Helicobacter pylori and Hetertopic Gastric Mucosain the Upper Esophagus (the Inlet Patch)Oscar Gutierrez, M.D., Taiji Akamatsu, M.D., Hector Cardona, M.D., David Y. Graham, M.D., andHala M.T. El-Zimaity, M.D.Gastrointestinal Mucosa Pathology Laboratory, Department of Medicine, Department of Pathology, VeteransAffairs Medical Center and Baylor College of Medicine, Houston, Texas, USA; Department of Endoscopy,Shinshu University Hospital, Matsumoto, Japan; and Department of Gastroenterology, National University ofColombia, Bogota, Colombia

OBJECTIVES: Helicobacter pylori (H. pylori) may colonizegastric mucosa wherever it is found in the GI tract. Heter-otopic gastric mucosa in the upper esophagus (inlet patch) isa potential site for H. pylori infection and may provide areservoir for oral-oral transmission or a niche where antibi-otics might have difficulty reaching. The aim of this studywas to analyze the intensity and distribution of H. pylori inthe inlet patch.

METHODS: Whenever a cervical inlet patch was observed,mucosal biopsy samples were taken to confirm the endo-scopic diagnosis and to search for H. pylori and activeinflammation. In addition, mucosal biopsy samples werealso taken from the gastric mucosa. Formalin-fixed biopsyspecimens were cut and stained with a new dual staindeveloped in our laboratory. The stain is a combination ofperiodic acid-Schiff and a silver stain that allows simulta-neous visualization of H. pylori and gastric type epithelium.The density of H. pylori was scored using a visual analogscale of 0 to 5. The type of mucosa in the inlet patch wasalso recorded.

RESULTS: The study included 48 patients; 37 had H. pylorigastritis and 27 of these (73%) had H. pylori identified ontheir heterotopic gastric mucosa. A higher density of H.pylori in the stomach was associated with a higher preva-lence in the inlets. Active inflammation correlated withactive infection in the inlet patch and the presence of antraltype mucosa.

CONCLUSION: H. pylori colonization of heterotopic gastricmucosa in the upper esophagus is common and is closelyrelated to the H. pylori density in the stomach. The fact thatH. pylori was not found in all cases suggests that anotherevent such as reflux may be required for H. pylori to colo-nize heterotopic mucosa. (Am J Gastroenterol 2003;98:1266–1270. © 2003 by Am. Coll. of Gastroenterology)

INTRODUCTION

Gastric type mucosa occurring in the upper one third of theesophagus within 3 cm of the upper esophageal sphincter isdesignated the “inlet patch.” Macroscopically, the inletpatch typically has a deep pink, velvety appearance; itpresents either as a single patch or as multiple patches ofgastric mucosa situated just below the upper esophagealsphincter. Microscopically, the patch can be lined witheither cardiac type glands or gastric body type mucosa. Asinlet patches are typically small (size range, �1 cm to �5cm) (1), the presence of an inlet patch is often overlooked atendoscopy; the chance of it being discovered is related tosize.

Inlet patches are found in approximately 2–4% of esoph-agi (2, 3) in all age groups. They are generally considered anincidental congenital finding, and most patients have nosymptoms referable to the inlet patch. Nonetheless, thepatch can become the site of small peptic erosions/ulcers,stenosis, fistula, intestinal metaplasia (4), high grade dys-plasia (5, 6), or adenocarcinoma (7–11). We report a pro-spective observational study designed to examine the rela-tionship of Helicobacter pylori (H. pylori) colonization ofheterotopic gastric mucosa at the upper esophagus (i.e., inletpatches).

MATERIALS AND METHODS

Study PatientsOver a 1-yr recruitment period, cervical inlet patches werespecifically looked for in patients undergoing upper GIendoscopy at the University Hospital of the National Uni-versity of Colombia, Bogota, Colombia. Patients were re-ferred for endoscopy for a variety of reasons, primarily forevaluation of dyspepsia. Heterotopic gastric mucosa of theupper esophagus was identified as salmon-rose patches thatwere clearly distinct from the adjacent grayish-pearlyesophageal mucosa (Fig. 1). Mucosal biopsy samples weretaken from the inlet patch (before the endoscope entered thestomach) and from the gastric mucosa. Gastric mucosal

THE AMERICAN JOURNAL OF GASTROENTEROLOGY Vol. 98, No. 6, 2003© 2003 by Am. Coll. of Gastroenterology ISSN 0002-9270/03/$30.00Published by Elsevier Inc. doi:10.1016/S0002-9270(03)00267-3

biopsy samples were obtained from predetermined, anatom-ically defined locations along the greater and lesser curva-ture of the stomach (12). The samples were taken usinglarge cup forceps (RADIAL JAW, MicroVasive, Water-town, MA).

At endoscopy, patients were classified according to thepresence of erosive esophagitis, gastroesophageal reflux dis-ease (GERD), and/or hiatal hernia. GERD patients wereclassified into five grades according to the criteria of Savaryand Miller (13).

The investigation conformed to principles outlined in theDeclaration of Helsinki. Informed consent was obtainedfrom all subjects, and the ethical review committee of theUniversidad Nacional de Colombia in Bogota, Colombia,approved the study.

Mucosal BiopsiesEach biopsy specimen was placed in a separate bottle offormalin and routinely processed. Serial sections were cut at4 �m and stained with a triple stain, either the Genta triplestain (14) or El-Zimaity triple stain (15). Each specimen wasreviewed by one pathologist and scored using a visualanalog scale from 0 (absent/normal) to 5 (maximal inten-sity) for H. pylori, polymorphonuclear leukocytes, and in-testinal metaplasia (16). The type of epithelium in the inletpatch biopsy sample was recorded. In addition, all biopsysamples from the inlet patch were stained with El-Zimaitydual stain (17) with hematoxylin as the counterstain (Figs. 1and 2). The dual stain uses a combination of periodic acid-Schiff and a silver stain, thus allowing simultaneous visu-alization of H. pylori and gastric type epithelium (18). Thisstain reliably allows recognition of even one or two bacteriapresent on the entire section. Briefly, slides are deparaf-finized, hydrated to water, oxidized in 0.5% periodic acidfor 5 min, and then placed in Schiff’s reagent for 3–5 min.They are stained with a modified silver method using he-matoxylin as counterstain (17).

Data AnalysesAll scores were entered into a database and analyzed usingSPSS 10 (SPSS, Chicago, IL) or STATA 7 (Stata, CollegeStation, TX). Analysis was done in several steps. First,variables were screened independently for association withpresence of H. pylori or active inflammation in the inletpatch. Fisher’s exact test or, when appropriate, the �2 test(both two-tailed) were used for comparison of proportions.Next, the results were used to construct a model (or models)to predict the presence of H. pylori or active inflammationin the inlet patch. All variables were treated as categoricalvariables in the univariate as well as the multivariate anal-ysis stage. Variables with statistical significance at the uni-variate level, as well variables with particular clinical inter-est, were entered in the final model. A model was developedthrough consecutive steps of backward elimination of non-significant variables and using goodness of fit tests. Statis-tical significance of differences and relationships were de-termined by p values of �0.05. Odds ratios were derivedfrom the coefficients of the model.

Figure 1. Inlet patches are located in the upper esophagus and hasantral type, transitional mucosa, or fundic type epithelium sur-rounded with esophageal squamous epithelium (El-Zimaity dualstain, �4).

Figure 2. H. pylori density is typically lower than that seen in thecorresponding stomach with few bacilli seen in the inlet patch(El-Zimaity dual stain, � oil immersion).

1267AJG – June, 2003 H. pylori in the Upper Esophagus

RESULTS

PatientsOver a 1-yr period, a total of 1495 patients undergoingupper GI endoscopy were screened endoscopically for thepresence of “inlet patch.” In all, 57 patients (29 male and 28female; median age 41 yr, range 17–75 yr) were identified.In nine patients the inlet biopsy samples were too small andsuperficial for detailed analyses, and these patients wereexcluded from the analyses. Clinical information was notavailable in three patients. The prevalence of the evaluatedclinical characteristics of patients with inlet patch, as well ascharacteristics of an age- and sex-matched control group,are summarized in Table 1.

Histological FeaturesA total of 152 slides were examined from the 48 patientsincluded in the study: 103 from the stomach (median two,range two to eight), and 49 from the inlet patch (median one,range one to two). The inlet patch had antral type mucosa in25 cases (54%), fundic type epithelium in five (11%), andtransitional mucosa in 16 (35%). In two patients, inlet patchmucosa was replaced with intestinal metaplasia.

H. pyloriH. pylori was identified in the inlet patch 73% (27/37) ofpatients with active H. pylori infection and in none (0/11) ofthe patients who were negative for gastric H. pylori infec-tion (p � 0.001) (Table 2). When H. pylori were seen, thedensity of infection was lower than that seen in the corre-sponding stomach (inlet H. pylori mean and median 2, range1–4 vs gastric H. pylori mean and median 3, range 1–5)(Fig. 2).

The type of mucosa did not influence its colonization withH. pylori. For example, among the 27 patients who were

positive for both gastric and inlet patch H. pylori, the inletpatch mucosa was antral type in 15, oxyntic type in three,and transitional type in nine. Of the 10 patients who werepositive for gastric H. pylori but negative for inlet H. pylori,the inlet patch had antral type mucosa in six cases andtransitional type mucosa in four (p � 0.548).

With univariate analysis in the logistic model, significantpredictors of the presence of H. pylori in the inlet patch weregastric H. pylori density (p � 0.008), age (p � 0.05), andpresence of a hiatal hernia (p � 0.06). The type of mucosa(antral type vs corpus-like) was not a significant predictorfactor for the presence of H. pylori (p � 0.816). GERD wasnot a significant predictor factor for the presence of H.pylori in the inlet patch. We evaluated for possible interac-tion of the various factors (e.g., reflux and/or hiatal herniawith H. pylori density in the stomach). None of these factorswere found to be significant. The final logistic model in-cluded gastric H. pylori density, age, and presence of ahiatal hernia. Gastric H. pylori density in the stomach wasthe only significant predictor of H. pylori status in the inletpatch (p � 0.03). For a SD increase in gastric H. pyloridensity, a finding of H. pylori in the inlet patch was twotimes more likely (OR � 2.284; 95% CI � 1.066–4.89)(Table 3).

Acute and Chronic InflammationACTIVE INFLAMMATION IN THE INLET PATCH.Active inflammation correlated well with active infectionand mucosa type. Patients with active infection and antraltype mucosa in the inlet patch were more likely to haveactive inflammation (p � 0.01). This relationship was alsoconfirmed using a logistic regression model. At the univar-iate level, the presence of H. pylori in the inlet (p � 0.047),as well as the type of mucosa (p � 0.008), were significantpredictors of the presence of active inflammation in the inletpatch. Other factors such as age, sex, and the presence of ahiatal hernia or reflux did not influence the presence ofactive inflammation in the inlet. Possible interactions amongvarious factors (e.g., reflux and/or hiatal hernia with H.pylori density in the stomach) were examined, and none wassignificant. The final logistic model included inlet H. pyloridensity, inlet mucosa type, presence of reflux and/or hiatalhernia, and age. At the multivariate level (final model), inletH. pylori density and type of mucosa were the only predic-tors of the presence of active inflammation in the inlet,holding all other factors in the model constant (p � 0.01)(Table 3). The odds of having active inflammation were twoto three times higher in patients with active H. pylori infec-tion in the inlet in nonoxyntic mucosa (antral or transitional)(OR � 2.48; 95% CI � 1.13–9.31).

CHRONIC INFLAMMATION IN THE INLET PATCH.The scores for chronic inflammation (mononuclear cells)were similar in patients with and without H. pylori infection,irrespective of inlet patch mucosa type (p � 1.00).

Table 1. Prevalence of Clinical Features Evaluated

Clinical Feature

Inlet PatchPatients: Frequency

(%)

Control Group:Frequency

(%)

Hiatal hernia 23/45 (51.1) 15/45 (33.3)Reflux (heartburn) 30/45 (66.7) 14/45 (31.1)Endoscopic esophagitis 13/45 (27.1) 11/45 (24.4)Barrett’s esophagus 1/45 0/45Duodenal ulcer 9/45 (20) 6/45 (13.3)H. pylori infection 37/45 (82%) 42/45 (93.3)

Table 2. Correlation of Active Inflammation in Inlet Patch WithH. pylori Infection

Inlet PatchH. pylori

Inlet Patch ActiveInflammation

TotalAbsent Present

Absent Gastric H. pylori Absent 8 1 9Present 7 3 10

Total 15 4 19Present Gastric H. pylori Present 14 13 27

Total 14 13 27

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Inlet Intestinal MetaplasiaIntestinal metaplasia was identified in the inlet patch inseven patients. H. pylori was present in the gastric and inletmucosa in four patients. Two patients had complete replace-ment of the underlying mucosa with intestinal metaplasia.The type of mucosa was evaluated in the remaining fivepatients; two had antral type and three transitional type.Active inflammation was present in two patients (scores 2and 3); both were positive for inlet H. pylori. Clinicalinformation was available in the seven patients. Three pa-tients had clinical and endoscopic evidence of GERD (H.pylori negative), and one patient had a hiatal hernia (H.pylori positive). Clinical and endoscopic evidence of GERDor hiatal hernia were not present in the remaining threepatients; two were positive for H. pylori. The number ofpatients with intestinal metaplasia in the inlet patch was toosmall for further analysis.

Correlation With Clinical and Endoscopic FindingsThe presence of clinical or endoscopic evidence of refluxand/or hiatal hernia had no influence on mucosal coloniza-tion with H. pylori or on the presence of active inflamma-tion. In both models that were developed to assess differ-ences in having inlet mucosa colonized with H. pylori oractive inflammation, the presence of reflux and/or hiatalhernia did not influence disease outcome (Table 3). Theseresults were consistent irrespective of GERD or hiatal her-nia severity.

DISCUSSION

Heterotopic gastric mucosa has been described throughoutthe GI tract including the tongue, floor of the mouth, sub-mandibular gland, small intestine, pancreas, gallbladder,and Meckel’s diverticulum (19–24). The term “inlet patch”is given to small islets of glandular tissue resembling gastricglands that are found in the esophagus within 3 cm of theupper esophageal sphincter (hence the designation “inletpatch”) (1). Although some autopsy studies have been done(25), no systematic approach is used to identify such cases,and the incidence is thus probably higher than the reportedprevalence of 2–4% (2, 3).

Although the origin of heterotopic gastric mucosa hadbeen a subject of debate (4, 26), most agree that it is likely

caused by entrapment of undifferentiated endodermal cellsduring development (27). At approximately 10 wk of ges-tation, a single layer of columnar cells lines the esophagus.Stratified squamous epithelium appears at 5 months of ges-tation in the middle third of the esophagus and extendsproximally and distally (28). If this process is not complete,some columnar cells may persist at birth, usually distallyover the esophageal cardiac glands or proximally over theupper one third of the esophagus (4, 27). Although mostheterotopias are innocuous phenomena, pathologicalchanges such as high grade dysplasia (5, 6) and adenocar-cinoma (7–11) have been described within the inlet patch.Considering H. pylori’s affinity for gastric-type mucosa(29–31), the importance of studying the relationship be-tween such mucosa and H. pylori seems obvious. Yet, moststudies have either ignored the issue (4) or have examinedH. pylori in heterotopic mucosa without providing informa-tion regarding the individual’s H. pylori status in the stom-ach (2, 32).

In the current study, H. pylori colonization of heterotopicgastric mucosa in the upper esophagus was common andclosely related to H. pylori density in the stomach (p �0.01). We took special care to biopsy the inlet patch beforeexamining the stomach to exclude the possibility that thepresence of H. pylori in the esophagus was related to con-tamination when the endoscope was withdrawn. Active in-flammation in the inlet patch was related to H. pylori pres-ence in the inlet patch. Superficially, our study is somewhatat odds with prior studies reporting that H. pylori was rarelyobserved in inlet patch mucosa (2, 33, 34) and that thepresence of H. pylori had no apparent correlation with acuteor chronic inflammation in the inlet patch (34). It is likelythat the difference between results relates to the backgroundprevalence of H. pylori infection in the population. Thisstudy was performed in Colombia, where H. pylori is veryprevalent. In prior studies, H. pylori was found in the inletpatch in 35% (34) and 50% (33) of the subset with gastricH. pylori. The low score of H. pylori in the inlet patch (meanand median 2) indicates that it would be easy to miss thebacteria histologically unless a specific stain such as the dualstain was used.

Avidan et al. (4), while studying 53 patients with cervicalinlet patch, found a significant association with Barrett’s

Table 3. OR Stratified by the Dependent Variable

Dependent Variable Independent VariableDelta

Coefficient* p Value OR 95% CI

Inlet H. pylori Gastric H. pylori 0.958* 0.028 2.284* 1.066 4.891Age 0.483 0.993 1.002 0.491 2.044Hiatal hernia �0.052 0.160 0.375 0.091 1.535

Inlet active inflammation Mucosa 1.25* 0.01 3.51* 1.24 9.94Inlet H. pylori 1.06* 0.01 2.89* 1.18 7.11Inlet H. pylori, mucosa type* 0.910* 0.019 2.48* 1.13 9.31Age 1.29 0.13 3.64 0.62 21.20Reflux �0.53 0.305 5.77 0.233 1.610

* Inlet H. pylori mucosa type is an interactive term. *Delta � 1 SD rather than 1 unit.

1269AJG – June, 2003 H. pylori in the Upper Esophagus

esophagus as well as with gastric ulcer. Although none ofour patients had Barrett’s esophagus, active inflammation inthe inlet patch correlated with both H. pylori infection andthe presence of antral type mucosa (p � 0.019). In thisstudy, the presence of GERD or hiatal hernia did not cor-relate with inlet patch colonization by H. pylori or with thepresence of active inflammation. The mechanism of H.pylori colonization of the inlet patch is unclear. Althoughcontamination can occur during ingestion of food, the cor-relation between gastric and inlet H. pylori suggest thatsome degree of reflux might play a role (35). It is not knownwhat effect cure of H. pylori infection might have on an inletpatch. Such a study is currently underway.

Reprint requests and correspondence: Hala M.T. El-Zimaity,M.D., Veterans Affairs Medical Center (111-D), Room 3A-320,2002 Holcombe Boulevard, Houston, TX 77030.

Received July 11, 2002; accepted Jan. 24, 2003.

REFERENCES

1. Owen DA. Stomach. In: Sternberg S, ed. Histology for pa-thologists, second ed. Philadelphia: Lippincott-Raven, 1997:481–93.

2. Jacobs E, Dehou MF. Heterotopic gastric mucosa in the upperesophagus: A prospective study of 33 cases and review ofliterature. Endoscopy 1997;29:710–5.

3. Borhan-Manesh F, Farnum JB. Incidence of heterotopic gas-tric mucosa in the upper oesophagus. Gut 1991;32:968–72.

4. Avidan B, Sonnenberg A, Chejfec G, et al. Is there a linkbetween cervical inlet patch and Barrett’s esophagus? Gastroi-ntest Endosc 2001;53:717–21.

5. Klaase JM, Lemaire LCJM, Rauws EAJ, et al. Heterotopicgastric mucosa of the cervical esophagus: A case of high-gradedysplasia treated with argon plasma coagulation and a case ofadenocarcinoma. Gastrointest Endosc 2001;53:101–4.

6. Mion F, Lambert R, Partensky C, et al. High-grade dysplasiain an adenoma of the upper esophagus developing on hetero-topic gastric mucosa. Endoscopy 1996;28:633–5.

7. Berkelhammer C, Bhagavan M, Templeton A, et al. Gastricinlet patch containing submucosally infiltrating adenocarci-noma. J Clin Gastroenterol 1997;25:678–81.

8. Sperling RM, Grendell JH. Adenocarcinoma arising in an inletpatch of the esophagus. Am J Gastroenterol 1995;90:150–2.

9. Lauwers GY, Scott GV, Vauthey JN. Adenocarcinoma of theupper esophagus arising in cervical ectopic gastric mucosa:Rare evidence of malignant potential of so-called “inletpatch.” Dig Dis Sci 1998;43:901–7.

10. Goodwin WJ, Larson DL, Sajjad SM. Adenocarcinoma of thecervical esophagus in a patient with extensive columnar cell-lined (Barrett’s) esophagus. Otolaryngol Head Neck Surg1983;91:446–9.

11. Takagi A, Ema Y, Horii S, et al. Early adenocarcinoma arisingfrom ectopic gastric mucosa in the cervical esophagus. Gas-trointest Endosc 1995;41:167–70.

12. El-Zimaity HMT, Al-Assi MT, Genta RM, Graham DY. Con-firmation of successful therapy of Helicobacter pylori infec-tion: Number and site of biopsies or a rapid urease test. Am JGastroenterol 1995;90:1962–4.

13. Ollyo JB, Fontolliet CH, Brossard E, Lang F. Savary’s newendoscopic classification of reflux esophagitis. Acta Endosc1992;22:307–20.

14. Genta RM, Robason GO, Graham DY. Simultaneous visual-

ization of Helicobacter pylori and gastric morphology: A newstain. Hum Pathol 1994;25:221–6.

15. El-Zimaity HMT, Ota H, Scott S, et al. A new triple stain forHelicobacter pylori suitable for the autostainer. Arch PatholLab Med 1998;122:732–6.

16. El-Zimaity HMT, Graham DY, Al-Assi MT, et al. Interob-server variation in the histopathological assessment of Heli-cobacter pylori gastritis. Hum Pathol 1996;27:35–41.

17. El-Zimaity HMT, Wu J, Akamatsu T, Graham DY. A reliablemethod for the simultaneous identification of H. pylori andgastric metaplasia in the duodenum. J Clin Pathol 1999;52:914–6.

18. El-Zimaity HMT, Wu J, Akamatsu T, Graham DY. A reliablemethod for the simultaneous identification of H. pylori andgastric metaplasia in the duodenum. J Clin Pathol 1999;52:914–6.

19. Taylor AL. The epithelial heterotopias of the alimentary tract.J Pathol Bacteriol 1927;30:415–49.

20. Wolff M, Rankow RM. Heterotopic gastric epithelium in thehead and neck region. Ann Plast Surg 1980;4:53–64.

21. Devereaux CE, Devereaux RG. Heterotopic gastric mucosa ofthe rectum with a review of the literature. J Clin Gastroenterol1994;19:41–5.

22. Shim YT, Kim SY. Heterotopic gastric mucosa and pancreatictissue in the skin of the abdominal wall. J Pediatr Surg 1992;27:1539–40.

23. Lamont N, Winthrop AL, Cole FM, et al. Heterotopic gastricmucosa in the gallbladder: A cause of chronic abdominal painin a child. J Pediatr Surg 1991;26:1293–5.

24. Kalman PG, Stone RM, Phillips MJ. Heterotopic gastric tissueof the bile duct. Surgery 1981;89:384–6.

25. Variend S, Howat AJ. Upper oesophageal gastric heterotopia:A prospective necropsy study in children. J Clin Pathol 1988;41:742–5.

26. Rattner HM, McKinley MJ. Heterotopic gastric mucosa of theupper esophagus. Gastroenterology 1986;90:1309 (letter).

27. Gray SW, Skandalikis JE. The esophagus. In: Gray SW, Skan-dalikis JE, eds. Embryology for surgeons. Philadelphia: WBSaunders, 1972:63–100.

28. Enterline H, Thompson J. The normal esophagus—embryol-ogy, structure, and function. In: Enterline H, Thompson JS,eds. Pathology of the esophagus. New York: Springer-Verlag,1984:1–26.

29. Kestemberg A, Marino G, de Lima E, et al. Gastric heterotopicmucosa in the rectum with Helicobacter pylori-like organisms:A rare cause of rectal bleeding. Int J Colorectal Dis 1993;8:9–12.

30. Stermer E, Hardoff D, Zuckerman E, Miselevich I. Helico-bacter pylori-associated peptic ulcer in heterotopic gastricmucosa within ileal duplication. J Clin Gastroenterol 1994;18:133–5.

31. Chan GS, Yuen ST, Chu KM, et al. Helicobacter pylori inMeckel’s diverticulum with heterotopic gastric mucosa in apopulation with relatively high H. pylori prevalence rate. JGastroenterol Hepatol 1999;14:313–6.

32. Cuddihy PJ, Maheshwar A, Griffith H. Symptomatic hetero-topic gastric mucosa in the upper oesophagus. J Laryngol Otol1998;112:979–81.

33. Flejou JF, Potet F, Molas G, et al. Campylobacter-like organ-isms in heterotopic gastric mucosa of the upper oesophagus.J Clin Pathol 1990;43:961 (letter).

34. Borhan-Manesh F, Farnum JB. Study of Helicobacter pyloricolonization of patches of heterotopic gastric mucosa (HGM)at the upper esophagus. Dig Dis Sci 1993;38:142–6.

35. Leung W-K, Siu KLK, Kwok CKL, et al. Isolation of Heli-cobacter pylori from vomitus in children and its implication ingastro-oral transmission. Am J Gastroenterol 1999;94:2881–4.

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