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Helicobacter pylori (Hp) related chronic gastritis is a common infection with varied prevalence rates throughout the world.[[1]] Ethnicity, country of birth and socioeconomic status are the most important risk factors. Although often asymptomatic, Hp has a number of well-known clinical associations including dyspepsia, peptic ulcer disease and gastric cancer; all leading to disability, hospitalisation and loss of life with resultant significant healthcare burden.[[2]] Most of these outcomes are preventable by timely diagnosis and successful eradication.[[3]] Although there are a number of different diagnostic tests available, any such test is limited by its performance within clinical context, its accessibility and cost. The New Zealand population is ethnically and geographically diverse and constantly evolving due to rising immigration.[[4]] Consequently, up-to-date Hp-related data is sparse. Healthcare in New Zealand is provided by district health boards (DHB) on a regional level, with most DHBs offering their own Hp diagnostic pathways.[[5,6]] Little is known about the diagnostic trends and expenses in the DHBs. With this in mind, we looked at New Zealand regional data covering a population of roughly 550,000.

Methods

We have retrospectively reviewed all Hp test results within the Canterbury District Health Board (CDHB) catchment area over six consecutive years between 2013–2018. The tests included Hp serology, rapid urease test known as Campylobacter-like organism test (CLO), Hp stool antigen test (SAT), urea breath test (UBT) and Hp culture and antibiotic sensitivity (Hp C&S). Histology-based results were excluded. The only demographic data collected was ethnicity as stated on the patient’s electronic record. The data was obtained with the help of the Canterbury Initiative Division of CDHB and covered all test requests from a location within CDHB boundaries. This included both the public and private sectors. Duplicate tests per single patient (defined as any additional test by the same modality linked to the same unique National Health Index identifier) were identified and only the historically first test per patient was included in test positivity rate calculations. Similarly, all equivocal test results were discounted in these test positivity rate calculations. This study received local ethical approval (CDHB Locality Authorisation) and was deemed out of scope for ethical approval by the Health and Disability Ethics Committee.

Results

A steady annual increase in overall numbers of tests carried out was recorded (Figure 1).

This was mirrored by increasing expenditure approaching $250,000 NZD per year in 2018 (Figure 2). The cost per test at the time, as advised by Canterbury Health Laboratories (in NZD and excluding goods and service tax (GST)), was: Hp serology $32.29; CLO $16.82; SAT $77.29; UBT $84.60; Hp C&S $59.25. These prices remained unchanged throughout this period. The CLO price is obviously exclusive of any gastroscopy related costs. As with other DHBs within New Zealand, in CDHB there is direct access to gastroscopy for symptomatic patients aged 55 years, or 45 years in at-risk ethnicities (i.e., without the need for prior specialist review). We found these two subgroups to be proportionately representative of the total CLO test cohorts at 53.5% and 12.1% respectively.

The following overall test volumes were recorded during the entire study period: Hp serology 17,291; CLO 10,070; SAT 8,331; UBT 322. Hp C&S was performed in only four cases during this time, rendering this test cohort inappropriate for further analysis. A total of 2,724 duplicate tests (50% of which was Hp serology) were identified and discounted from test positivity rate calculations. In addition, a total of 440 equivocal results (mostly Hp serology) were also excluded.

One hundred percent of SAT and roughly 75% of Hp serology tests were requested in primary care. The test utilisation by ethnicity is displayed in Table 1.

Relevant demographic data from official Canterbury censuses in 2013 and 2018 are provided for comparison in Table 2.[[4]]

Annual Hp test results are displayed in Figure 3. The test positivity rates appeared static overall during this period, however, the UBT cohort is too small to provide a reliable trend. Mean annual positive test rates over 2013–2018 period were: Hp serology 12.3%; CLO 7.2%; SAT 10.2%; UBT 17.5%. The compound mean annual test positivity across all test modalities was 10.4%, bearing in mind that an unknown number of patients could have been cross-tested with different test modalities that we couldn’t account for. A detailed breakdown by ethnicity is provided in Table 1.

Although we have no information regarding the actual indication to test, a vast majority was likely undertaken in symptomatic patients. We stress that this is not a cross-sectional population sample and that Hp infection is commonly asymptomatic.[[3]] As such, the data only show Hp positivity in the tested cohort, but do not show population prevalence.

View Supplementary material.

Discussion

This is the largest Hp test cohort published in New Zealand to date and the first study that directly addresses diagnostic costs. As this is only a regional study, we cannot assume similar trends and expenditure elsewhere in New Zealand. However, it is quite plausible that other DHBs would have comparable data, except perhaps for differing test positivity rates according to regional ethnicity profiles.

The progressive increase in testing and related expense isn’t surprising and mirrors current trends in healthcare in New Zealand. Nevertheless, the costs incurred are significant (Figure 2). Should the diagnostic practices be similar in the rest of New Zealand with a population of 5 million, the projected annual nationwide cost (as of 2018) would sit at around 2.5 million NZD. If we were to include histology from gastric biopsy (local price is $94.14 NZD), the annual cost might see further significant increase. Once again, this excludes the major cost of gastroscopy. Also notable is the discrepancy between population growth and number of tests performed. The Canterbury population has increased by 11.1% during this period. In contrast, overall Hp test numbers rose by 37% and Hp test expenditure by 42.6%. This small difference between test numbers and cost is explained by increasing use of SATs, which are more expensive.

In terms of general trends, both SAT and CLO utilisation is increasing. The rise in SAT likely relates to improved diagnostic pathway awareness, while the increasing CLO use could be in part due to a relative ease of access to gastroscopy. UBT, considered a gold standard, seems a more marginalised test now, likely owing to its relative complexity and difficult access. The essentially absent data on Hp antibiotic sensitivity/resistance is certainly troubling with potential negative implications for eradication treatment outcomes. There also continues to be a high usage of Hp serology despite the existing guidelines advising against this.[[5–7]] These guidelines suggest that such testing in a country with a low overall Hp prevalence (such as New Zealand) is best left for population-based research rather than for a diagnosis with intent to treat given its poor sensitivity and specificity in such setting.[[1,3]] In addition, the repetition of Hp serology testing in the same patient serves little purpose beyond increasing the overall costs and this was certainly a common occurrence in our cohort.

All of the non-serology-based tests, including SAT, CLO and UBT (and histology) rely on the presence of thriving Hp bacteria. The frequent use of proton pump inhibitors (PPIs) and antibiotics contributes to temporary suppression of Hp growth and thus significantly increases the rate of false negative test results.[[8–14]] In our experience, this well established phenomenon is often not accounted for in clinical practice, although we acknowledge this study offers no data to support this observation. Nevertheless, better awareness of these principles, especially in the realm of primary care, should lead to improved diagnosis (especially of the at-risk cohorts) and possibly to reduced costs related to better test utilisation.

In contrast to this potentially inappropriate overuse of tests, we found disproportionately low numbers of tests in at-risk ethnic minorities. For instance, Māori were significantly under-represented in all test modalities (Tables 1 and 2). This may well be yet another indicator of healthcare inequity in New Zealand. For illustration, the following compares the proportion of Hp tests in certain ethnicities in relation to the Canterbury Census; only 48.2% Māori and 67.8% Pasifika were tested for Hp compared with 82.7% of NZ Europeans. This is contrasted by significantly higher test positivity rates in these groups (Māori 21.2%, Pasifika 37.8%) compared with 8.4% in NZ Europeans. However, a particular test modality preference as opposed to test access could be a co-factor in certain cultures. A case in point might be the SAT cohort. We found this test to be significantly over-represented in our Asian subgroup (Table 1).

Data on Hp prevalence in New Zealand is patchy and varied.[[15–21]] Nonetheless, the overall Hp prevalence in this country is considered low by global standards (below 30%).[[1]] From the little information available, the South Island population seems to have a lower Hp prevalence than the North Island, likely owing to its differing ethnic make-up with a higher proportion of NZ Europeans.[[4]] A 1996 study from Canterbury found a Hp seroprevalence of 24% in this randomly selected population sample.[[21]] Approximately 20 years later, Hp seroprevalence in our tested cohort was 12.3%. As our cohort mostly consists of symptomatic patients, the true population seroprevalence in Canterbury may possibly be even lower. This trend is supported by other studies noting an overall decrease in seroprevalence in younger New Zealand birth cohorts.[[19,22]]

We found a surprisingly low test positivity in our CLO test cohort (7.2%). The explanation could lie in a combination of: poor test sensitivity in the presence of concurrent PPI use; relatively high numbers of NZ Europeans who underwent gastroscopy (>80%); opportunistic CLO testing at gastroscopy in the absence of relevant symptoms or findings; and, perhaps, a liberal access to gastroscopy with current referral guidelines anecdotally leading to a high number of gastroscopies with normal findings. Conversely, our UBT cohort had a relatively high positive test rate. However, this subgroup is more likely to represent either treatment failures or highly selected cases with resultant higher pre-test probability.

Our study drawbacks include lack of data on treatment and its outcomes as the local ethics approval specifically denied us access to this primary care-based information. In addition, no data exists on timing-dependent tests (UBT, SAT and CLO) in relation to PPI and/or antibiotic treatment. In other words, the rate of false negative test results is unknown, yet possibly significant. We haven’t examined histology from gastric biopsies that could provide additional data, however, even this test can be falsely negative in the presence of PPIs and/or antibiotics. Lastly, and perhaps most importantly, this study does not report a true population prevalence given the nature of our cohort.

In conclusion, Hp testing and related expenditure is increasing and is disproportionate to the population growth. At-risk ethnicities are underrepresented in the tested cohorts despite the significantly higher test positivity rates in these groups. A primary care-oriented focus on improved adherence to diagnostic guidelines along with emphasis on testing at-risk minorities could address both issues. This could bring both a cost reduction in Hp testing and possibly lead to improved health outcomes of those most at risk of Hp infection.

Summary

Abstract

Aim

To ascertain Helicobacter pylori (Hp) diagnosis trends and cost in a New Zealand cohort.

Method

All Hp tests within Canterbury between 2013–2018 were retrospectively reviewed, exclusive of histology. Overall numbers for each test modality, expenditure and test positivity rates were calculated and matched to ethnicity.

Results

Over the six-year period, Hp testing increased 37% and associated cost by 42.6%, compared with population growth of 11.1%. Primary care requested 82% of the non-invasive tests. Despite guidelines recommending against Hp serology, this was the most frequent test and duplicate testing in the same patient was common. Mean annual test positivity rates were: Hp serology 12.3%; Campylobacter-like organism 7.2%; Hp stool antigen test 10.2%; urea breath test 17.5%. The mean across all test modalities was 10.4%. Test proportion per ethnicity was lower in Māori (48.2%) and Pasifika (67.8%), compared with Europeans (82.7%). This was in contrast with significantly higher test positivity rates (Māori 21.2%, Pasifika 37.8%) compared with Europeans 8.4%.

Conclusion

Hp testing and related costs increase is disproportionate to population growth. At risk ethnicities are under-represented in the tested cohort despite higher test positivity rates. Primary care-focussed intervention could lead to reduced cost and improved equity in Hp diagnosis.

Author Information

Jan Kubovy: Consultant Gastroenterologist, Department of Gastroenterology, Christchurch Hospital, Christchurch, New Zealand. Murray L Barclay: Consultant Gastroenterologist and Clinical Pharmacologist, Departments of Gastroenterology and Clinical Pharmacology, Christchurch Hospital, and Clinical Professor, University of Otago, Christchurch, New Zealand.

Acknowledgements

Nikki Elliot, Canterbury Initiative Clinical Analyst.

Correspondence

Jan Kubovy: Department of Gastroenterology, Level 2, Riverside, Christchurch Hospital, Riccarton Avenue, Christchurch, 8011, New Zealand.

Correspondence Email

jan.kubovy@cdhb.health.nz

Competing Interests

Nil.

1) Hooi JK, Lai WY, Ng WK, Suen MM, Underwood FE, Tanyingoh D, Malfertheiner P, Graham DY, Wong VW, Wu JC, Chan FK. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017 Aug 1;153(2):420-9.

2) Rothenbacher D, Brenner H. Burden of Helicobacter pylori and H. pylori-related diseases in developed countries: recent developments and future implications. Microbes Infect. 2003 Jul 1;5(8):693-703.

3) Malfertheiner P, Megraud F, O'morain CA, Gisbert JP, Kuipers EJ, Axon AT, Bazzoli F, Gasbarrini A, Atherton J, Graham DY, Hunt R. Management of Helicobacter pylori infection—the Maastricht V/Florence consensus report. Gut. 2017 Jan 1;66(1):6-30.

4) 2018 Census [Internet]. New Zealand: Stats NZ [cited 2022]. Available from: https://www.stats.govt.nz/topics/census#2018-census.

5) Canterbury Community Health Pathways [Internet]. [cited 2022]. Available at: https://canterbury.communityhealthpathways.org/24341.htm.

6) The changing face of Helicobacter pylori testing [Internet]. New Zealand: BPAC NZ. [cited 2022]. Available at: https://bpac.org.nz/BT/2014/May/h-pylori.aspx.

7) World Gastroenterology Organisation Global Guidelines Helicobacter Pylori [Internet]. World Gastroenterology Organisation. [cited 2022]. Available at: https://www.worldgastroenterology.org/guidelines/helicobacter-pylori/helicobacter-pylori-english.

8) Manes G, Balzano A, Iaquinto G, Ricci C, Piccirillo MM, Giardullo N, Todisco A, Lioniello M, Vaira D. Accuracy of the stool antigen test in the diagnosis of Helicobacter pylori infection before treatment and in patients on omeprazole therapy. Dig Liver Dis. 2001 Jan 17;15(1):73-9.

9) Uotani T, Graham DY. Diagnosis of Helicobacter pylori using the rapid urease test. Ann Transl Med. 2015 Jan;3(1):215.

10) Shirin D, Matalon S, Avidan B, Broide E, Shirin H. Real-world Helicobacter pylori diagnosis in patients referred for esophagoduodenoscopy: The gap between guidelines and clinical practice. United European Gastroenterol J. 2016 Dec;4(6):762-9.

11) El-Serag HB, Kao JY, Kanwal F, Gilger M, LoVecchio F, Moss SF, Crowe S, Elfant A, Haas T, Hapke RJ, Graham DY. Houston consensus conference on testing for Helicobacter pylori infection in the United States. Clin Gastroenterol Hepatol. 2018 Jul 1;16(7):992-1002.

12) Taj Y, Essa F, Kazmi SU, Abdullah E. Sensitivity and specificity of various diagnostic tests in the detection of Helicobacter pylori. J Coll Physicians Surg P: JCPSP. 2003 Feb 1;13(2):90-3.

13) Olafsson S, Patel B, Jackson C, Cai J. Helicobacter Pylori Breath Testing in an Open Access System has a High Rate of Potentially False Negative Results due to Protocol Violations. Helicobacter. 2012 Oct;17(5):391-5.

14) Mittal S, Trakroo S, Kate V, Jagdish S. Evaluation of the effect of presence of blood in the stomach on endoscopic diagnostic tests for Helicobacter pylori infection. Indian Journal Med Microbiol. 2011 Oct 1;29(4):379-82.

15) Hsiang J, Selvaratnam S, Taylor S, Yeoh J, Tan YM, Huang J, Patrick A. Increasing primary antibiotic resistance and ethnic differences in eradication rates of Helicobacter pylori infection in New Zealand—a new look at an old enemy. NZ Med J. 2013 Oct 18;126(1384):64-76.

16) Fraser AG, Scragg R, Metcalf P, McCullough S, Yeates NJ. Prevalence of Helicobacter pylori infection in different ethnic groups in New Zealand children and adults. Aust N Z J Med. 1996 Oct;26(5):646-51.

17) Fraser AG, Peng SL, Jass JR. Intestinal metaplasia subtypes and Helicobacter pylori infection: a comparison of ethnic groups in New Zealand. J Gastroenterol Hepatol. 1998 Jun;13(6):560-5.

18) Fraser AG, Scragg R, Schaaf D, Metcalf P, Grant CC. Helicobacter pylori infection and iron deficiency in teenage females in New Zealand. N Z Med J. 2010;123(1313):38-45.

19) Fawcett JP, Shaw JP, Cockburn M, Brooke M, Barbezat GO. Seroprevalence of Helicobacter pylori in a birth cohort of 21-year-old New Zealanders. Eur J Gastroenterol Hepatol. 1996 Apr 1;8(4):365-9.

20) Fawcett JP, Shaw JP, Brooke M, Walker A, Barbezat GO. Seroprevalence of Helicobacter pylori in a longitudinal study of New Zealanders at ages 11 and 21. Aust N Z J Med. 1998 Oct;28(5):585-9.

21) Collett JA, Burt MJ, Frampton CM, Yeo KH, Chapman TM, Buttimore RC, Cook HB, Chapman BA. Seroprevalence of Helicobacter pylori in the adult population of Christchurch: risk factors and relationship to dyspeptic symptoms and iron studies. N Z Med J. 1999 Aug 1;112(1093):292-5.

22) McDonald AM, Sarfati D, Baker MG, Blakely T. Trends in Helicobacter pylori Infection Among Māori, Pacific, and European Birth Cohorts in New Zealand. Helicobacter. 2015 Apr;20(2):139-45.

For the PDF of this article,
contact nzmj@nzma.org.nz

View Article PDF

Helicobacter pylori (Hp) related chronic gastritis is a common infection with varied prevalence rates throughout the world.[[1]] Ethnicity, country of birth and socioeconomic status are the most important risk factors. Although often asymptomatic, Hp has a number of well-known clinical associations including dyspepsia, peptic ulcer disease and gastric cancer; all leading to disability, hospitalisation and loss of life with resultant significant healthcare burden.[[2]] Most of these outcomes are preventable by timely diagnosis and successful eradication.[[3]] Although there are a number of different diagnostic tests available, any such test is limited by its performance within clinical context, its accessibility and cost. The New Zealand population is ethnically and geographically diverse and constantly evolving due to rising immigration.[[4]] Consequently, up-to-date Hp-related data is sparse. Healthcare in New Zealand is provided by district health boards (DHB) on a regional level, with most DHBs offering their own Hp diagnostic pathways.[[5,6]] Little is known about the diagnostic trends and expenses in the DHBs. With this in mind, we looked at New Zealand regional data covering a population of roughly 550,000.

Methods

We have retrospectively reviewed all Hp test results within the Canterbury District Health Board (CDHB) catchment area over six consecutive years between 2013–2018. The tests included Hp serology, rapid urease test known as Campylobacter-like organism test (CLO), Hp stool antigen test (SAT), urea breath test (UBT) and Hp culture and antibiotic sensitivity (Hp C&S). Histology-based results were excluded. The only demographic data collected was ethnicity as stated on the patient’s electronic record. The data was obtained with the help of the Canterbury Initiative Division of CDHB and covered all test requests from a location within CDHB boundaries. This included both the public and private sectors. Duplicate tests per single patient (defined as any additional test by the same modality linked to the same unique National Health Index identifier) were identified and only the historically first test per patient was included in test positivity rate calculations. Similarly, all equivocal test results were discounted in these test positivity rate calculations. This study received local ethical approval (CDHB Locality Authorisation) and was deemed out of scope for ethical approval by the Health and Disability Ethics Committee.

Results

A steady annual increase in overall numbers of tests carried out was recorded (Figure 1).

This was mirrored by increasing expenditure approaching $250,000 NZD per year in 2018 (Figure 2). The cost per test at the time, as advised by Canterbury Health Laboratories (in NZD and excluding goods and service tax (GST)), was: Hp serology $32.29; CLO $16.82; SAT $77.29; UBT $84.60; Hp C&S $59.25. These prices remained unchanged throughout this period. The CLO price is obviously exclusive of any gastroscopy related costs. As with other DHBs within New Zealand, in CDHB there is direct access to gastroscopy for symptomatic patients aged 55 years, or 45 years in at-risk ethnicities (i.e., without the need for prior specialist review). We found these two subgroups to be proportionately representative of the total CLO test cohorts at 53.5% and 12.1% respectively.

The following overall test volumes were recorded during the entire study period: Hp serology 17,291; CLO 10,070; SAT 8,331; UBT 322. Hp C&S was performed in only four cases during this time, rendering this test cohort inappropriate for further analysis. A total of 2,724 duplicate tests (50% of which was Hp serology) were identified and discounted from test positivity rate calculations. In addition, a total of 440 equivocal results (mostly Hp serology) were also excluded.

One hundred percent of SAT and roughly 75% of Hp serology tests were requested in primary care. The test utilisation by ethnicity is displayed in Table 1.

Relevant demographic data from official Canterbury censuses in 2013 and 2018 are provided for comparison in Table 2.[[4]]

Annual Hp test results are displayed in Figure 3. The test positivity rates appeared static overall during this period, however, the UBT cohort is too small to provide a reliable trend. Mean annual positive test rates over 2013–2018 period were: Hp serology 12.3%; CLO 7.2%; SAT 10.2%; UBT 17.5%. The compound mean annual test positivity across all test modalities was 10.4%, bearing in mind that an unknown number of patients could have been cross-tested with different test modalities that we couldn’t account for. A detailed breakdown by ethnicity is provided in Table 1.

Although we have no information regarding the actual indication to test, a vast majority was likely undertaken in symptomatic patients. We stress that this is not a cross-sectional population sample and that Hp infection is commonly asymptomatic.[[3]] As such, the data only show Hp positivity in the tested cohort, but do not show population prevalence.

View Supplementary material.

Discussion

This is the largest Hp test cohort published in New Zealand to date and the first study that directly addresses diagnostic costs. As this is only a regional study, we cannot assume similar trends and expenditure elsewhere in New Zealand. However, it is quite plausible that other DHBs would have comparable data, except perhaps for differing test positivity rates according to regional ethnicity profiles.

The progressive increase in testing and related expense isn’t surprising and mirrors current trends in healthcare in New Zealand. Nevertheless, the costs incurred are significant (Figure 2). Should the diagnostic practices be similar in the rest of New Zealand with a population of 5 million, the projected annual nationwide cost (as of 2018) would sit at around 2.5 million NZD. If we were to include histology from gastric biopsy (local price is $94.14 NZD), the annual cost might see further significant increase. Once again, this excludes the major cost of gastroscopy. Also notable is the discrepancy between population growth and number of tests performed. The Canterbury population has increased by 11.1% during this period. In contrast, overall Hp test numbers rose by 37% and Hp test expenditure by 42.6%. This small difference between test numbers and cost is explained by increasing use of SATs, which are more expensive.

In terms of general trends, both SAT and CLO utilisation is increasing. The rise in SAT likely relates to improved diagnostic pathway awareness, while the increasing CLO use could be in part due to a relative ease of access to gastroscopy. UBT, considered a gold standard, seems a more marginalised test now, likely owing to its relative complexity and difficult access. The essentially absent data on Hp antibiotic sensitivity/resistance is certainly troubling with potential negative implications for eradication treatment outcomes. There also continues to be a high usage of Hp serology despite the existing guidelines advising against this.[[5–7]] These guidelines suggest that such testing in a country with a low overall Hp prevalence (such as New Zealand) is best left for population-based research rather than for a diagnosis with intent to treat given its poor sensitivity and specificity in such setting.[[1,3]] In addition, the repetition of Hp serology testing in the same patient serves little purpose beyond increasing the overall costs and this was certainly a common occurrence in our cohort.

All of the non-serology-based tests, including SAT, CLO and UBT (and histology) rely on the presence of thriving Hp bacteria. The frequent use of proton pump inhibitors (PPIs) and antibiotics contributes to temporary suppression of Hp growth and thus significantly increases the rate of false negative test results.[[8–14]] In our experience, this well established phenomenon is often not accounted for in clinical practice, although we acknowledge this study offers no data to support this observation. Nevertheless, better awareness of these principles, especially in the realm of primary care, should lead to improved diagnosis (especially of the at-risk cohorts) and possibly to reduced costs related to better test utilisation.

In contrast to this potentially inappropriate overuse of tests, we found disproportionately low numbers of tests in at-risk ethnic minorities. For instance, Māori were significantly under-represented in all test modalities (Tables 1 and 2). This may well be yet another indicator of healthcare inequity in New Zealand. For illustration, the following compares the proportion of Hp tests in certain ethnicities in relation to the Canterbury Census; only 48.2% Māori and 67.8% Pasifika were tested for Hp compared with 82.7% of NZ Europeans. This is contrasted by significantly higher test positivity rates in these groups (Māori 21.2%, Pasifika 37.8%) compared with 8.4% in NZ Europeans. However, a particular test modality preference as opposed to test access could be a co-factor in certain cultures. A case in point might be the SAT cohort. We found this test to be significantly over-represented in our Asian subgroup (Table 1).

Data on Hp prevalence in New Zealand is patchy and varied.[[15–21]] Nonetheless, the overall Hp prevalence in this country is considered low by global standards (below 30%).[[1]] From the little information available, the South Island population seems to have a lower Hp prevalence than the North Island, likely owing to its differing ethnic make-up with a higher proportion of NZ Europeans.[[4]] A 1996 study from Canterbury found a Hp seroprevalence of 24% in this randomly selected population sample.[[21]] Approximately 20 years later, Hp seroprevalence in our tested cohort was 12.3%. As our cohort mostly consists of symptomatic patients, the true population seroprevalence in Canterbury may possibly be even lower. This trend is supported by other studies noting an overall decrease in seroprevalence in younger New Zealand birth cohorts.[[19,22]]

We found a surprisingly low test positivity in our CLO test cohort (7.2%). The explanation could lie in a combination of: poor test sensitivity in the presence of concurrent PPI use; relatively high numbers of NZ Europeans who underwent gastroscopy (>80%); opportunistic CLO testing at gastroscopy in the absence of relevant symptoms or findings; and, perhaps, a liberal access to gastroscopy with current referral guidelines anecdotally leading to a high number of gastroscopies with normal findings. Conversely, our UBT cohort had a relatively high positive test rate. However, this subgroup is more likely to represent either treatment failures or highly selected cases with resultant higher pre-test probability.

Our study drawbacks include lack of data on treatment and its outcomes as the local ethics approval specifically denied us access to this primary care-based information. In addition, no data exists on timing-dependent tests (UBT, SAT and CLO) in relation to PPI and/or antibiotic treatment. In other words, the rate of false negative test results is unknown, yet possibly significant. We haven’t examined histology from gastric biopsies that could provide additional data, however, even this test can be falsely negative in the presence of PPIs and/or antibiotics. Lastly, and perhaps most importantly, this study does not report a true population prevalence given the nature of our cohort.

In conclusion, Hp testing and related expenditure is increasing and is disproportionate to the population growth. At-risk ethnicities are underrepresented in the tested cohorts despite the significantly higher test positivity rates in these groups. A primary care-oriented focus on improved adherence to diagnostic guidelines along with emphasis on testing at-risk minorities could address both issues. This could bring both a cost reduction in Hp testing and possibly lead to improved health outcomes of those most at risk of Hp infection.

Summary

Abstract

Aim

To ascertain Helicobacter pylori (Hp) diagnosis trends and cost in a New Zealand cohort.

Method

All Hp tests within Canterbury between 2013–2018 were retrospectively reviewed, exclusive of histology. Overall numbers for each test modality, expenditure and test positivity rates were calculated and matched to ethnicity.

Results

Over the six-year period, Hp testing increased 37% and associated cost by 42.6%, compared with population growth of 11.1%. Primary care requested 82% of the non-invasive tests. Despite guidelines recommending against Hp serology, this was the most frequent test and duplicate testing in the same patient was common. Mean annual test positivity rates were: Hp serology 12.3%; Campylobacter-like organism 7.2%; Hp stool antigen test 10.2%; urea breath test 17.5%. The mean across all test modalities was 10.4%. Test proportion per ethnicity was lower in Māori (48.2%) and Pasifika (67.8%), compared with Europeans (82.7%). This was in contrast with significantly higher test positivity rates (Māori 21.2%, Pasifika 37.8%) compared with Europeans 8.4%.

Conclusion

Hp testing and related costs increase is disproportionate to population growth. At risk ethnicities are under-represented in the tested cohort despite higher test positivity rates. Primary care-focussed intervention could lead to reduced cost and improved equity in Hp diagnosis.

Author Information

Jan Kubovy: Consultant Gastroenterologist, Department of Gastroenterology, Christchurch Hospital, Christchurch, New Zealand. Murray L Barclay: Consultant Gastroenterologist and Clinical Pharmacologist, Departments of Gastroenterology and Clinical Pharmacology, Christchurch Hospital, and Clinical Professor, University of Otago, Christchurch, New Zealand.

Acknowledgements

Nikki Elliot, Canterbury Initiative Clinical Analyst.

Correspondence

Jan Kubovy: Department of Gastroenterology, Level 2, Riverside, Christchurch Hospital, Riccarton Avenue, Christchurch, 8011, New Zealand.

Correspondence Email

jan.kubovy@cdhb.health.nz

Competing Interests

Nil.

1) Hooi JK, Lai WY, Ng WK, Suen MM, Underwood FE, Tanyingoh D, Malfertheiner P, Graham DY, Wong VW, Wu JC, Chan FK. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017 Aug 1;153(2):420-9.

2) Rothenbacher D, Brenner H. Burden of Helicobacter pylori and H. pylori-related diseases in developed countries: recent developments and future implications. Microbes Infect. 2003 Jul 1;5(8):693-703.

3) Malfertheiner P, Megraud F, O'morain CA, Gisbert JP, Kuipers EJ, Axon AT, Bazzoli F, Gasbarrini A, Atherton J, Graham DY, Hunt R. Management of Helicobacter pylori infection—the Maastricht V/Florence consensus report. Gut. 2017 Jan 1;66(1):6-30.

4) 2018 Census [Internet]. New Zealand: Stats NZ [cited 2022]. Available from: https://www.stats.govt.nz/topics/census#2018-census.

5) Canterbury Community Health Pathways [Internet]. [cited 2022]. Available at: https://canterbury.communityhealthpathways.org/24341.htm.

6) The changing face of Helicobacter pylori testing [Internet]. New Zealand: BPAC NZ. [cited 2022]. Available at: https://bpac.org.nz/BT/2014/May/h-pylori.aspx.

7) World Gastroenterology Organisation Global Guidelines Helicobacter Pylori [Internet]. World Gastroenterology Organisation. [cited 2022]. Available at: https://www.worldgastroenterology.org/guidelines/helicobacter-pylori/helicobacter-pylori-english.

8) Manes G, Balzano A, Iaquinto G, Ricci C, Piccirillo MM, Giardullo N, Todisco A, Lioniello M, Vaira D. Accuracy of the stool antigen test in the diagnosis of Helicobacter pylori infection before treatment and in patients on omeprazole therapy. Dig Liver Dis. 2001 Jan 17;15(1):73-9.

9) Uotani T, Graham DY. Diagnosis of Helicobacter pylori using the rapid urease test. Ann Transl Med. 2015 Jan;3(1):215.

10) Shirin D, Matalon S, Avidan B, Broide E, Shirin H. Real-world Helicobacter pylori diagnosis in patients referred for esophagoduodenoscopy: The gap between guidelines and clinical practice. United European Gastroenterol J. 2016 Dec;4(6):762-9.

11) El-Serag HB, Kao JY, Kanwal F, Gilger M, LoVecchio F, Moss SF, Crowe S, Elfant A, Haas T, Hapke RJ, Graham DY. Houston consensus conference on testing for Helicobacter pylori infection in the United States. Clin Gastroenterol Hepatol. 2018 Jul 1;16(7):992-1002.

12) Taj Y, Essa F, Kazmi SU, Abdullah E. Sensitivity and specificity of various diagnostic tests in the detection of Helicobacter pylori. J Coll Physicians Surg P: JCPSP. 2003 Feb 1;13(2):90-3.

13) Olafsson S, Patel B, Jackson C, Cai J. Helicobacter Pylori Breath Testing in an Open Access System has a High Rate of Potentially False Negative Results due to Protocol Violations. Helicobacter. 2012 Oct;17(5):391-5.

14) Mittal S, Trakroo S, Kate V, Jagdish S. Evaluation of the effect of presence of blood in the stomach on endoscopic diagnostic tests for Helicobacter pylori infection. Indian Journal Med Microbiol. 2011 Oct 1;29(4):379-82.

15) Hsiang J, Selvaratnam S, Taylor S, Yeoh J, Tan YM, Huang J, Patrick A. Increasing primary antibiotic resistance and ethnic differences in eradication rates of Helicobacter pylori infection in New Zealand—a new look at an old enemy. NZ Med J. 2013 Oct 18;126(1384):64-76.

16) Fraser AG, Scragg R, Metcalf P, McCullough S, Yeates NJ. Prevalence of Helicobacter pylori infection in different ethnic groups in New Zealand children and adults. Aust N Z J Med. 1996 Oct;26(5):646-51.

17) Fraser AG, Peng SL, Jass JR. Intestinal metaplasia subtypes and Helicobacter pylori infection: a comparison of ethnic groups in New Zealand. J Gastroenterol Hepatol. 1998 Jun;13(6):560-5.

18) Fraser AG, Scragg R, Schaaf D, Metcalf P, Grant CC. Helicobacter pylori infection and iron deficiency in teenage females in New Zealand. N Z Med J. 2010;123(1313):38-45.

19) Fawcett JP, Shaw JP, Cockburn M, Brooke M, Barbezat GO. Seroprevalence of Helicobacter pylori in a birth cohort of 21-year-old New Zealanders. Eur J Gastroenterol Hepatol. 1996 Apr 1;8(4):365-9.

20) Fawcett JP, Shaw JP, Brooke M, Walker A, Barbezat GO. Seroprevalence of Helicobacter pylori in a longitudinal study of New Zealanders at ages 11 and 21. Aust N Z J Med. 1998 Oct;28(5):585-9.

21) Collett JA, Burt MJ, Frampton CM, Yeo KH, Chapman TM, Buttimore RC, Cook HB, Chapman BA. Seroprevalence of Helicobacter pylori in the adult population of Christchurch: risk factors and relationship to dyspeptic symptoms and iron studies. N Z Med J. 1999 Aug 1;112(1093):292-5.

22) McDonald AM, Sarfati D, Baker MG, Blakely T. Trends in Helicobacter pylori Infection Among Māori, Pacific, and European Birth Cohorts in New Zealand. Helicobacter. 2015 Apr;20(2):139-45.

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Helicobacter pylori (Hp) related chronic gastritis is a common infection with varied prevalence rates throughout the world.[[1]] Ethnicity, country of birth and socioeconomic status are the most important risk factors. Although often asymptomatic, Hp has a number of well-known clinical associations including dyspepsia, peptic ulcer disease and gastric cancer; all leading to disability, hospitalisation and loss of life with resultant significant healthcare burden.[[2]] Most of these outcomes are preventable by timely diagnosis and successful eradication.[[3]] Although there are a number of different diagnostic tests available, any such test is limited by its performance within clinical context, its accessibility and cost. The New Zealand population is ethnically and geographically diverse and constantly evolving due to rising immigration.[[4]] Consequently, up-to-date Hp-related data is sparse. Healthcare in New Zealand is provided by district health boards (DHB) on a regional level, with most DHBs offering their own Hp diagnostic pathways.[[5,6]] Little is known about the diagnostic trends and expenses in the DHBs. With this in mind, we looked at New Zealand regional data covering a population of roughly 550,000.

Methods

We have retrospectively reviewed all Hp test results within the Canterbury District Health Board (CDHB) catchment area over six consecutive years between 2013–2018. The tests included Hp serology, rapid urease test known as Campylobacter-like organism test (CLO), Hp stool antigen test (SAT), urea breath test (UBT) and Hp culture and antibiotic sensitivity (Hp C&S). Histology-based results were excluded. The only demographic data collected was ethnicity as stated on the patient’s electronic record. The data was obtained with the help of the Canterbury Initiative Division of CDHB and covered all test requests from a location within CDHB boundaries. This included both the public and private sectors. Duplicate tests per single patient (defined as any additional test by the same modality linked to the same unique National Health Index identifier) were identified and only the historically first test per patient was included in test positivity rate calculations. Similarly, all equivocal test results were discounted in these test positivity rate calculations. This study received local ethical approval (CDHB Locality Authorisation) and was deemed out of scope for ethical approval by the Health and Disability Ethics Committee.

Results

A steady annual increase in overall numbers of tests carried out was recorded (Figure 1).

This was mirrored by increasing expenditure approaching $250,000 NZD per year in 2018 (Figure 2). The cost per test at the time, as advised by Canterbury Health Laboratories (in NZD and excluding goods and service tax (GST)), was: Hp serology $32.29; CLO $16.82; SAT $77.29; UBT $84.60; Hp C&S $59.25. These prices remained unchanged throughout this period. The CLO price is obviously exclusive of any gastroscopy related costs. As with other DHBs within New Zealand, in CDHB there is direct access to gastroscopy for symptomatic patients aged 55 years, or 45 years in at-risk ethnicities (i.e., without the need for prior specialist review). We found these two subgroups to be proportionately representative of the total CLO test cohorts at 53.5% and 12.1% respectively.

The following overall test volumes were recorded during the entire study period: Hp serology 17,291; CLO 10,070; SAT 8,331; UBT 322. Hp C&S was performed in only four cases during this time, rendering this test cohort inappropriate for further analysis. A total of 2,724 duplicate tests (50% of which was Hp serology) were identified and discounted from test positivity rate calculations. In addition, a total of 440 equivocal results (mostly Hp serology) were also excluded.

One hundred percent of SAT and roughly 75% of Hp serology tests were requested in primary care. The test utilisation by ethnicity is displayed in Table 1.

Relevant demographic data from official Canterbury censuses in 2013 and 2018 are provided for comparison in Table 2.[[4]]

Annual Hp test results are displayed in Figure 3. The test positivity rates appeared static overall during this period, however, the UBT cohort is too small to provide a reliable trend. Mean annual positive test rates over 2013–2018 period were: Hp serology 12.3%; CLO 7.2%; SAT 10.2%; UBT 17.5%. The compound mean annual test positivity across all test modalities was 10.4%, bearing in mind that an unknown number of patients could have been cross-tested with different test modalities that we couldn’t account for. A detailed breakdown by ethnicity is provided in Table 1.

Although we have no information regarding the actual indication to test, a vast majority was likely undertaken in symptomatic patients. We stress that this is not a cross-sectional population sample and that Hp infection is commonly asymptomatic.[[3]] As such, the data only show Hp positivity in the tested cohort, but do not show population prevalence.

View Supplementary material.

Discussion

This is the largest Hp test cohort published in New Zealand to date and the first study that directly addresses diagnostic costs. As this is only a regional study, we cannot assume similar trends and expenditure elsewhere in New Zealand. However, it is quite plausible that other DHBs would have comparable data, except perhaps for differing test positivity rates according to regional ethnicity profiles.

The progressive increase in testing and related expense isn’t surprising and mirrors current trends in healthcare in New Zealand. Nevertheless, the costs incurred are significant (Figure 2). Should the diagnostic practices be similar in the rest of New Zealand with a population of 5 million, the projected annual nationwide cost (as of 2018) would sit at around 2.5 million NZD. If we were to include histology from gastric biopsy (local price is $94.14 NZD), the annual cost might see further significant increase. Once again, this excludes the major cost of gastroscopy. Also notable is the discrepancy between population growth and number of tests performed. The Canterbury population has increased by 11.1% during this period. In contrast, overall Hp test numbers rose by 37% and Hp test expenditure by 42.6%. This small difference between test numbers and cost is explained by increasing use of SATs, which are more expensive.

In terms of general trends, both SAT and CLO utilisation is increasing. The rise in SAT likely relates to improved diagnostic pathway awareness, while the increasing CLO use could be in part due to a relative ease of access to gastroscopy. UBT, considered a gold standard, seems a more marginalised test now, likely owing to its relative complexity and difficult access. The essentially absent data on Hp antibiotic sensitivity/resistance is certainly troubling with potential negative implications for eradication treatment outcomes. There also continues to be a high usage of Hp serology despite the existing guidelines advising against this.[[5–7]] These guidelines suggest that such testing in a country with a low overall Hp prevalence (such as New Zealand) is best left for population-based research rather than for a diagnosis with intent to treat given its poor sensitivity and specificity in such setting.[[1,3]] In addition, the repetition of Hp serology testing in the same patient serves little purpose beyond increasing the overall costs and this was certainly a common occurrence in our cohort.

All of the non-serology-based tests, including SAT, CLO and UBT (and histology) rely on the presence of thriving Hp bacteria. The frequent use of proton pump inhibitors (PPIs) and antibiotics contributes to temporary suppression of Hp growth and thus significantly increases the rate of false negative test results.[[8–14]] In our experience, this well established phenomenon is often not accounted for in clinical practice, although we acknowledge this study offers no data to support this observation. Nevertheless, better awareness of these principles, especially in the realm of primary care, should lead to improved diagnosis (especially of the at-risk cohorts) and possibly to reduced costs related to better test utilisation.

In contrast to this potentially inappropriate overuse of tests, we found disproportionately low numbers of tests in at-risk ethnic minorities. For instance, Māori were significantly under-represented in all test modalities (Tables 1 and 2). This may well be yet another indicator of healthcare inequity in New Zealand. For illustration, the following compares the proportion of Hp tests in certain ethnicities in relation to the Canterbury Census; only 48.2% Māori and 67.8% Pasifika were tested for Hp compared with 82.7% of NZ Europeans. This is contrasted by significantly higher test positivity rates in these groups (Māori 21.2%, Pasifika 37.8%) compared with 8.4% in NZ Europeans. However, a particular test modality preference as opposed to test access could be a co-factor in certain cultures. A case in point might be the SAT cohort. We found this test to be significantly over-represented in our Asian subgroup (Table 1).

Data on Hp prevalence in New Zealand is patchy and varied.[[15–21]] Nonetheless, the overall Hp prevalence in this country is considered low by global standards (below 30%).[[1]] From the little information available, the South Island population seems to have a lower Hp prevalence than the North Island, likely owing to its differing ethnic make-up with a higher proportion of NZ Europeans.[[4]] A 1996 study from Canterbury found a Hp seroprevalence of 24% in this randomly selected population sample.[[21]] Approximately 20 years later, Hp seroprevalence in our tested cohort was 12.3%. As our cohort mostly consists of symptomatic patients, the true population seroprevalence in Canterbury may possibly be even lower. This trend is supported by other studies noting an overall decrease in seroprevalence in younger New Zealand birth cohorts.[[19,22]]

We found a surprisingly low test positivity in our CLO test cohort (7.2%). The explanation could lie in a combination of: poor test sensitivity in the presence of concurrent PPI use; relatively high numbers of NZ Europeans who underwent gastroscopy (>80%); opportunistic CLO testing at gastroscopy in the absence of relevant symptoms or findings; and, perhaps, a liberal access to gastroscopy with current referral guidelines anecdotally leading to a high number of gastroscopies with normal findings. Conversely, our UBT cohort had a relatively high positive test rate. However, this subgroup is more likely to represent either treatment failures or highly selected cases with resultant higher pre-test probability.

Our study drawbacks include lack of data on treatment and its outcomes as the local ethics approval specifically denied us access to this primary care-based information. In addition, no data exists on timing-dependent tests (UBT, SAT and CLO) in relation to PPI and/or antibiotic treatment. In other words, the rate of false negative test results is unknown, yet possibly significant. We haven’t examined histology from gastric biopsies that could provide additional data, however, even this test can be falsely negative in the presence of PPIs and/or antibiotics. Lastly, and perhaps most importantly, this study does not report a true population prevalence given the nature of our cohort.

In conclusion, Hp testing and related expenditure is increasing and is disproportionate to the population growth. At-risk ethnicities are underrepresented in the tested cohorts despite the significantly higher test positivity rates in these groups. A primary care-oriented focus on improved adherence to diagnostic guidelines along with emphasis on testing at-risk minorities could address both issues. This could bring both a cost reduction in Hp testing and possibly lead to improved health outcomes of those most at risk of Hp infection.

Summary

Abstract

Aim

To ascertain Helicobacter pylori (Hp) diagnosis trends and cost in a New Zealand cohort.

Method

All Hp tests within Canterbury between 2013–2018 were retrospectively reviewed, exclusive of histology. Overall numbers for each test modality, expenditure and test positivity rates were calculated and matched to ethnicity.

Results

Over the six-year period, Hp testing increased 37% and associated cost by 42.6%, compared with population growth of 11.1%. Primary care requested 82% of the non-invasive tests. Despite guidelines recommending against Hp serology, this was the most frequent test and duplicate testing in the same patient was common. Mean annual test positivity rates were: Hp serology 12.3%; Campylobacter-like organism 7.2%; Hp stool antigen test 10.2%; urea breath test 17.5%. The mean across all test modalities was 10.4%. Test proportion per ethnicity was lower in Māori (48.2%) and Pasifika (67.8%), compared with Europeans (82.7%). This was in contrast with significantly higher test positivity rates (Māori 21.2%, Pasifika 37.8%) compared with Europeans 8.4%.

Conclusion

Hp testing and related costs increase is disproportionate to population growth. At risk ethnicities are under-represented in the tested cohort despite higher test positivity rates. Primary care-focussed intervention could lead to reduced cost and improved equity in Hp diagnosis.

Author Information

Jan Kubovy: Consultant Gastroenterologist, Department of Gastroenterology, Christchurch Hospital, Christchurch, New Zealand. Murray L Barclay: Consultant Gastroenterologist and Clinical Pharmacologist, Departments of Gastroenterology and Clinical Pharmacology, Christchurch Hospital, and Clinical Professor, University of Otago, Christchurch, New Zealand.

Acknowledgements

Nikki Elliot, Canterbury Initiative Clinical Analyst.

Correspondence

Jan Kubovy: Department of Gastroenterology, Level 2, Riverside, Christchurch Hospital, Riccarton Avenue, Christchurch, 8011, New Zealand.

Correspondence Email

jan.kubovy@cdhb.health.nz

Competing Interests

Nil.

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2) Rothenbacher D, Brenner H. Burden of Helicobacter pylori and H. pylori-related diseases in developed countries: recent developments and future implications. Microbes Infect. 2003 Jul 1;5(8):693-703.

3) Malfertheiner P, Megraud F, O'morain CA, Gisbert JP, Kuipers EJ, Axon AT, Bazzoli F, Gasbarrini A, Atherton J, Graham DY, Hunt R. Management of Helicobacter pylori infection—the Maastricht V/Florence consensus report. Gut. 2017 Jan 1;66(1):6-30.

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7) World Gastroenterology Organisation Global Guidelines Helicobacter Pylori [Internet]. World Gastroenterology Organisation. [cited 2022]. Available at: https://www.worldgastroenterology.org/guidelines/helicobacter-pylori/helicobacter-pylori-english.

8) Manes G, Balzano A, Iaquinto G, Ricci C, Piccirillo MM, Giardullo N, Todisco A, Lioniello M, Vaira D. Accuracy of the stool antigen test in the diagnosis of Helicobacter pylori infection before treatment and in patients on omeprazole therapy. Dig Liver Dis. 2001 Jan 17;15(1):73-9.

9) Uotani T, Graham DY. Diagnosis of Helicobacter pylori using the rapid urease test. Ann Transl Med. 2015 Jan;3(1):215.

10) Shirin D, Matalon S, Avidan B, Broide E, Shirin H. Real-world Helicobacter pylori diagnosis in patients referred for esophagoduodenoscopy: The gap between guidelines and clinical practice. United European Gastroenterol J. 2016 Dec;4(6):762-9.

11) El-Serag HB, Kao JY, Kanwal F, Gilger M, LoVecchio F, Moss SF, Crowe S, Elfant A, Haas T, Hapke RJ, Graham DY. Houston consensus conference on testing for Helicobacter pylori infection in the United States. Clin Gastroenterol Hepatol. 2018 Jul 1;16(7):992-1002.

12) Taj Y, Essa F, Kazmi SU, Abdullah E. Sensitivity and specificity of various diagnostic tests in the detection of Helicobacter pylori. J Coll Physicians Surg P: JCPSP. 2003 Feb 1;13(2):90-3.

13) Olafsson S, Patel B, Jackson C, Cai J. Helicobacter Pylori Breath Testing in an Open Access System has a High Rate of Potentially False Negative Results due to Protocol Violations. Helicobacter. 2012 Oct;17(5):391-5.

14) Mittal S, Trakroo S, Kate V, Jagdish S. Evaluation of the effect of presence of blood in the stomach on endoscopic diagnostic tests for Helicobacter pylori infection. Indian Journal Med Microbiol. 2011 Oct 1;29(4):379-82.

15) Hsiang J, Selvaratnam S, Taylor S, Yeoh J, Tan YM, Huang J, Patrick A. Increasing primary antibiotic resistance and ethnic differences in eradication rates of Helicobacter pylori infection in New Zealand—a new look at an old enemy. NZ Med J. 2013 Oct 18;126(1384):64-76.

16) Fraser AG, Scragg R, Metcalf P, McCullough S, Yeates NJ. Prevalence of Helicobacter pylori infection in different ethnic groups in New Zealand children and adults. Aust N Z J Med. 1996 Oct;26(5):646-51.

17) Fraser AG, Peng SL, Jass JR. Intestinal metaplasia subtypes and Helicobacter pylori infection: a comparison of ethnic groups in New Zealand. J Gastroenterol Hepatol. 1998 Jun;13(6):560-5.

18) Fraser AG, Scragg R, Schaaf D, Metcalf P, Grant CC. Helicobacter pylori infection and iron deficiency in teenage females in New Zealand. N Z Med J. 2010;123(1313):38-45.

19) Fawcett JP, Shaw JP, Cockburn M, Brooke M, Barbezat GO. Seroprevalence of Helicobacter pylori in a birth cohort of 21-year-old New Zealanders. Eur J Gastroenterol Hepatol. 1996 Apr 1;8(4):365-9.

20) Fawcett JP, Shaw JP, Brooke M, Walker A, Barbezat GO. Seroprevalence of Helicobacter pylori in a longitudinal study of New Zealanders at ages 11 and 21. Aust N Z J Med. 1998 Oct;28(5):585-9.

21) Collett JA, Burt MJ, Frampton CM, Yeo KH, Chapman TM, Buttimore RC, Cook HB, Chapman BA. Seroprevalence of Helicobacter pylori in the adult population of Christchurch: risk factors and relationship to dyspeptic symptoms and iron studies. N Z Med J. 1999 Aug 1;112(1093):292-5.

22) McDonald AM, Sarfati D, Baker MG, Blakely T. Trends in Helicobacter pylori Infection Among Māori, Pacific, and European Birth Cohorts in New Zealand. Helicobacter. 2015 Apr;20(2):139-45.

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