Correlation between Quantitative <sup>13</sup>C-Urea Breath Test and <i>Helicobacter pylori</i> Treatment Success in a Population-Based Cohort

Boltin, Doron; Levi, Zohar; Perets, Tsachi Tsadok; Schmilovitz-Weiss, Hemda; Gingold-Belfer, Rachel; Dickman, Ram; Dotan, Iris

doi:https://doi.org/10.1155/2018/5439539

Gastroenterology Research and Practice

On this page

Abstract Introduction Materials and Methods Results Discussion Data Availability Conflicts of Interest References Copyright Related Articles

Research Article | Open Access

Volume 2018 | Article ID 5439539 | https://doi.org/10.1155/2018/5439539

Correlation between Quantitative ¹³C-Urea Breath Test and Helicobacter pylori Treatment Success in a Population-Based Cohort

Doron Boltin,¹Zohar Levi,¹Tsachi Tsadok Perets,²Hemda Schmilovitz-Weiss,¹Rachel Gingold-Belfer,¹Ram Dickman,¹and Iris Dotan¹

Academic Editor: Tatsuya Toyokawa

Received15 Jul 2018

Revised07 Oct 2018

Accepted24 Oct 2018

Published13 Nov 2018

Abstract

Background. There are continual efforts to identify factors which influence the success of first-line therapy for Helicobacter pylori (H. pylori) infection. The ¹³C-urea breath test result (C13-UBT) utilizes H. pylori urease activity and is a highly accurate diagnostic assay. We aimed to determine whether the magnitude of C13-UBT result is related to treatment success. Methods. Adult patients who underwent a first-time ¹³C-urea breath test between January 2010 and January 2016 were included. In order to isolate a naïve test-and-treat population who were unlikely to have undergone an initial endoscopy-based H. pylori test, we excluded patients > 45 years and those with a previous C13-UBT. Data were extracted from the Clalit Health Services laboratory database. Results. A total of 94,590 subjects (36.1% male, age 28.5 ± 6.0 years) who underwent a first-time C13-UBT during the study period were included. C13-UBT was positive in 48,509 (51.3%) subjects. A confirmatory posttreatment C13-UBT was performed in 18,375 (37.8%), and eradication was successful in 12,018 (65.4%). The mean C13-UBT recording was 20.6 ± 16.2 DOB in subjects with successful eradication and 19.5 ± 13.1 DOB in subjects with treatment failure (OR, 1.01; 95% CI 1.00-1.01, ). Among patients in the upper quintile of C13-UBT measurement, eradication was achieved in 67.6%, compared to 62.6% in the lower quintile (OR, 1.22; 95% CI 1.11-1.35, ). Subjects in the top 1 percentile (C13-UBT ≥ 70 DOB) achieved eradication in 75.0%, compared to 65.3% among subjects with C13-UBT < 70 DOB (OR, 1.59; 95% CI 1.05-2.41, ). Conclusions. The superiority in H. pylori eradication observed in subjects with a higher C13-UBT DOB is small but significant. Further studies should examine the physiological and microbiological basis for this finding.

1. Introduction

Helicobacter pylori (H. pylori) infection affects up to 50% of the world’s population and is the leading cause of peptic ulcer disease, gastric cancer, and MALT lymphoma [1]. The most widely available and accurate noninvasive test for the diagnosis of H. pylori is the ¹³C-urea breath test (C13-UBT) [2]. This test exploits the urease-producing characteristic of the organism and involves measuring expired ¹³CO₂ following oral ingestion of ¹³C-urea. When H. pylori infection is present, ¹³C-urea is cleaved by bacterial urease to 2NH₃ and ¹³CO₂. Absorbed ¹³CO₂ is excreted via the lungs and measured in the expired air at baseline and 30 minutes following ingestion of the tracer. A positive result is indicated by an increase in expired ¹³C over baseline or delta over baseline (DOB) [3–5].

The magnitude of a DOB value is affected by multiple patient-related factors including gender, nationality, fasting, medications, and posture [6–9]. Test characteristics such as ¹³C-urea dosage, test meal, and test duration are also directly related to C13-UBT accuracy and may affect DOB magnitude [10–15].

DOB magnitude is also related to the severity of H. pylori infection. The density of H. pylori as well as histopathological chronicity and activity indices has been shown to positively correlate with DOB magnitude [16–25]. On the other hand, there appears to be no apparent correlation between DOB magnitude and dyspepsia or peptic ulceration [21, 25, 26].

Eradication of H. pylori remains a challenge, and there are continual efforts to identify factors which influence treatment success. The relationship between the histopathological severity of gastritis and the likelihood of treatment success is complex. Several studies have suggested that a higher degree of chronic active inflammation in the gastric mucosa is associated with H. pylori treatment success [27–30]. On the other hand, a high degree of mucosal atrophy decreases the likelihood of treatment success [30]. It is unclear whether the magnitude of C13-UBT result is related to treatment success. The aim of this study was to examine whether the C13-UBT result is related to the likelihood of subsequent successful eradication of H. pylori.

2. Materials and Methods

2.1. Patients

We retrospectively identified adult patients > 18 years who underwent a first-time ¹³C-urea breath test (C13-UBT) between 1 January 2010 and 31 December 2015 in Clalit Health Services (CHS). In order to exclude patients who may have previously received antibiotic treatment for H. pylori, we first excluded patients ≥ 45 years old who may have undergone an initial endoscopy-based H. pylori test in accordance with guidelines at the time of inclusion [31]. Subsequently, we excluded subjects who had undergone a C13-UBT in the 2 years prior to inclusion (1 January 2008-31 December 2009). Finally, we excluded patients who underwent a C13-UBT following a negative test. For the purpose of this study, we assumed that antibiotic treatment was administered following a positive C13-UBT and prior to a subsequent C13-UBT.

2.2. Sample Acquisition and Analysis

Breath samples were obtained from CHS facilities which incorporate 14 hospitals and 1300 primary care and referral clinics throughout eight districts. Breath tests were conducted by dedicated nurses. Patients were given 75 mg of ¹³C-labeled urea mixed with a test meal of 100 ml orange juice. All C13-UBT breath samples were transported and processed at a central laboratory at Rabin Medical Center, Petah Tikva, Israel. Samples were analyzed with a Gilson XL222 Automatic Breath Sampler (Gilson, Middleton, WI, USA) and an AP2003 Isotope Ratio Mass Spectrometer (IRMS) (Analytical Precision, Phoenix, AZ, USA). The ratio of expired ¹³C and ¹²C measured in parts per thousand was obtained at baseline and 30 minutes following ingestion of ¹³C-urea (T30-T0). The final result was expressed as the difference between the two scores, delta over baseline (DOB). A cutoff 3.5 DOB was used in accordance with the manufacturer’s specifications. An increase above 3.5 DOB was considered positive for the presence of H. pylori infection.

2.3. Data Extraction

Demographic data and C13-UBT results were extracted from the central computerized CHS database. CHS is the largest health maintenance organization in Israel and the second largest health maintenance organization in the world, with more than 3.8 million enrollees. Data were retrieved and stored following the approval of the Institutional Review Board at Rabin Medical Center and according to the principles of the Declaration of Helsinki and Good Clinical Practice.

2.4. Statistical Analysis

All analyses were performed using SPSS version 24.0 statistical analysis software (IBM Inc., Chicago, IL, USA). The distributions of continuous variables were assessed for normality using the Kolmogorov-Smirnov test (cutoff at ) and are described as means ± standard deviations (SD). Nominal variables were compared by using the chi-square test. Receiver operator curve (ROC) was plotted and analyzed with the Youden index. A multivariate forward logistic regression model was used in the statistical analysis to estimate odds ratios (OR) and 95% confidence interval. All tests were two-sided and considered significant at .

3. Results

A total of 94,590 subjects (36.1% male, age 28.5 ± 6.0 years) who underwent a first-time C13-UBT during the study period were included. C13-UBT was positive in 48,509 (51.3%) subjects. A confirmatory posttreatment C13-UBT was performed in 18,375 (37.8%), and eradication was successful in 12,018 (65.4%).

Among the 18,375 H. pylori-positive subjects who underwent a second C13-UBT, the mean initial C13-UBT recording was 20.6 ± 16.2 DOB among subjects with successful eradication and 19.5 ± 13.1 DOB in subjects with treatment failure (OR, 1.01; 95% CI 1.00-1.01, ) (Table 1). ROC analysis determined that a cutoff of 14.9 DOB could predict treatment success with 45.2% sensitivity and 58.5% specificity.

Among the patients in the upper quintile of C13-UBT measurement, eradication was achieved in 67.6%, compared to 62.6% in the lower quintile (OR, 1.22; 95% CI 1.11-1.35, ) (Figure 1). The results were similar when using a multivariate logistic regression model adjusted for age and sex (OR, 1.28; 95% CI 1.15-1.42; ) (Table 2).

Subjects in the top 1 percentile with C13-UBT ≥ 70 DOB achieved eradication in 75.0%, compared to 65.3% among subjects with C13-UBT < 70 DOB (OR, 1.59; 95% CI 1.05-2.41, ) (Figure 2). The results were similar when using a multivariate logistic regression model adjusted for age and sex (OR, 1.62; 95% CI 1.07-2.45, ) (Table 2).

4. Discussion

We found that among subjects undergoing C13-UBT, as the DOB magnitude increases, the likelihood of successful eradication of H. pylori increases as well.

The magnitude of the DOB value is directly related to H. pylori urease activity. Therefore, it is unsurprising that DOB magnitude has been correlated with the density of H. pylori as measured by PCR, as well as by the grade of chronic active inflammation, as evidenced by infiltration of lymphocytes and neutrophils in the gastric mucosa [16–25, 32]. DOB magnitude has also been correlated with the frequency and intensity of dyspepsia [33]. Gastric mucosal atrophy, on the other hand, is associated with reduced bacterial density [34, 35]. It follows that subjects with a greater degree of gastric mucosal atrophy have lower DOB magnitude [23, 32]. A low PGI/II ratio, indicating gastric atrophy, has also been correlated with lower DOB magnitude [32]. It should be noted, however, that others did not find an association between bacterial density and DOB magnitude, although these studies did not include an assessment of chronic active inflammation [36, 37].

A previous study has examined the relationship between DOB magnitude and treatment success. In contrast to our findings, Gisbert et al. found no correlation between DOB magnitude and the likelihood of successful eradication, among 600 subjects [38]. Previous studies have examined the association between inflammation score, as measured by the revised Sydney System, and the likelihood of successful treatment [39]. Three studies have found that higher degrees of chronic active inflammation are associated with treatment success [27–29]. An additional study found that a high degree of mucosal atrophy decreases the likelihood of treatment success [30]. These studies did not include a molecular assessment of bacterial load or quantitative C13-UBT. However, if we consider the evidence that DOB magnitude is directly proportional to inflammatory cell infiltrate and inversely proportional to atrophy, as discussed, then these studies may be consistent with our findings, which suggest that DOB magnitude is proportional to treatment success. Taken together, it seems that subjects with a more severe inflammatory infiltrate are more likely to have a high bacterial load, a higher DOB, and greater treatment success. Subjects with mucosal atrophy and a lower bacterial load are more likely to have lower DOB magnitude and more treatment failure. Clearly, there is abundant overlap between these two scenarios, and while it may be a valid observation in a population setting, there is little relevance with respect to an individual patient.

There are several possible mechanisms why a high DOB value or inflammation score is associated with treatment success. Increased chronic active inflammation might trigger a favorable host response that facilitates eradication of the organism with appropriate treatment. Labenz et al. found that patients with successful eradication had a higher gastric pH compared with patients with treatment failure. A higher pH may augment the effect of amoxicillin by lowering the minimal inhibitory concentration, increase drug stability in the gastric lumen, and increase luminal concentration by slowing gastric emptying [40–42]. Nevertheless, the relationship between DOB magnitude and inflammation score is not completely clear, and these mechanisms might only explain why inflammation, but not DOB, is related to treatment success.

A limitation of our study is the lack of histopathology data to correlate our findings. Another limitation is the likely presence of multiple confounders which cannot be accounted for. Firstly, there are multiple factors which determine DOB magnitude, besides bacterial density, which may account for the observed difference in treatment success. These include patient factors, bacterial factors, and test/laboratory factors [6–15]. Secondly, there are confounding factors which may account for differences in treatment success. These include drug compliance, antibiotic resistance, antibiotic regimen, drug-drug interactions, CYP2C19 polymorphisms, and smoking. Nevertheless, given the large sample size, it is unlikely that controlling for these factors would significantly alter the results. Another limitation is the relatively low eradication rate of 65.4%. Previous data suggest that over 90% of subjects received clarithromycin-based triple therapy [43], despite the fact that primary resistance of H. pylori to clarithromycin in our region is >20% [44, 45]. According to the current treatment guidelines, clarithromycin-based triple therapy is not recommended in regions where the primary clarithromycin resistance exceeds 15% [1, 46]. Nevertheless, clarithromycin-based triple therapy remains by far the most common treatment protocol utilized [43]. If subjects had received more efficacious treatment regimens with a higher eradication rate, it is possible that the DOB magnitude would no longer be significantly associated with treatment success.

For the purpose of this study, we assumed that antibiotic treatment was administered following a positive C13-UBT and prior to a subsequent C13-UBT. Some subjects, however, may not have received treatment or may have received more than one treatment course prior to repeating C13-UBT. We have no data on the various treatment protocols used. Although we excluded subjects above the age of 45 years, some subjects may have undergone endoscopy-based tests for H. pylori diagnosis and may have received treatment prior to the index test. Finally, our cohort is limited to 18-45-year-olds. We excluded subjects over the age of 45 since these patients were more likely to have undergone an upper gastrointestinal endoscopy as their initial test for dyspepsia. Otherwise, patients with a positive C13-UBT following a positive endoscopy-based test and subsequent treatment would have been inaccurately categorized as treatment naïve. Since we could not reliably identify patients who had previously undergone an endoscopy-based test for H. pylori, we chose to exclude patients > 45 years old. Our results may not be applicable to older subjects with more longstanding infection, higher rates of gastric atrophy, and perhaps better treatment compliance. The strength of our study lies in the large cohort, the rigorous exclusion criteria, and the quality of the database used.

In conclusion, we found that higher DOB magnitude is associated with a greater degree of successful eradication of H. pylori. Further studies which incorporate histopathological and clinical variables are needed to verify and elucidate the physiological basis for our findings.

Data Availability

The raw data used to support the findings of this study are available from the corresponding author upon request.

Conflicts of Interest

The authors have no conflicts of interest to declare.

References

P. Malfertheiner, F. Megraud, C. A. O'Morain et al., “Management of Helicobacter pylori infection—the Maastricht V/Florence Consensus Report,” Gut, vol. 66, no. 1, pp. 6–30, 2017.
View at: Publisher Site | Google Scholar
L. M. Best, Y. Takwoingi, S. Siddique et al., “Non-invasive diagnostic tests for Helicobacter pylori infection,” Cochrane Database of Systematic Reviews, vol. 3, article CD012080, 2018.
View at: Publisher Site | Google Scholar
E. Lotterer, J. Ramaker, F. E. Lüdtke, R. Tegeler, J. V. Geletneky, and F. E. Bauer, “The simplified 13C-urea breath test - one point analysis for detection of Helicobacter pylori infection,” Zeitschrift für Gastroenterologie, vol. 29, no. 11, pp. 590–594, 1991.
View at: Google Scholar
J. C. Atherton and R. C. Spiller, “The urea breath test for Helicobacter pylori,” Gut, vol. 35, no. 6, pp. 723–725, 1994.
View at: Publisher Site | Google Scholar
A. F. Goddard and R. P. H. Logan, “Review article: urea breath tests for detecting Helicobacter pylori,” Alimentary Pharmacology & Therapeutics, vol. 11, no. 4, pp. 641–649, 1997.
View at: Publisher Site | Google Scholar
L. Gatta, N. Vakil, C. Ricci et al., “Effect of proton pump inhibitors and antacid therapy on 13C urea breath tests and stool test for Helicobacter pylori infection,” The American Journal of Gastroenterology, vol. 99, no. 5, pp. 823–829, 2004.
View at: Publisher Site | Google Scholar
B. J. Johnston, N. Gruer, and P. Johnson, “Effect of subject position on the performance of the ¹³C-urea breath test for the detection of Helicobacter pylori,” Gut, vol. 43, 1998.
View at: Google Scholar
I. Eisdorfer, V. Shalev, S. Goren, G. Chodick, and K. Muhsen, “Sex differences in urea breath test results for the diagnosis of Helicobacter pylori infection: a large cross-sectional study,” Biology of Sex Differences, vol. 9, no. 1, p. 1, 2018.
View at: Publisher Site | Google Scholar
G. Bode, D. Rothenbacher, H. Brenner, and G. Adler, “Variation in the ¹³C-urea breath test value by nationality in Helicobacter pylori-infected children,” Scandinavian Journal of Gastroenterology, vol. 33, no. 5, pp. 468–472, 1998.
View at: Publisher Site | Google Scholar
C. Kato, T. Sugiyama, K. Sato et al., “Appropriate cut-off value of ¹³C-urea breath test after eradication of Helicobacter pylori infection in Japan,” Journal of Gastroenterology and Hepatology, vol. 18, no. 12, pp. 1379–1383, 2003.
View at: Publisher Site | Google Scholar
L. Gatta, N. Vakil, C. Ricci et al., “A rapid, low-dose, ¹³C-urea tablet for the detection of Helicobacter pylori infection before and after treatment,” Alimentary Pharmacology & Therapeutics, vol. 17, no. 6, pp. 793–798, 2003.
View at: Publisher Site | Google Scholar
J. E. Domínguez-Muñoz, A. Leodolter, T. Sauerbruch, and P. Malfertheiner, “A citric acid solution is an optimal test drink in the ¹³C-urea breath test for the diagnosis of Helicobacter pylori infection,” Gut, vol. 40, no. 4, pp. 459–462, 1997.
View at: Publisher Site | Google Scholar
H. M. Malaty, H. M. T. el-Zimaity, R. M. Genta, P. D. Klein, and D. Y. Graham, “Twenty-minute fasting version of the US ¹³C-urea breath test for the diagnosis of H. pylori infection,” Helicobacter, vol. 1, no. 3, pp. 165–167, 1996.
View at: Publisher Site | Google Scholar
W. M. Wang, S. C. Lee, H. J. Ding et al., “Quantification of Helicobacter pylori infection: simple and rapid ¹³C-urea breath test in Taiwan,” Journal of Gastroenterology, vol. 33, no. 3, pp. 330–335, 1998.
View at: Publisher Site | Google Scholar
S. Ohara, M. Kato, M. Asaka, and T. Toyota, “Studies of ¹³C-urea breath test for diagnosis of Helicobacter pylori infection in Japan,” Journal of Gastroenterology, vol. 33, no. 1, pp. 6–13, 1998.
View at: Publisher Site | Google Scholar
F. Perri, R. Clemente, M. Pastore et al., “The ¹³C-urea breath test as a predictor of intragastric bacterial load and severity of Helicobacter pylori gastritis,” Scandinavian Journal of Clinical and Laboratory Investigation, vol. 58, no. 1, pp. 19–28, 1998.
View at: Publisher Site | Google Scholar
R. M. Zagari, P. Pozzato, C. Martuzzi et al., “¹³C-urea breath test to assess Helicobacter pylori bacterial load,” Helicobacter, vol. 10, no. 6, pp. 615–619, 2005.
View at: Publisher Site | Google Scholar
M.-C. Chang, Y.-T. Chang, C.-T. Sun, M. S. Wu, H. P. Wang, and J. T. Lin, “Quantitative correlation of Helicobacter pylori stool antigen (HpSA) test with ¹³C-urea breath test (13C-UBT) by the updated Sydney grading system of gastritis,” Hepato-Gastroenterology, vol. 49, no. 44, pp. 576–579, 2002.
View at: Google Scholar
D. Kobayashi, Y. Eishi, T. Ohkusa et al., “Gastric mucosal density of Helicobacter pylori estimated by real-time PCR compared with results of urea breath test and histological grading,” Journal of Medical Microbiology, vol. 51, no. 4, pp. 305–311, 2002.
View at: Publisher Site | Google Scholar
B. S. Sheu, S. C. Lee, H. B. Yang, and X. Z. Lin, “Quantitative result of ¹³C urea breath test at 15 minutes may correlate with the bacterial density of H. pylori in the stomach,” Hepatogastroenterology, vol. 46, no. 27, pp. 2057–2062, 1999.
View at: Google Scholar
Y.-W. Chang, S.-K. Min, K.-J. Kim et al., “Delta ¹³C-urea breath test value is a useful indicator for Helicobacter pylori eradication in patients with functional dyspepsia,” Journal of Gastroenterology and Hepatology, vol. 18, no. 6, pp. 726–731, 2003.
View at: Publisher Site | Google Scholar
P. Vincent, L. Michaud, E. M. de Lasalle, B. Benon, D. Turck, and F. Gottrand, “¹³C-urea breath test and gastric mucosal colonization by Helicobacter pylori in children: quantitative relation and usefulness for diagnosis of infection,” Helicobacter, vol. 4, no. 4, pp. 233–237, 1999.
View at: Publisher Site | Google Scholar
K. Iijima, S. Ohara, H. Sekine et al., “Correlation between ¹³C-urea breath test and gastric histological findings in Helicobacter pylori positive patients,” Nihon Shokakibyo Gakkai Zasshi, vol. 95, no. 1, pp. 18–25, 1998.
View at: Google Scholar
V. Ellenrieder, B. Glasbrenner, C. Stoffels et al., “Qualitative and semi-quantitative value of a modified ¹³C-urea breath test for identification of Helicobacter pylori infection,” European Journal of Gastroenterology & Hepatology, vol. 9, no. 11, pp. 1085–1089, 1997.
View at: Publisher Site | Google Scholar
J. C. Debongnie, S. Pauwels, A. Raat, Y. de Meeus, J. Haot, and P. Mainguet, “Quantification of Helicobacter pylori infection in gastritis and ulcer disease using a simple and rapid carbon-14-urea breath test,” Journal of Nuclear Medicine, vol. 32, no. 6, pp. 1192–1198, 1991.
View at: Google Scholar
T. K. Sharma, V. M. Prasad, and A. F. Cutler, “Quantitative noninvasive testing for Helicobacter pylori does not predict gastroduodenal ulcer disease,” Gastrointestinal Endoscopy, vol. 44, no. 6, pp. 679–682, 1996.
View at: Publisher Site | Google Scholar
T. Kamada, K. Haruma, K. Komoto et al., “Effect of smoking and histological gastritis severity on the rate of H. pylori eradication with omeprazole, amoxicillin, and clarithromycin,” Helicobacter, vol. 4, no. 3, pp. 204–210, 1999.
View at: Publisher Site | Google Scholar
A. F. Cutler and T. T. Schubert, “Patient factors affecting Helicobacter pylori eradication with triple therapy,” The American Journal of Gastroenterology, vol. 88, no. 4, pp. 505–509, 1993.
View at: Google Scholar
J. Labenz, M. Stolte, A. L. Blum et al., “Intragastric acidity as a predictor of the success of Helicobacter pylori eradication: a study in peptic ulcer patients with omeprazole and amoxicillin,” Gut, vol. 37, no. 1, pp. 39–43, 1995.
View at: Publisher Site | Google Scholar
I. H. Kalkan, F. Sapmaz, S. Güliter, and P. Atasoy, “Severe gastritis decreases success rate of Helicobacter pylori eradication,” Wiener Klinische Wochenschrift, vol. 128, no. 9-10, pp. 329–334, 2016.
View at: Publisher Site | Google Scholar
N. J. Talley, N. B. Vakil, and P. Moayyedi, “American gastroenterological association technical review on the evaluation of dyspepsia,” Gastroenterology, vol. 129, no. 5, pp. 1756–1780, 2005.
View at: Publisher Site | Google Scholar
X. Chen, K. Haruma, T. Kamada et al., “Factors that affect results of the ¹³C urea breath test in Japanese patients,” Helicobacter, vol. 5, no. 2, pp. 98–103, 2000.
View at: Publisher Site | Google Scholar
F. Franceschi, A. Armuzzi, F. Cremonini et al., “¹³CO₂ excretion and expression of dyspeptic symptoms in patients evaluated for Helicobacter pylori infection by [¹³C] urea breath test,” Digestive Diseases and Sciences, vol. 47, no. 4, pp. 804–808, 2002.
View at: Publisher Site | Google Scholar
A. Kokkola, T. Kosunen, P. Puolakkainen et al., “Spontaneous disappearance of Helicobacter pylori antibodies in patients with advanced atrophic corpus gastritis,” APMIS, vol. 111, no. 6, pp. 619–624, 2003.
View at: Publisher Site | Google Scholar
A. Kokkola, H. Rautelin, P. Puolakkainen et al., “Diagnosis of Helicobacter pylori infection in patients with atrophic gastritis: comparison of histology, ¹³C-urea breath test, and serology,” Scandinavian Journal of Gastroenterology, vol. 35, no. 2, pp. 138–141, 2000.
View at: Publisher Site | Google Scholar
J. Auroux, D. Lamarque, J. Tankovic et al., “Comparaison de la quantification de l'infection gastrique à Helicobacter pylori par culture, histologie, et test respiratoire à l'urée marquée au ¹³C,” Gastroentérologie Clinique et Biologique, vol. 22, no. 4, pp. 407–412, 1998.
View at: Google Scholar
S. Tummala, S. G. Sheth, J. D. Goldsmith et al., “Quantifying gastric Helicobacter pylori infection: a comparison of quantitative culture, urease breath testing, and histology,” Digestive Diseases and Sciences, vol. 52, no. 2, pp. 396–401, 2007.
View at: Publisher Site | Google Scholar
J. P. Gisbert, D. Olivares, I. Jimenez, and J. M. Pajares, “Is there any correlation between ¹³C-urea breath test values and response to first-line and rescue Helicobacter pylori eradication therapies?” Digestive and Liver Disease, vol. 38, no. 4, pp. 254–259, 2006.
View at: Publisher Site | Google Scholar
M. F. Dixon, R. M. Genta, J. H. Yardley, and P. Correa, “Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994,” The American Journal of Surgical Pathology, vol. 20, no. 10, pp. 1161–1181, 1996.
View at: Publisher Site | Google Scholar
M. L. Grayson, G. M. Eliopoulos, M. J. Ferraro, and R. C. Moellering Jr, “Effect of varying pH on the susceptibility of Campylobacter pylori to antimicrobial agents,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 8, no. 10, pp. 888-889, 1989.
View at: Publisher Site | Google Scholar
P. Mainguet, M. Delmée, and J. C. Debongnie, “Omeprazole, Campylobacter pylori, and duodenal ulcer,” The Lancet, vol. 2, no. 8659, pp. 389-390, 1989.
View at: Google Scholar
H. P. Parkman, J. L. C. Urbain, L. C. Knight et al., “Effect of gastric acid suppressants on human gastric motility,” Gut, vol. 42, no. 2, pp. 243–250, 1998.
View at: Publisher Site | Google Scholar
D. Boltin, N. Kimchi, R. Dickman, R. Gingold-Belfer, Y. Niv, and S. Birkenfeld, “Attitudes and practice related to Helicobacter pylori infection among primary care physicians,” European Journal of Gastroenterology & Hepatology, vol. 28, no. 9, pp. 1035–1040, 2016.
View at: Publisher Site | Google Scholar
N. Pastukh, D. Binyamin, A. On, M. Paritsky, and A. Peretz, “GenoType® HelicoDR test in comparison with histology and culture for Helicobacter pylori detection and identification of resistance mutations to clarithromycin and fluoroquinolones,” Helicobacter, vol. 22, no. 6, 2017.
View at: Publisher Site | Google Scholar
A. Peretz, M. Paritsky, O. Nasser et al., “Resistance of Helicobacter pylori to tetracycline, amoxicillin, clarithromycin and metronidazole in Israeli children and adults,” The Journal of Antibiotics, vol. 67, no. 8, pp. 555–557, 2014.
View at: Publisher Site | Google Scholar
W. D. Chey, G. I. Leontiadis, C. W. Howden, and S. F. Moss, “ACG clinical guideline: treatment of Helicobacter pylori infection,” The American Journal of Gastroenterology, vol. 112, no. 2, pp. 212–239, 2017.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2018 Doron Boltin et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

2786

Downloads

1203

Citations