a `test and treat' strategy in patients under 45 or 55 years and with no alarm symptoms (i.e. anemia, weight loss, dysphagia, palpable mass, malabsorption, etc.)(figure 4). There are several sources of clinical evidence on which this strategy is founded. McColl et al. recently performed a randomized, controlled trial on 708 dyspeptic patients, and (95% CI: 0.19±0.99)(95% CI: 0.74±0.91) (95% CI: 0.69±1)(95% CI: 0.82±0.97) reported that, in patients less than 55 years of (95% CI: 0.68±1)(95% CI: 0.87±0.99) age with uncomplicated dyspepsia, `test and treat' (95% CI: 0.77±0.96)(95% CI: 0.89±1) was as effective and safe as endoscopy. Furthermore, they found that the strategy was as reassur- (95% CI: 0.71±1)(95% CI: 0.94±1) ing to the patients as endoscopy [38]. Similarly, Arents et al. showed that the `test and treat' strategy reduced the total number of endoscopies a Days after start of treatment. by 62% as compared with a prompt Positive or negative for H. pylori by biopsies 35 days after start of treatment. endoscopy
6 494 Clinical Microbiology and Infection, Volume 9 Number 6, June 2003 Figure 4 Management of uninvestigated dyspepsia. strategy, with similar outcomes in dyspeptic symptoms, quality of life, and patient satisfaction [39]. It has also been shown that the cost of management per patient per year for dyspeptic patients of the `test and treat' strategy was , while that of endoscopy was [40]. This strategy seems also to reduce the morbidity of dyspeptic patients. In a preliminary study performed on 267 dyspeptic patients recruited from a large car company, Madisch et al. found that the H. pylori `test and treat' strategy was effective in reducing both disease-related direct costs (i.e. antacid consumption, house doctor consultations)and indirect costs (i.e. absenteeism from work)[41]. The cost-effectiveness of diagnostic testing was evaluated recently in an economic model. The costs of different testing strategies were evaluated when the pretest probability was low, intermediate, or high. In general, the cost of serology is low in most countries, while the urea breath test and the stool antigen test are more expensive. Despite this, the improved accuracy of the stool and breath tests makes either of these tests cost-effective compared to serology or near patient tests. The lower the prevalence (and the pretest probability of infection), the less useful are serology and whole blood tests [42]. However, some other considerations need to be taken into account. If we consider what test patients would prefer, there is little doubt that this is urea breath test. However, if we consider the issue from the point of view of the healthcare providers, things are different. The cost of a mass spectrophotometer is high, its service requirements for one year are extremely expensive, not including spare parts, and, nally, dedicated personnel are needed. On the other hand, the stool test only requires an optical spectrophotometer, which is usually present in any laboratory, with negligible costs for maintenance or spare parts. Also, it does not require dedicated personnel. Hence, the breath test may be the best in private practice, but not in the national healthcare system, where, probably, the stool test is more cost-effective. REFERENCES 1. Warren JR, Marshall BJ. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 1983; I: 1273±5. 2. Graham DY. Therapy of Helicobacter pylori: current status and issues. Gastroenterology 2000; 118: S2±8. 3. International Agency for Research on Cancer, World Health Organization. Infection with Helicobacter pylori. In: Schistosomes, liver flukes and Helicobacter pylori. Lyon: IARC, 1994: 177± complication_upergi.asp 5. Malfertheiner P, Megraud F, O'Morain C et al. Current concepts in the management of H. pylori infection- The Maastricht Consensus Report. Aliment Pharmacol Ther 2002; 16: 167± Rubin G, Meineche-Schmidt V, Roberts A, Childs S, de Wit N. The management of H. pylori infection in primary care. Guidelines from the ESPCG. Eur J Clin Pract 1999; 5: 98± American Gastroenterological Association. Medical position statement. Evaluation of dyspepsia. Gastroenterology 1998; 114: 579± Sackett DL, Haynes BR, Guyatt GH, Tugwell P. Clinical epidemiology: a basic science for clinical medicine. In: Sackett DL, Hayness RB, Guyatt GH, Tugwell P, eds. Interpretation of diagnostic data, 2nd edn. London: Little, Brown, 1985: 69± Loy CT, Irwig LM, Katelaris PH et al. Do commercial serological kits for Helicobacter pylori infection
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Am J Gastroenterol 1993; 88: 1865± Moulton-Barret RG, Triadafilopoulos G, Michener R, Gologorsky D. Serum 13 C bicarbonate in the assessment of gastric Helicobacter pylori urease activity. Am J Gastroenterol 1993; 88: 369± Dun CDR, Blac M, Cowell DC et al. Ammonia vapour in the mouth as a diagnostic marker for Helicobacter pylori infection: preliminary proof of principal pharmacological investigations. Br J Biomed Sci 2000; 58: 66± Vaira D, Malfertheiner P, Megraud F et al. Diagnosis of Helicobacter pylori infection with a new noninvasive antigen-based assay. Lancet 1999; 354: 30± Vaira D, Vakil N, Menegatti M et al. The stool antigen test for detection of Helicobacter pylori after eradication therapy. Ann Intern Med 2002; 136: 280± Agha-Amiri K, Peitz U, Mainz D, Kahl S, Leodolter A, Malfertheiner P. A novel immunoassay based on monoclonal antibodies for the detection of Helicobacter pylori antigens in human stool. 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8 496 Clinical Microbiology and Infection, Volume 9 Number 6, June 2003 compared with non-invasive H. pylori testing alone in the management of dyspepsia. BMJ 2002; 324: 999± Arents NL, Thijs JC, Van Zwet AA, Kleibeur JH. Screening and treating for Helicobacter pylori (`test and treat strategy')in dyspepsia reduces number of endoscopies with similar clinical outcome as compared to prompt endoscopy. Gastroenterology 2001; 120: Jones R, Tait C, Sladen G, Weston-Baker J. A trial of a test and treat strategy for Helicobacter pylori positive dyspeptic patients in general practice. Int J Clin Pract 1999; 53: 413± Madisch A, Grabowski G, Guth A, von Guericke O. Hp test and treat strategy reduces both diseaserelated absenteeism from work, house doctor consultations and antacid consumption in uninvestigated dyspeptic staff members of a large factory. Gastroenterology 2001; 120: Vakil N, Rhew D, Soll A, Ofman J. The costeffectiveness of diagnostic testing strategies for H. pylori. Am J Gastroenterol 2000; 95: 1691±8.
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