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Original Article |

Small Intestinal Bacterial Overgrowth in Patients With Lower Gastrointestinal Symptoms and a History of Previous Abdominal Surgery FREE

Patrizio Petrone, MD; Grant Sarkisyan, MD; Eileen Coloma, NP; Gabriel Akopian, MD; Adrian Ortega, MD; Howard S. Kaufman, MD, MBA
[+] Author Affiliations

Author Affiliations: Huntington Medical Research Institutes (Drs Petrone and Kaufman) and Huntington Memorial Hospital (Drs Petrone, Akopian, and Kaufman), Pasadena, California, and Division of Colorectal [[amp]] Pelvic Floor Surgery, Department of Surgery, University of Southern California Keck School of Medicine, Los Angeles (Drs Sarkisyan, Fern[[aacute]]ndez, Akopian, and Ortega, and Ms Coloma).


Arch Surg. 2011;146(4):444-447. doi:10.1001/archsurg.2011.55.
Text Size: A A A
Published online

Background  The small intestinal bacterial overgrowth (SIBO) breath test has had positive results in 84% of patients with irritable bowel syndrome vs 20% of controls. We hypothesized that SIBO would be more prevalent in patients with symptoms consistent with irritable bowel syndrome who have undergone previous abdominal surgery.

Objective  To identify causative factors for SIBO.

Design  Retrospective review.

Setting  Tertiary colorectal surgery clinic.

Main Outcome Measure  Result of SIBO breath test.

Results  We identified 77 patients whose differential diagnosis included SIBO from January 1, 2005, to December 31, 2007; 18 were excluded because of noncompliance with testing and 2 because of a decision to treat SIBO without formal testing. Symptoms were chronic abdominal pain in 30 patients (53%), bloating in 25 (44%), constipation in 37 (65%), and diarrhea in 7 (12%). Mean (SD) symptom duration was 45 (22) months. Of the 57 patients enrolled in this study, 45 (79%) tested positive for SIBO and 37 (82%) of those had a history of surgery, whereas 12 (21%) tested negative for SIBO and 9 (75%) of those had a history of surgery. Of the 36 SIBO-positive patients with a history of abdominal surgery (mean number of procedures, 2), the surgery locations were as follows: female reproductive organs, 23 (64%); hindgut, 15 (42%); foregut, 8 (22%); and midgut, 6 (17%). Open surgery alone was performed in 32 patients (56%) vs laparoscopic surgery in 7 (12%). Both open and laparoscopic procedures had been performed in 6 patients (11%). Four patients (7%) had a history of small intestinal obstruction. The mean age of SIBO-positive patients was higher than that of SIBO-negative patients (57 vs 44 years; P < .01). Analysis did not reveal any clinically significant independent factor associated with SIBO.

Conclusion  Physicians should consider SIBO in the differential diagnosis of patients with normal anatomic findings and chronic lower gastrointestinal complaints.

Figures in this Article

Symbiotic bacteria are normally compartmentalized to the distal gut, thanks to both the ileocecal valve and the normal interdigestive motility.1 When the ileocecal valve is compromised secondary to a medical disease (eg, celiac, Crohn's disease, or ulcerative colitis) or resection, bacteria normally resident in the colon can migrate to the proximal gut, which is sterile in healthy individuals.1

The upper limit of concentration of normal intestinal microflora is approximately 1 × 105 colony-forming units/mL of small intestinal aspirate.25 A higher concentration is defined as small intestinal bacterial overgrowth (SIBO)25 and implies an abnormal colonization of the upper gut as a consequence of a failure of defense mechanisms.6 The presence of adhesions after surgery may play a role in stasis and contribute to bacterial overgrowth.

The condition of SIBO has been associated with irritable bowel syndrome (IBS) and a variety of autonomic symptoms.4 The SIBO breath test relies on the conversion of lactulose to methane and/or hydrogen by bacteria in the small intestine (Figure 1), and results are often positive in patients with IBS. We hypothesized that SIBO would be more prevalent in patients with IBS-like symptoms who had undergone previous abdominal surgery.

Place holder to copy figure label and caption
Figure 1.

Excessive hydrogen and methane production revealed by breath test for small intestinal bacterial overgrowth.

Graphic Jump Location

After institutional review board approval, a tertiary colorectal surgery clinic database was used to retrospectively identify patients whose differential diagnosis included SIBO from January 1, 2005, to December 31, 2007. Patient data recorded included demographic characteristics, medical and surgical history, presenting symptoms, diagnostic evaluations including breath test, and treatment. Data from follow-up visits were also recorded. Patients who were SIBO positive were compared with SIBO-negative patients in a case-control fashion. Pediatric patients were not included in this study.

DATA ANALYSIS

Differences in means were assessed using the Wilcoxon rank-sum test. Differences in proportions were assessed using the χ2 test. Statistical significance was set at P < .05. Multiple regression analysis was performed to identify causative factors for SIBO. All statistical analysis was performed using SAS software, version 9.1 (SAS Institute, Inc, Cary, North Carolina).

ANTIBIOTIC TREATMENT

Patients with SIBO were treated with a 2-week course of antibiotics (rifaximin). Patients were reassessed after treatment.

During the 36-month period of this study (January 1, 2005, to December 31, 2007), a total of 77 patients who underwent the breath test for SIBO were identified at the Division of Colorectal & Pelvic Floor Surgery, Department of Surgery, University of Southern California University Hospital (Los Angeles). Of those 77 patients, 18 were excluded because of noncompliance with testing and 2 were excluded because of a decision to treat them for SIBO without formal testing.

Of the remaining 57 patients, 50 (88%) were female and 7 (12%) were male. The mean (SD) age was 54 (16) years (range, 17-91 years), and the mean (SD) weight was 151 (31) lb (range, 93-264 lb). Most (82%) of these patients were white; 14% were Hispanic.

The most common presenting symptoms were constipation in 37 patients (65%), chronic abdominal pain in 30 (53%), bloating in 25 (44%), and diarrhea in 7 (12%). The mean (SD) symptom duration was 45 (22) months.

Of the 57 patients enrolled in this study, 45 (79%) tested positive for SIBO and 37 (82%) of those had a history of surgery, whereas 12 (21%) tested negative for SIBO and 9 (75%) of those had a history of surgery (Figure 2). The mean age of SIBO-positive patients was higher than that of SIBO-negative patients (57 vs 44 years; P < .01). Symptoms resolved in 22 patients (49%) treated with gastrointestinal tract antibiotics.

Place holder to copy figure label and caption
Figure 2.

Comparison of groups by results of breath test for small intestinal bacterial overgrowth (SIBO).

Graphic Jump Location

Of the 36 SIBO-positive patients with a history of abdominal surgery (mean number of procedures, 2), the surgery locations were as follows: female reproductive organs, 23 (64%); hindgut, 15 (42%); foregut, 8 (22%); and midgut, 6 (17%). Open surgery alone was performed in 32 patients (56%) vs laparoscopic surgery in 7 (12%). Both open and laparoscopic procedures had been performed in 6 patients (11%). Four patients (7%) had a history of small intestinal obstruction.

Logistic regression analysis did not reveal any clinically significant independent factor associated with SIBO.

Two types of bacterial overgrowth can be differentiated: gastric overgrowth with upper respiratory tract microflora due to failure of the gastric acid barrier, mainly caused by Helicobacter pylori, and intestinal overgrowth due to failure of the intestinal clearance as a result of impaired intestinal peristalsis or anatomical abnormalities, caused by gram-negative bacilli.4 The distribution depends on the type of failure, and unless specified, the term bacterial overgrowth refers to SIBO.6

Endoscopy provides an accurate means to identify abnormalities of the gastrointestinal tract, but it is invasive and expensive and has risks of complications. Culture of intestinal contents is the ideal method for detecting bacterial overgrowth2,4 and allows identification of both types of bacterial overgrowth, but the labor and cost involved make its clinical use difficult.6 Furthermore, the problem with the direct approach is the access. Although bacterial overgrowth can occur only in the more distal portions of the small intestine, direct aspiration and culture are limited by the reach of the endoscope (approximately 60 cm). As a result, the detection of bacterial overgrowth by endoscopy is considerably less prevalent than such detection by breath tests.

With regard to indirect tests, the 13C- or 14C- d-xylose or lactulose breath test and the glucose, lactose, or lactulose hydrogen breath tests are available.6 The carbohydrate breath tests are used to diagnose carbohydrate malabsorption and to identify patients with SIBO7 in a simple, noninvasive, and less expensive way, and they can provide the desired information.

A variety of results have been used as a positive finding, including the presence of a “double peak,” the first peak corresponding to lactulose metabolized by small intestinal bacteria and the second peak corresponding to lactulose reaching the cecum.8,9 Saad and Chey7 assume that the presence of a common single peak can be either the result of fermentation in the small bowel, in the case of SIBO, or simply colonic fermentation, which can happen in patients with IBS and diarrhea who have accelerated ileocecal transit, resulting in a false-positive breath test.10

Lately, Lupascu et al11 and Nucera et al12 have shown an interest in the overlap of SIBO and IBS. Causes of IBS are still unknown, but it has been hypothesized that there is a dysregulation of visceral function and a strong association with emotional factors and stress.13 Specific intestinal microbes have been reported to contribute to the onset of IBS.1416

Small intestinal bacterial overgrowth is common in a colorectal surgery population presenting with lower gastrointestinal complaints. The clinical significance of SIBO is the chronic presence of pain, bloating, diarrhea, and malabsorption, similar to the symptoms seen in IBS patients17 and in the patient population of this study.

Previous studies in which the prevalence of SIBO in IBS patients was investigated gave contradictory results.1820 Different criteria for IBS and different breath tests may account for the discrepancies in the prevalence of SIBO.11

In a comprehensive study, Lupascu et al11 reported positive breath test results in 31% of IBS patients and 4% of healthy subjects. This difference was statistically significant, suggesting an epidemiologic association between SIBO and IBS. Recently, Lin21 reported that SIBO was found in 78% to 84% of patients with common symptoms of IBS.

With regard to the physiology of symptoms of SIBO and IBS, it has been proposed that in SIBO patients, there is an abnormal production of gases localized in the small intestine, which could explain the bloating and abdominal pain.22 Sugar malabsorption with increased carbohydrate fermentation, organic acid production, and bowel pH reduction may play a role in other symptoms, such as diarrhea.12

A known complication of SIBO, bacterial translocation,23 is the movement of gut bacteria from the lumen across the mucosal barrier,24 which can lead to the appearance of gut bacteria in the mesenteric lymph nodes and visceral organs, as demonstrated experimentally in rats.25 A potentially important consequence of the bacterial translocation is the immune response activation. Bacterial translocation and the production of lipopolysaccharide by gram-negative bacteria might explain the abnormal motility and visceral hypersensitivity present in the IBS patients2628 and could be related to other immune-mediated disorders, such as fibromyalgia, interstitial cystitis, and chronic fatigue syndrome.2932

In an attempt to reestablish the normal gut ecology, SIBO patients are often treated with cultures of beneficial species of enteric bacteria known as probiotics.1 However, this approach is limited because the number and distribution of species of the gut are still unknown.1 Among the strategies proposed for the normalization of symptoms are an elemental diet for 2 weeks,33 a 10-day course of traditional systemic antibiotics,34 and a 10-day course of nonabsorbable antibiotics. The success of these therapies ranges from 5% to 80%.1

Antibiotics can modulate the abnormal microflora. Rifaximin was the drug used in our study. This rifamycin derivative was effective in the treatment of SIBO35 because it has effects on intestinal anaerobic and facultative bacteria along the entire small intestine36 and is a poorly absorbed antibiotic.37

Although a history of abdominal and pelvic surgery in the patient population of this study was not associated with a statistically higher prevalence of SIBO, the prevalence of positive SIBO breath test results was greater than historical control rates. In our study, most (82%) patients who tested positive for SIBO had a history of surgery. The presence of adhesions as a result of surgical procedures and the potential for intestinal stasis may play an important role in the onset and maintenance of SIBO.

This study is limited by the retrospective design and the small number of subjects enrolled, and further study is needed to assess the risk of SIBO after abdominal and pelvic surgery. However, SIBO should be considered in the differential diagnosis of patients with normal anatomic findings and chronic lower gastrointestinal complaints.

Correspondence: Howard S. Kaufman, MD, MBA, Huntington Medical Research Institutes, 10 Pico St, Pasadena, CA 91105 (hkaufman@hmri.org).

Accepted for Publication: March 24, 2010.

Author Contributions: Drs Petrone and Kaufman had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Sarkisyan and Kaufman. Acquisition of data: Fernández, Coloma, Akopian, and Ortega. Analysis and interpretation of data: Petrone. Drafting of the manuscript: Petrone, Sarkisyan, Fernández, Coloma, Akopian, and Ortega. Critical revision of the manuscript for important intellectual content: Kaufman. Statistical analysis: Petrone and Kaufman. Study supervision: Petrone, Sarkisyan, Fernández, Coloma, Akopian, Ortega, and Kaufman.

Financial Disclosure: None reported.

Previous Presentation: The results of this study were presented at the 49th Annual Meeting of the Society for Surgery of the Alimentary Tract; May 20, 2008; San Diego, California.

Van Citters  GWLin  HC Management of small intestinal bacterial overgrowth. Curr Gastroenterol Rep 2005;7 (4) 317- 320
PubMed Link to Article
Simon  GLGorbach  SL Intestinal flora in health and disease. Gastroenterology 1984;86 (1) 174- 193
PubMed
Saltzman  JRKowdley  KVPedrosa  MC  et al.  Bacterial overgrowth without clinical malabsorption in elderly hypochlorhydric subjects. Gastroenterology 1994;106 (3) 615- 623
PubMed
King  CEToskes  PP Small intestine bacterial overgrowth. Gastroenterology 1979;76 (5, pt 1) 1035- 1055
PubMed
Clarke  RTJBeauchop  T Methods for studying gut microbes.  In: Clarke  RTJ, Beauchop  T, eds. Microbial Ecology of the Gut. London, England: Academic Press; 1997:1-33
Husebye  E The pathogenesis of gastrointestinal bacterial overgrowth. Chemotherapy 2005;51 (suppl 1) 1- 22
Link to Article
Saad  RJChey  WD Breath tests for gastrointestinal disease: the real deal or just a lot of hot air? Gastroenterology 2007;133 (6) 1763- 1766
PubMed Link to Article
Romagnuolo  JSchiller  DBailey  RJ Using breath tests wisely in a gastroenterology practice: an evidence-based review of indications and pitfalls in interpretation. Am J Gastroenterol 2002;97 (5) 1113- 1126
PubMed Link to Article
Simrén  MStotzer  PO Use and abuse of hydrogen breath tests. Gut 2006;55 (3) 297- 303
PubMed Link to Article
Hutchinson  RNotghi  ASmith  NBHarding  LKKumar  D Scintigraphic measurement of ileocaecal transit in irritable bowel syndrome and chronic idiopathic constipation. Gut 1995;36 (4) 585- 589
PubMed Link to Article
Lupascu  AGabrielli  MLauritano  EC  et al.  Hydrogen glucose breath test to detect small intestinal bacterial overgrowth: a prevalence case-control study in irritable bowel syndrome. Aliment Pharmacol Ther 2005;22 (11-12) 1157- 1160
PubMed Link to Article
Nucera  GGabrielli  MLupascu  A  et al.  Abnormal breath tests to lactose, fructose and sorbitol in irritable bowel syndrome may be explained by small intestinal bacterial overgrowth. Aliment Pharmacol Ther 2005;21 (11) 1391- 1395
PubMed Link to Article
Hunt  RH Evolving concepts in the pathophysiology of functional gastrointestinal disorders. J Clin Gastroenterol 2002;35 (1 suppl) S2- S6
Link to Article
Balsari  ACeccarelli  ADubini  FFesce  EPoli  G The fecal microbial population in the irritable bowel syndrome. Microbiologica 1982;5 (3) 185- 194
PubMed
King  TSElia  MHunter  JO Abnormal colonic fermentation in irritable bowel syndrome. Lancet 1998;352 (9135) 1187- 1189
PubMed Link to Article
Giacometti  ACirioni  OFiorentini  AFortuna  MScalise  G Irritable bowel syndrome in patients with Blastocystis hominis infection. Eur J Clin Microbiol Infect Dis 1999;18 (6) 436- 439
PubMed Link to Article
Singh  VVToskes  PP Small bowel bacterial overgrowth: presentation, diagnosis, and treatment. Curr Treat Options Gastroenterol 2004;7 (1) 19- 28
PubMed Link to Article
Kerlin  PWong  L Breath hydrogen testing in bacterial overgrowth of the small intestine. Gastroenterology 1988;95 (4) 982- 988
PubMed
Pimentel  MChow  EJLin  HC Eradication of small intestinal bacterial overgrowth reduces symptoms of irritable bowel syndrome. Am J Gastroenterol 2000;95 (11) 3503- 3506
PubMed Link to Article
Riordan  SM McIver  CJWalker  BMDuncombe  VMBolin  TDThomas  MC The lactulose breath hydrogen test and small intestinal bacterial overgrowth. Am J Gastroenterol 1996;91 (9) 1795- 1803
PubMed
Lin  HC Small intestinal bacterial overgrowth: a framework for understanding irritable bowel syndrome. JAMA 2004;292 (7) 852- 858
PubMed Link to Article
Harder  HSerra  JAzpiroz  FPassos  MCAguadé  SMalagelada  JR Intestinal gas distribution determines abdominal symptoms. Gut 2003;52 (12) 1708- 1713
PubMed Link to Article
Berg  RDGarlington  AW Translocation of certain indigenous bacteria from the gastrointestinal tract to the mesenteric lymph nodes and other organs in a gnotobiotic mouse model. Infect Immun 1979;23 (2) 403- 411
PubMed
Berg  RDWommack  EDeitch  EA Immunosuppression and intestinal bacterial overgrowth synergistically promote bacterial translocation. Arch Surg 1988;123 (11) 1359- 1364
PubMed Link to Article
Nieuwenhuijs  VBVerheem  Avan Duijvenbode-Beumer  H  et al.  The role of interdigestive small bowel motility in the regulation of gut microflora, bacterial overgrowth, and bacterial translocation in rats. Ann Surg 1998;228 (2) 188- 193
PubMed Link to Article
Wirthlin  DJCullen  JJSpates  ST  et al.  Gastrointestinal transit during endotoxemia: the role of nitric oxide. J Surg Res 1996;60 (2) 307- 311
PubMed Link to Article
Goyal  RKHirano  I The enteric nervous system. N Engl J Med 1996;334 (17) 1106- 1115
PubMed Link to Article
Ritchie  J Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 1973;14 (2) 125- 132
PubMed Link to Article
Aaron  LABuchwald  D A review of the evidence for overlap among unexplained clinical conditions. Ann Intern Med 2001;134 (9, pt 2) 868- 881
PubMed Link to Article
Veale  DKavanagh  GFielding  JFFitzgerald  O Primary fibromyalgia and the irritable bowel syndrome: different expressions of a common pathogenetic process. Br J Rheumatol 1991;30 (3) 220- 222
PubMed Link to Article
Sperber  ADAtzmon  YNeumann  L  et al.  Fibromyalgia in the irritable bowel syndrome: studies of prevalence and clinical implications. Am J Gastroenterol 1999;94 (12) 3541- 3546
PubMed Link to Article
Wein  AJHanno  PM Targets for therapy of the painful bladder. Urology 2002;59 (5 suppl 1) 68- 73
Link to Article
Pimentel  MConstantino  TKong  YBajwa  MRezaei  APark  S A 14-day elemental diet is highly effective in normalizing the lactulose breath test. Dig Dis Sci 2004;49 (1) 73- 77
PubMed Link to Article
Pimentel  MChow  EJLin  HC Normalization of lactulose breath testing correlates with symptom improvement in irritable bowel syndrome: a double-blind, randomized, placebo-controlled study. Am J Gastroenterol 2003;98 (2) 412- 419
PubMed
Scarpignato  CPelosini  I Rifaximin, a poorly absorbed antibiotic: pharmacology and clinical potential. Chemotherapy 2005;51(suppl 1)36- 66
PubMed Link to Article
Attar  AFlourié  BRambaud  JCFranchisseur  CRuszniewski  PBouhnik  Y Antibiotic efficacy in small intestinal bacterial overgrowth-related chronic diarrhea: a crossover, randomized trial. Gastroenterology 1999;117 (4) 794- 797
PubMed Link to Article
Di Stefano  MCorazza  GR Treatment of small intestine bacterial overgrowth and related symptoms by rifaximin. Chemotherapy 2005;51(suppl 1)103- 109
PubMed Link to Article

Figures

Place holder to copy figure label and caption
Figure 1.

Excessive hydrogen and methane production revealed by breath test for small intestinal bacterial overgrowth.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Comparison of groups by results of breath test for small intestinal bacterial overgrowth (SIBO).

Graphic Jump Location

Tables

References

Van Citters  GWLin  HC Management of small intestinal bacterial overgrowth. Curr Gastroenterol Rep 2005;7 (4) 317- 320
PubMed Link to Article
Simon  GLGorbach  SL Intestinal flora in health and disease. Gastroenterology 1984;86 (1) 174- 193
PubMed
Saltzman  JRKowdley  KVPedrosa  MC  et al.  Bacterial overgrowth without clinical malabsorption in elderly hypochlorhydric subjects. Gastroenterology 1994;106 (3) 615- 623
PubMed
King  CEToskes  PP Small intestine bacterial overgrowth. Gastroenterology 1979;76 (5, pt 1) 1035- 1055
PubMed
Clarke  RTJBeauchop  T Methods for studying gut microbes.  In: Clarke  RTJ, Beauchop  T, eds. Microbial Ecology of the Gut. London, England: Academic Press; 1997:1-33
Husebye  E The pathogenesis of gastrointestinal bacterial overgrowth. Chemotherapy 2005;51 (suppl 1) 1- 22
Link to Article
Saad  RJChey  WD Breath tests for gastrointestinal disease: the real deal or just a lot of hot air? Gastroenterology 2007;133 (6) 1763- 1766
PubMed Link to Article
Romagnuolo  JSchiller  DBailey  RJ Using breath tests wisely in a gastroenterology practice: an evidence-based review of indications and pitfalls in interpretation. Am J Gastroenterol 2002;97 (5) 1113- 1126
PubMed Link to Article
Simrén  MStotzer  PO Use and abuse of hydrogen breath tests. Gut 2006;55 (3) 297- 303
PubMed Link to Article
Hutchinson  RNotghi  ASmith  NBHarding  LKKumar  D Scintigraphic measurement of ileocaecal transit in irritable bowel syndrome and chronic idiopathic constipation. Gut 1995;36 (4) 585- 589
PubMed Link to Article
Lupascu  AGabrielli  MLauritano  EC  et al.  Hydrogen glucose breath test to detect small intestinal bacterial overgrowth: a prevalence case-control study in irritable bowel syndrome. Aliment Pharmacol Ther 2005;22 (11-12) 1157- 1160
PubMed Link to Article
Nucera  GGabrielli  MLupascu  A  et al.  Abnormal breath tests to lactose, fructose and sorbitol in irritable bowel syndrome may be explained by small intestinal bacterial overgrowth. Aliment Pharmacol Ther 2005;21 (11) 1391- 1395
PubMed Link to Article
Hunt  RH Evolving concepts in the pathophysiology of functional gastrointestinal disorders. J Clin Gastroenterol 2002;35 (1 suppl) S2- S6
Link to Article
Balsari  ACeccarelli  ADubini  FFesce  EPoli  G The fecal microbial population in the irritable bowel syndrome. Microbiologica 1982;5 (3) 185- 194
PubMed
King  TSElia  MHunter  JO Abnormal colonic fermentation in irritable bowel syndrome. Lancet 1998;352 (9135) 1187- 1189
PubMed Link to Article
Giacometti  ACirioni  OFiorentini  AFortuna  MScalise  G Irritable bowel syndrome in patients with Blastocystis hominis infection. Eur J Clin Microbiol Infect Dis 1999;18 (6) 436- 439
PubMed Link to Article
Singh  VVToskes  PP Small bowel bacterial overgrowth: presentation, diagnosis, and treatment. Curr Treat Options Gastroenterol 2004;7 (1) 19- 28
PubMed Link to Article
Kerlin  PWong  L Breath hydrogen testing in bacterial overgrowth of the small intestine. Gastroenterology 1988;95 (4) 982- 988
PubMed
Pimentel  MChow  EJLin  HC Eradication of small intestinal bacterial overgrowth reduces symptoms of irritable bowel syndrome. Am J Gastroenterol 2000;95 (11) 3503- 3506
PubMed Link to Article
Riordan  SM McIver  CJWalker  BMDuncombe  VMBolin  TDThomas  MC The lactulose breath hydrogen test and small intestinal bacterial overgrowth. Am J Gastroenterol 1996;91 (9) 1795- 1803
PubMed
Lin  HC Small intestinal bacterial overgrowth: a framework for understanding irritable bowel syndrome. JAMA 2004;292 (7) 852- 858
PubMed Link to Article
Harder  HSerra  JAzpiroz  FPassos  MCAguadé  SMalagelada  JR Intestinal gas distribution determines abdominal symptoms. Gut 2003;52 (12) 1708- 1713
PubMed Link to Article
Berg  RDGarlington  AW Translocation of certain indigenous bacteria from the gastrointestinal tract to the mesenteric lymph nodes and other organs in a gnotobiotic mouse model. Infect Immun 1979;23 (2) 403- 411
PubMed
Berg  RDWommack  EDeitch  EA Immunosuppression and intestinal bacterial overgrowth synergistically promote bacterial translocation. Arch Surg 1988;123 (11) 1359- 1364
PubMed Link to Article
Nieuwenhuijs  VBVerheem  Avan Duijvenbode-Beumer  H  et al.  The role of interdigestive small bowel motility in the regulation of gut microflora, bacterial overgrowth, and bacterial translocation in rats. Ann Surg 1998;228 (2) 188- 193
PubMed Link to Article
Wirthlin  DJCullen  JJSpates  ST  et al.  Gastrointestinal transit during endotoxemia: the role of nitric oxide. J Surg Res 1996;60 (2) 307- 311
PubMed Link to Article
Goyal  RKHirano  I The enteric nervous system. N Engl J Med 1996;334 (17) 1106- 1115
PubMed Link to Article
Ritchie  J Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 1973;14 (2) 125- 132
PubMed Link to Article
Aaron  LABuchwald  D A review of the evidence for overlap among unexplained clinical conditions. Ann Intern Med 2001;134 (9, pt 2) 868- 881
PubMed Link to Article
Veale  DKavanagh  GFielding  JFFitzgerald  O Primary fibromyalgia and the irritable bowel syndrome: different expressions of a common pathogenetic process. Br J Rheumatol 1991;30 (3) 220- 222
PubMed Link to Article
Sperber  ADAtzmon  YNeumann  L  et al.  Fibromyalgia in the irritable bowel syndrome: studies of prevalence and clinical implications. Am J Gastroenterol 1999;94 (12) 3541- 3546
PubMed Link to Article
Wein  AJHanno  PM Targets for therapy of the painful bladder. Urology 2002;59 (5 suppl 1) 68- 73
Link to Article
Pimentel  MConstantino  TKong  YBajwa  MRezaei  APark  S A 14-day elemental diet is highly effective in normalizing the lactulose breath test. Dig Dis Sci 2004;49 (1) 73- 77
PubMed Link to Article
Pimentel  MChow  EJLin  HC Normalization of lactulose breath testing correlates with symptom improvement in irritable bowel syndrome: a double-blind, randomized, placebo-controlled study. Am J Gastroenterol 2003;98 (2) 412- 419
PubMed
Scarpignato  CPelosini  I Rifaximin, a poorly absorbed antibiotic: pharmacology and clinical potential. Chemotherapy 2005;51(suppl 1)36- 66
PubMed Link to Article
Attar  AFlourié  BRambaud  JCFranchisseur  CRuszniewski  PBouhnik  Y Antibiotic efficacy in small intestinal bacterial overgrowth-related chronic diarrhea: a crossover, randomized trial. Gastroenterology 1999;117 (4) 794- 797
PubMed Link to Article
Di Stefano  MCorazza  GR Treatment of small intestine bacterial overgrowth and related symptoms by rifaximin. Chemotherapy 2005;51(suppl 1)103- 109
PubMed Link to Article

Correspondence

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For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.
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