Carabotti M, D’Ercole C, Iossa A, Corazziari E, Silecchia G, Severi C. Helicobacter pylori infection in obesity and its clinical outcome after bariatric surgery. World J Gastroenterol 2014; 20(3): 647-653
Corresponding Author of This Article
Carola Severi, MD PhD, Assistant Professor, Department of Internal Medicine and Medical Specialties, University Sapienza, Viale del Policlinico, 00161 Roma, Italy. email@example.com
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Marilia Carabotti, Chiara D’Ercole, Enrico Corazziari, Carola Severi, Department of Internal Medicine and Medical Specialties, University Sapienza, 00161 Roma, Italy
Angelo Iossa, Gianfranco Silecchia, Department of Medical Surgical Sciences and Biotechnology, University Sapienza, 04100 Latina, Italy
ORCID number: $[AuthorORCIDs]
Author contributions: Carabotti M and Severi C contributed to study conception and design, and acquisition and interpretation of data, and wrote the manuscript; D’Ercole C and Iossa A contributed to the bibliographic research; Silecchia G and Corazziari E revised the manuscript critically for important intellectual content.
Supported by University Sapienza 000324_2012_AR_SEVERI-SEVERI-PROGETTO RICERCA SAPIENZA 2012
Correspondence to: Carola Severi, MD PhD, Assistant Professor, Department of Internal Medicine and Medical Specialties, University Sapienza, Viale del Policlinico, 00161 Roma, Italy. firstname.lastname@example.org
Telephone: +39-6-49978384 Fax: +39-6-4463737
Received: October 14, 2013 Revised: November 12, 2013 Accepted: November 28, 2013 Published online: January 21, 2014
The present review summarizes the prevalence and active clinical problems in obese patients with Helicobacter pylori (H. pylori) infection, as well as the outcomes after bariatric surgery in this patient population. The involvement of H. pylori in the pathophysiology of obesity is still debated. It may be that the infection is protective against obesity, because of the gastritis-induced decrease in production and secretion of the orexigenic hormone ghrelin. However, recent epidemiological studies have failed to show an association between H. pylori infection and reduced body mass index. H. pylori infection might represent a limiting factor in the access to bariatric bypass surgery, even if high-quality evidence indicating the advantages of preoperative H. pylori screening and eradication is lacking. The clinical management of infection is complicated by the lower eradication rates with standard therapeutic regimens reported in obese patients than in the normal-weight population. Prospective clinical studies to ameliorate both H. pylori eradication rates and control the clinical outcomes of H. pylori infection after different bariatric procedures are warranted.
Core tip: This review deals with the active clinical problems related to Helicobacter pylori (H. pylori) infection in obese patients. Even if still controversial, the infection might represent a confounding and limiting factor in bariatric surgery, due to the high incidence of postoperative foregut symptoms and/or lesions in non-eradicated patients. The controversies on preoperative H. pylori screening are highlighted, as well as those related to its clinical management, which is complicated by the low eradication rates in obesity. Finally, a revision of studies on the possible correlation between H. pylori and body mass index and its possible protective role in development of obesity is included.
Citation: Carabotti M, D’Ercole C, Iossa A, Corazziari E, Silecchia G, Severi C. Helicobacter pylori infection in obesity and its clinical outcome after bariatric surgery. World J Gastroenterol 2014; 20(3): 647-653
Helicobacter pylori (H. pylori) is one of the most common human infections and it is estimated that more than half of the world population is infected. H. pylori is an ancient colonizer of the human stomach and represents the main etiological factor in the development of gastritis, peptic ulcer and gastric malignant lesions. The infection is still highly prevalent in developing countries but it is disappearing in the developed world (Table 1; modified from). Indeed, epidemiological studies show that H. pylori infection still occurs more frequently in socioeconomically deprived populations living in crowded places with poor hygienic conditions, and conversely, has a lower frequency in people of high socioeconomic status. The influence of these factors on H. pylori infection in obesity remains to be ascertained. A study on obese patients who were candidates for bariatric surgery highlighted race as a risk factor for H. pylori infection, in that African-Americans and Hispanics had a higher probability than Caucasians of being infected, with significant odds ratios of 4.05 and 2.6, respectively. Interestingly, these two ethnic groups, at least in the United States, have the highest obesity rates.
Table 1 Prevalence of Helicobacter pylori infection in the general population worldwide.
United States and Canada
PREVALENCE OF H. PYLORI INFECTION IN OBESE PATIENTS
The prevalence of H. pylori infection in morbidly obese patients is still controversial. Candidates for bariatric surgery have a preoperative prevalence of H. pylori ranging from 8.7% in a German cohort to 85.5% in a Saudi cohort, with other series showing intermediate values. Overall, available studies report a lower prevalence of H. pylori infection in obese patients than in the general population (Table 2). Nevertheless, the few studies that have compared simultaneously the prevalence between lean and obese patients are in disagreement, with half[3,4,8] showing a higher H. pylori prevalence in obese patients and the other half[18,23,27] an opposite trend. Discrepancies might be related to both small sample size and variability in diagnostic testing. Different methods are used to diagnose H. pylori infection. Serology was largely used in these studies but it has a low diagnostic accuracy of only 80%-84%, and is only useful to exclude H. pylori infection. Indeed, positive serology should be confirmed by a test for active infection, such as stool antigen assay or urea breath test (UBT). The former has a sensitivity of 94% and a specificity of 92%, whereas UBT has a sensitivity of 88%-95% and specificity of 95%-100%. Finally, histology has an excellent sensitivity and specificity, especially when specific immunostaining is used to detect H. pylori bacteria, and could be partially replaced by biopsy urease testing in patients who have discontinued treatment with proton pump inhibitors or antibiotics.
Table 2 Prevalence of Helicobacter pylori infection in obese and normal weight patients worldwide.
% H. pylori + obese (n)
% H. pylori + control (n)
H. pylori detection
Serology + histology
ND: Not defined; H. pylori: Helicobacter pylori.
The majority of studies have used only one method to diagnose H. pylori infection. When more than one test was used, single tests were not compared with each other and used alternatively. The only study that compared serology to histology found good accordance between the two methods. Testing for active infection has been rare. UBT and stool antigen assay have been used only in one study, without any comparison with histology. Even though antisecretory therapy affects diagnostic accuracy of most H. pylori diagnostic tests, patients with ongoing antisecretory treatment have been excluded only in one study.
H. pylori infection plays a special role in obesity for two main reasons: (1) its possible relationship with body mass index (BMI); and (2) it is a negative factor in limiting access to bariatric surgery.
H. PYLORI INFECTION AND PATHOPHYSIOLOGY OF OBESITY
Both environmental and host agents are involved in the pathophysiology of obesity, including diet, physical inactivity, and drug use, but also genetics and neurophysiological factors. However, an established factor in the development of obesity is dysregulation of the mechanisms that control food intake; mainly under the control of the hormones leptin and ghrelin that are secreted by the gastric mucosa. Leptin primarily suppresses food intake and therefore induces weight loss. Ghrelin increases abruptly before the onset of a meal and decreases rapidly after eating; it has orexigenic effects and inhibits the secretion of leptin. The relationship between ghrelin and H. pylori infection in obesity has received much attention in recent years because H. pylori gastric mucosal colonization may impair gastric ghrelin production, with subsequent reduction of hunger. Consequently, it has been hypothesized that H. pylori infection might have a protective role against obesity.
Several studies[29-32] have investigated the relationship between H. pylori-related gastritis and ghrelin, by comparing H. pylori-positive with H. pylori-negative patients, or patients before and after eradication treatment, analyzing circulating ghrelin levels, the number of ghrelin immunoreactive cells per cubic millimeter in gastric mucosa[33-35] and ghrelin mRNA expression[33,36,37]. The results of these studies have been conflicting, however, a recent systematic review concluded that circulating ghrelin levels are lower in the presence of H. pylori infection. Moreover, studies dealing with morbidly obese patients who are candidates for bariatric surgery have shown discordant results with regard to the relationship between H. pylori and ghrelin. Obese patients have been reported to have a reduced or increased number of immunoreactive ghrelin cells, even if their number was lower in H. pylori-positive than -negative patients.
A possible explanation of these conflicting results can be ascribed to H. pylori-related gastritis patterns. The outcome of H. pylori infection differs according to gastritis extension, which generally starts with antritis subsequently progressing to pan-gastritis, which may be associated with atrophy. In the presence of atrophy, secretory activity decreases, which probably involves ghrelin production. Upper gastrointestinal endoscopy with multiple mucosal sampling is required to define the pattern of H. pylori-related gastritis, even if an indirect non-invasive serological method is represented by the ratio between pepsinogen (PG) I and II; a low PG I/II ratio being suggestive of the presence of atrophy. By the use of PG I/II ratio, it has been shown that, within 1 year of H. pylori eradication, BMI increased only in the low PG I/II ratio group, suggesting that the sole presence of atrophy has a relevant role in influencing body weight. Indeed BMI, after adjusting for sex and age, was significantly lower in patients with atrophic gastritis than in those without atrophy. Other factors can contribute to explain the controversial results about the relationship between H. pylori and ghrelin. First, the different time elapsing from eradication might have influenced the mucosal healing process and then restored normal secretory activity. Second, age might play a role because atrophy is more frequent in elderly patients. Finally, changes in plasma ghrelin concentrations are not strictly associated with gastric mucosal expression and this may be attributed to the presence of ghrelin isoforms with different biological activities.
H. PYLORI INFECTION AND BMI
Even if the significant increase in BMI observed after H. pylori eradication treatment highlights a possible inverse correlation between H. pylori infection and obesity, both in adults[44,45] and children, available data are controversial. Indeed, several studies did not find any influence of bacterial eradication on body weight[37,47]. Furthermore, epidemiological studies have failed to show any association between H. pylori infection and BMI, with a meta-analysis of 18 observational studies, including 10000 subjects, that reported a slightly higher BMI in H. pylori-positive patients.
Two theories emerge from these studies. Studies that observed a significant increase in BMI after successful H. pylori eradication support a protective role of infection towards obesity, which likely occurs through decreased production and secretion of the orexigenic hormone ghrelin. Studies reporting a higher prevalence of infection in obese patients disclaim a protective role of H. pylori and support the increased incidence and severity of infection observed in obese patients. Obesity can alter innate and adaptive immunity, with immunological impairment related to the grade of obesity, resulting in less maturation of monocytes into macrophages, reduced polymorphonuclear bactericidal capacity, and a significant decrease in NK cell activity.
However discrepancies among studies can be ascribed to other factors. As previously mentioned, a misleading factor is the frequent lack of classification of the patients according to their gastritis patterns, especially atrophy. Furthermore, the relationship between H. pylori and BMI can be strongly influenced by the dietary change that can occur after eradication. Indeed, H. pylori eradication can ameliorate dyspeptic symptoms favoring dietary excess.
H. PYLORI AND BARIATRIC SURGERY
In the field of bariatric surgery, the American Association of Clinical Endocrinologists/The Obesity Society/American Society for Metabolic and Bariatric Surgery guidelines do not provide clear indication about preoperative H. pylori screening and management. The document recommends H. pylori screening in patients belonging to high-prevalence areas and upper endoscopy in selected cases. Previous European guidelines recommended upper gastrointestinal endoscopy before bariatric surgery in any symptomatic or asymptomatic patient in order to treat any lesions, including H. pylori infection, that may cause postoperative complications. The advantages of preoperative H. pylori screening and eradication are still controversial, mainly due to a lack of randomized control trials (RCTs). However, different attitudes might be influenced by the differences in health systems and access to upper gastrointestinal endoscopy.
Routine upper endoscopy studies, with concurrent H. pylori screening and biopsies to rule out pathological abnormalities (e.g., esophagitis, polyps, hiatal hernia, gastritis, and duodenitis), have reported that abnormalities are present in up to 91% of bariatric candidates[12,16,22], with a higher incidence in patients with concomitant H. pylori infection[11,14,52]. Some of these alterations are expected to be cured by tailored bariatric surgery (i.e., hiatal hernia and gastroesophageal reflux disease), even if the main concern is represented by postsurgical gastric malignancy, especially after bariatric procedures with gastric bypass. The majority of obese patients with upper gastrointestinal lesions at the time of routine preoperative endoscopy are asymptomatic, with only 20% of the obese patients with pathological findings presenting with upper gastrointestinal symptoms. Also, esophageal dysmotility, frequently observed in these patients, occurs in the absence of symptoms. The lack of visceral sensation in obese patients has been ascribed to alterations in the autonomic nervous system[55,56]. Thus, the decision to perform endoscopy before bariatric surgery on the basis of clinical presentation may be misleading.
Concerning the management of obese patients who are candidates for bariatric surgery, the main clinical issue is represented by H. pylori resistance to antibiotic eradication, which could delay access to bariatric surgery. Obese patients showed a significantly lower rate of eradication than controls, at least to the 7-d regimens, with BMI being an independent risk factor for eradication failure. Although the mechanisms by which obese patients have a poor eradication rate remain to be elucidated, it seems likely to be due to the following reasons leading to subtherapeutic drug concentrations. First, the physiological changes that occur in obesity, such as possible delayed gastric emptying, may lead to a decrease in the rate of drug absorption, regardless of the characteristics of the drug. Second, the volume of distribution of drugs may be altered in obese patients because the increased adipose tissue mass can influence medications with lipophilic properties[59,60]. Clearly, the need of a tailored eradication regimen for obese patients based on body weight arises, but no clinical trials have compared standard therapy versus weight-based regimens. An increase in the eradication treatment efficacy can be obtained by extending the treatment period. A recent trial, aimed to compare 7- and 14-d first-line treatment with clarithromycin-based triple therapy in obese patients, showed that the latter is more effective.
EFFECT OF H. PYLORI INFECTION ON BARIATRIC SURGERY OUTCOMES
The majority of the studies, focused on standard laparoscopic Roux-en-Y gastric bypass (LRYGB) outcomes, have reported a reduced prevalence of postsurgical lesions after successful H. pylori eradication. After LRYGB, H. pylori eradicated patients present with a reduced incidence of viscus perforations and of postoperative marginal ulcers. In this latter retrospective study of 560 patients, the incidence of ulcers was 2.4% in patients that were tested and treated for H. pylori infection prior to surgery compared to 6.8% in those who did not undergo such screening. However, other authors have reported that, even though marginal ulcer rates following gastric bypass were higher in patients with H. pylori, the higher risk persisted even if the pathogen had been eradicated. Indeed, after either LRYGB or laparoscopic sleeve gastrectomy[65,66], postsurgical lesions, mainly concerning gastric ulcers, are attributed to surgical procedures, and not to H. pylori infection. Moreover a recent retrospective study did not show any effect of H. pylori status, whether preoperatively positive or persistently positive after treatment, on the rates of marginal ulcer or stomal stenosis in patients undergoing LRYGB. So far, high-quality evidence indicating the advantages of preoperative H. pylori screening and eradication is lacking and prospective well-designed RCTs are necessary to establish the real clinical outcomes of H. pylori-positive and -negative patients after surgery. It should also be considered that the gastric environment for H. pylori colonization may dramatically change after bariatric surgery with possible spontaneous clearance of infection.
If the management of H. pylori infection in obese patients who are candidates for bariatric surgery is still controversial, there are plausible reasons to attempt eradication in H. pylori-positive patients, particularly in those undergoing LRYGB in whom a large part of the stomach is inaccessible to upper endoscopy after surgery. First, eradication should decrease the risk of gastroduodenal peptic lesions in the gastrojejunostomy site after gastric bypass, and thus decrease early as well as later ulcer-related postoperative symptoms and complications, which are higher in H. pylori-positive patients. Second, there is evidence of a moderate benefit of H. pylori on symptomatic dyspepsia[70,71]. Third, H. pylori is a class I carcinogen in the development of gastric cancer with an odds ratio of 2.0-5.9. A recent systematic review on upper gastrointestinal malignancy after bariatric surgery concluded that, even if the incidence were rare, it is advisable to screen patients before surgery because adenocarcinoma, strictly related to H. pylori infection, was present in most cases. In addition, the coexistence of H. pylori infection with obesity can potentiate the cytokine-mediated crosstalk between inflamed gastric and adipose tissues, augmenting immune responses at both sites, and thereby contributing to a pro-tumorigenic gastric microenvironment.
Available data on H. pylori infection and obesity are still controversial. Current guidelines do not indicate clearly the management of H. pylori infection in obese patients who are candidates for bariatric surgery, and the need for H. pylori screening and eradication before surgery is still debated. The eradication treatment is often hampered by the low eradication rates obtained with first-line 7-d treatment. Prospective clinical studies aimed to ameliorate both H. pylori eradication rates and to evaluate the clinical outcomes of H. pylori infection after the different bariatric procedures are warranted.
P- Reviewers: Hussain A, Leitman IM, Wilcox CM S- Editor: Cui XM L- Editor: A E- Editor: Zhang DN
Malfertheiner P, Megraud F, O’Morain CA, Atherton J, Axon AT, Bazzoli F, Gensini GF, Gisbert JP, Graham DY, Rokkas T. Management of Helicobacter pylori infection--the Maastricht IV/ Florence Consensus Report.Gut. 2012;61:646-664.
Iwańczak F, Iwańczak B. Treatment of Helicobacter pylori infection in the aspect of increasing antibiotic resistance.Adv Clin Exp Med. 2012;21:671-680.
Arslan E, Atilgan H, Yavaşoğlu I. The prevalence of Helicobacter pylori in obese subjects.Eur J Intern Med. 2009;20:695-697.
Erim T, Cruz-Correa MR, Szomstein S, Velis E, Rosenthal R. Prevalence of Helicobacter pylori seropositivity among patients undergoing bariatric surgery: a preliminary study.World J Surg. 2008;32:2021-2025.
Nassir R, Qi L, Kosoy R, Garcia L, Allison M, Ochs-Balcom HM, Tylavsky F, Manson JE, Shigeta R, Robbins J. Relationship between adiposity and admixture in African-American and Hispanic-American women.Int J Obes (Lond). 2012;36:304-313.
Küper MA, Kratt T, Kramer KM, Zdichavsky M, Schneider JH, Glatzle J, Stüker D, Königsrainer A, Brücher BL. Effort, safety, and findings of routine preoperative endoscopic evaluation of morbidly obese patients undergoing bariatric surgery.Surg Endosc. 2010;24:1996-2001.
Al-Akwaa AM. Prevalence of Helicobacter pylori infection in a group of morbidly obese Saudi patients undergoing bariatric surgery: a preliminary report.Saudi J Gastroenterol. 2010;16:264-267.
Dutta SK, Arora M, Kireet A, Bashandy H, Gandsas A. Upper gastrointestinal symptoms and associated disorders in morbidly obese patients: a prospective study.Dig Dis Sci. 2009;54:1243-1246.
Verma S, Sharma D, Kanwar P, Sohn W, Mohanty SR, Tortolani AJ, Gorecki P. Prevalence of Helicobacter pylori infection in bariatric patients: a histologic assessment.Surg Obes Relat Dis. 2013;9:679-685.
Zeni TM, Frantzides CT, Mahr C, Denham EW, Meiselman M, Goldberg MJ, Spiess S, Brand RE. Value of preoperative upper endoscopy in patients undergoing laparoscopic gastric bypass.Obes Surg. 2006;16:142-146.
Ramaswamy A, Lin E, Ramshaw BJ, Smith CD. Early effects of Helicobacter pylori infection in patients undergoing bariatric surgery.Arch Surg. 2004;139:1094-1096.
Madan AK, Speck KE, Hiler ML. Routine preoperative upper endoscopy for laparoscopic gastric bypass: is it necessary?Am Surg. 2004;70:684-686.
Hartin CW, ReMine DS, Lucktong TA. Preoperative bariatric screening and treatment of Helicobacter pylori.Surg Endosc. 2009;23:2531-2534.
Vanek VW, Catania M, Triveri K, Woodruff RW. Retrospective review of the preoperative biliary and gastrointestinal evaluation for gastric bypass surgery.Surg Obes Relat Dis. 2006;2:17-22; discussion 22-23.
Papasavas PK, Gagné DJ, Donnelly PE, Salgado J, Urbandt JE, Burton KK, Caushaj PF. Prevalence of Helicobacter pylori infection and value of preoperative testing and treatment in patients undergoing laparoscopic Roux-en-Y gastric bypass.Surg Obes Relat Dis. 2008;4:383-388.
Csendes A, Burgos AM, Smok G, Beltran M. Endoscopic and histologic findings of the foregut in 426 patients with morbid obesity.Obes Surg. 2007;17:28-34.
Dietz J, Ulbrich-Kulcynski JM, Souto KE, Meinhardt NG. Prevalence of upper digestive endoscopy and gastric histopathology findings in morbidly obese patients.Arq Gastroenterol. 2012;49:52-55.
Maksud FA, Alves JS, Diniz MT, Barbosa AJ. Density of ghrelin-producing cells is higher in the gastric mucosa of morbidly obese patients.Eur J Endocrinol. 2011;165:57-62.
Teivelis MP, Faintuch J, Ishida R, Sakai P, Bresser A, Gama-Rodrigues J. Endoscopic and ultrasonographic evaluation before and after Roux-en-Y gastric bypass for morbid obesity.Arq Gastroenterol. 2007;44:8-13.
Muñoz R, Ibáñez L, Salinas J, Escalona A, Pérez G, Pimentel F, Guzmán S, Boza C. Importance of routine preoperative upper GI endoscopy: why all patients should be evaluated?Obes Surg. 2009;19:427-431.
de Moura Almeida A, Cotrim HP, Santos AS, Bitencourt AG, Barbosa DB, Lobo AP, Rios A, Alves E. Preoperative upper gastrointestinal endoscopy in obese patients undergoing bariatric surgery: is it necessary?Surg Obes Relat Dis. 2008;4:144-149; discussion 144-149.
Azagury D, Dumonceau JM, Morel P, Chassot G, Huber O. Preoperative work-up in asymptomatic patients undergoing Roux-en-Y gastric bypass: is endoscopy mandatory?Obes Surg. 2006;16:1304-1311.
Kyriazanos ID, Sfiniadakis I, Gizaris V, Hountis P, Hatziveis K, Dafnopoulou A, Datsakis K. The incidence of Helicobacter pylori infection is not increased among obese young individuals in Greece.J Clin Gastroenterol. 2002;34:541-546.
Almazeedi S, Al-Sabah S, Al-Mulla A, Al-Murad A, Al-Mossawi A, Al-Enezi K, Jumaa T, Bastaki W. Gastric histopathologies in patients undergoing laparoscopic sleeve gastrectomies.Obes Surg. 2013;23:314-319.
Wang HH, Lee WJ, Liew PL, Yang CS, Liang RJ, Wang W, Lin JT, Wu MS. The influence of Helicobacter pylori infection and corpus gastritis on the postoperative outcomes of laparoscopic vertical banded gastroplasty.Obes Surg. 2006;16:297-307.
Liew PL, Lee WJ, Lee YC, Chen WY. Gastric ghrelin expression associated with Helicobacter pylori infection and chronic gastritis in obese patients.Obes Surg. 2006;16:612-619.
Wu MS, Lee WJ, Wang HH, Huang SP, Lin JT. A case-control study of association of Helicobacter pylori infection with morbid obesity in Taiwan.Arch Intern Med. 2005;165:1552-1555.
Cummings DE. Helicobacter pylori and ghrelin: Interrelated players in body-weight regulation?Am J Med. 2004;117:436-439.
Nwokolo CU, Freshwater DA, O’Hare P, Randeva HS. Plasma ghrelin following cure of Helicobacter pylori.Gut. 2003;52:637-640.
Isomoto H, Ueno H, Saenko VA, Mondal MS, Nishi Y, Kawano N, Ohnita K, Mizuta Y, Ohtsuru A, Yamashita S. Impact of Helicobacter pylori infection on gastric and plasma ghrelin dynamics in humans.Am J Gastroenterol. 2005;100:1711-1720.
Gokcel A, Gumurdulu Y, Kayaselcuk F, Serin E, Ozer B, Ozsahin AK, Guvener N. Helicobacter pylori has no effect on plasma ghrelin levels.Eur J Endocrinol. 2003;148:423-426.
Osawa H, Kita H, Ohnishi H, Nakazato M, Date Y, Bowlus CL, Ishino Y, Watanabe E, Shiiya T, Ueno H. Changes in plasma ghrelin levels, gastric ghrelin production, and body weight after Helicobacter pylori cure.J Gastroenterol. 2006;41:954-961.
Osawa H, Nakazato M, Date Y, Kita H, Ohnishi H, Ueno H, Shiiya T, Satoh K, Ishino Y, Sugano K. Impaired production of gastric ghrelin in chronic gastritis associated with Helicobacter pylori.J Clin Endocrinol Metab. 2005;90:10-16.
Méndez-Sánchez N, Pichardo-Bahena R, Vásquez-Fernández F, Lezama-Mora JI, León-Canales AL, Barredo-Prieto B, González-Avila D, Ponciano-Rodríguez G, Uribe M. Effect of Helicobacter pylori infection on gastric ghrelin expression and body weight.Rev Gastroenterol Mex. 2007;72:359-364.
Tatsuguchi A, Miyake K, Gudis K, Futagami S, Tsukui T, Wada K, Kishida T, Fukuda Y, Sugisaki Y, Sakamoto C. Effect of Helicobacter pylori infection on ghrelin expression in human gastric mucosa.Am J Gastroenterol. 2004;99:2121-2127.
Isomoto H, Nakazato M, Ueno H, Date Y, Nishi Y, Mukae H, Mizuta Y, Ohtsuru A, Yamashita S, Kohno S. Low plasma ghrelin levels in patients with Helicobacter pylori-associated gastritis.Am J Med. 2004;117:429-432.
Jang EJ, Park SW, Park JS, Park SJ, Hahm KB, Paik SY, Sin MK, Lee ES, Oh SW, Park CY. The influence of the eradication of Helicobacter pylori on gastric ghrelin, appetite, and body mass index in patients with peptic ulcer disease.J Gastroenterol Hepatol. 2008;23 Suppl 2:S278-S285.
Nweneka CV, Prentice AM. Helicobacter pylori infection and circulating ghrelin levels - a systematic review.BMC Gastroenterol. 2011;11:7.
El-Omar EM, Oien K, El-Nujumi A, Gillen D, Wirz A, Dahill S, Williams C, Ardill JE, McColl KE. Helicobacter pylori infection and chronic gastric acid hyposecretion.Gastroenterology. 1997;113:15-24.
Kekki M, Samloff IM, Varis K, Ihamäki T. Serum pepsinogen I and serum gastrin in the screening of severe atrophic corpus gastritis.Scand J Gastroenterol Suppl. 1991;186:109-116.
Suto H, Yamazaki Y, Yoshida I, Yamakawa A, Ohtani M, Ito Y, Kuriyama M, Kato T, Azuma T. The effects of Helicobacter pylori eradication on body mass index and dyspeptic symptoms.Digestion. 2009;79:235-242.
Torisu T, Matsumoto T, Takata Y, Ansai T, Soh I, Awano S, Nakamichi I, Kagiyama S, Sonoki K, Yoshida A. Atrophic gastritis, but not antibody to Helicobacter pylori, is associated with body mass index in a Japanese population.J Gastroenterol. 2008;43:762-766.
Ando T, Mizuno S, Ishida T, Kondo Y, Miki I, Yoshida M, Azuma T, Ishikawa T, Takagi T, Yagi N. Plasma ghrelin isoforms and gastric ghrelin O-acyltransferase expression are influenced by Helicobacter pylori status.Nutrition. 2012;28:967-972.
Lane JA, Murray LJ, Harvey IM, Donovan JL, Nair P, Harvey RF. Randomised clinical trial: Helicobacter pylori eradication is associated with a significantly increased body mass index in a placebo-controlled study.Aliment Pharmacol Ther. 2011;33:922-929.
Fujiwara Y, Higuchi K, Arafa UA, Uchida T, Tominaga K, Watanabe T, Arakawa T. Long-term effect of Helicobacter pylori eradication on quality of life, body mass index, and newly developed diseases in Japanese patients with peptic ulcer disease.Hepatogastroenterology. 2002;49:1298-1302.
Yang YJ, Sheu BS, Yang HB, Lu CC, Chuang CC. Eradication of Helicobacter pylori increases childhood growth and serum acylated ghrelin levels.World J Gastroenterol. 2012;18:2674-2681.
Kawano S, Kawahara A, Nakai R, Fu HY, Tsuji S, Tsujii M. Helicobacter pylori infection does not affect serum leptin concentration and body mass index (BMI) in asymptomatic subjects.J Gastroenterol. 2001;36:579-580.
Danesh J, Peto R. Risk factors for coronary heart disease and infection with Helicobacter pylori: meta-analysis of 18 studies.BMJ. 1998;316:1130-1132.
Osawa H. Ghrelin and Helicobacter pylori infection.World J Gastroenterol. 2008;14:6327-6333.
Mechanick JI, Youdim A, Jones DB, Garvey WT, Hurley DL, McMahon MM, Heinberg LJ, Kushner R, Adams TD, Shikora S. Clinical practice guidelines for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient-2013 update: cosponsored by American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic & Bariatric Surgery.Obesity (Silver Spring). 2013;21 Suppl 1:S1-27.
Sauerland S, Angrisani L, Belachew M, Chevallier JM, Favretti F, Finer N, Fingerhut A, Garcia Caballero M, Guisado Macias JA, Mittermair R. Obesity surgery: evidence-based guidelines of the European Association for Endoscopic Surgery (EAES).Surg Endosc. 2005;19:200-221.
Schirmer B, Erenoglu C, Miller A. Flexible endoscopy in the management of patients undergoing Roux-en-Y gastric bypass.Obes Surg. 2002;12:634-638.
Verset D, Houben JJ, Gay F, Elcheroth J, Bourgeois V, Van Gossum A. The place of upper gastrointestinal tract endoscopy before and after vertical banded gastroplasty for morbid obesity.Dig Dis Sci. 1997;42:2333-2337.
Koppman JS, Poggi L, Szomstein S, Ukleja A, Botoman A, Rosenthal R. Esophageal motility disorders in the morbidly obese population.Surg Endosc. 2007;21:761-764.
Peterson HR, Rothschild M, Weinberg CR, Fell RD, McLeish KR, Pfeifer MA. Body fat and the activity of the autonomic nervous system.N Engl J Med. 1988;318:1077-1083.
Hong D, Kamath M, Wang S, Tabet J, Tougas G, Anvari M. Assessment of the afferent vagal nerve in patients with gastroesophageal reflux.Surg Endosc. 2002;16:1042-1045.
Abdullahi M, Annibale B, Capoccia D, Tari R, Lahner E, Osborn J, Leonetti F, Severi C. The eradication of Helicobacter pylori is affected by body mass index (BMI).Obes Surg. 2008;18:1450-1454.
Maddox A, Horowitz M, Wishart J, Collins P. Gastric and oesophageal emptying in obesity.Scand J Gastroenterol. 1989;24:593-598.
Cheymol G. Effects of obesity on pharmacokinetics implications for drug therapy.Clin Pharmacokinet. 2000;39:215-231.
Pai MP, Bearden DT. Antimicrobial dosing considerations in obese adult patients.Pharmacotherapy. 2007;27:1081-1091.
Zullo A, Severi C, Vannella L, Hassan C, Sbrozzi-Vanni A, Annibale B. Role of gastritis pattern on Helicobacter pylori eradication.Intern Emerg Med. 2012;7:517-522.
Cerqueira RM, Manso MC, Correia MR, Fernandes CD, Vilar H, Nora M, Martins P. Helicobacter pylori eradication therapy in obese patients undergoing gastric bypass surgery--fourteen days superior to seven days?Obes Surg. 2011;21:1377-1381.
Rasmussen JJ, Fuller W, Ali MR. Marginal ulceration after laparoscopic gastric bypass: an analysis of predisposing factors in 260 patients.Surg Endosc. 2007;21:1090-1094.
Yang CS, Lee WJ, Wang HH, Huang SP, Lin JT, Wu MS. The influence of Helicobacter pylori infection on the development of gastric ulcer in symptomatic patients after bariatric surgery.Obes Surg. 2006;16:735-739.
Loewen M, Giovanni J, Barba C. Screening endoscopy before bariatric surgery: a series of 448 patients.Surg Obes Relat Dis. 2008;4:709-712.
Albawardi A, Almarzooqi S, Torab FC. Helicobacter pylori in sleeve gastrectomies: prevalence and rate of complications.Int J Clin Exp Med. 2013;6:140-143.
Rawlins L, Rawlins MP, Brown CC, Schumacher DL. Effect of Helicobacter pylori on marginal ulcer and stomal stenosis after Roux-en-Y gastric bypass.Surg Obes Relat Dis. 2013;9:760-764.
Keren D, Matter I, Rainis T, Goldstein O, Stermer E, Lavy A. Sleeve gastrectomy leads to Helicobacter pylori eradication.Obes Surg. 2009;19:751-756.
Scheffel O, Daskalakis M, Weiner RA. Two important criteria for reducing the risk of postoperative ulcers at the gastrojejunostomy site after gastric bypass: patient compliance and type of gastric bypass.Obes Facts. 2011;4 Suppl 1:39-41.
Moayyedi P, Soo S, Deeks J, Forman D, Mason J, Innes M, Delaney B. Systematic review and economic evaluation of Helicobacter pylori eradication treatment for non-ulcer dyspepsia. Dyspepsia Review Group.BMJ. 2000;321:659-664.
Carabotti M, Silecchia G, Greco F, Leonetti F, Piretta L, Rengo M, Rizzello M, Osborn J, Corazziari E, Severi C. Impact of laparoscopic sleeve gastrectomy on upper gastrointestinal symptoms.Obes Surg. 2013;23:1551-1557.
Eslick GD, Lim LL, Byles JE, Xia HH, Talley NJ. Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis.Am J Gastroenterol. 1999;94:2373-2379.
Scozzari G, Trapani R, Toppino M, Morino M. Esophagogastric cancer after bariatric surgery: systematic review of the literature.Surg Obes Relat Dis. 2013;9:133-142.
Ericksen RE, Rose S, Westphalen CB, Shibata W, Muthupalani S, Tailor Y, Friedman RA, Han W, Fox JG, Ferrante AW Jr. Obesity accelerates Helicobacter felis-induced gastric carcinogenesis by enhancing immature myeloid cell trafficking and TH17 response.Gut. 2013;Epub ahead of print.