Skip to main content
Top
Published in: Digestive Diseases and Sciences 4/2018

01-04-2018 | Original Article

Stool PCR for Gastrointestinal Pathogens in Patients With and Without Immune-Mediated Intestinal Diseases

Authors: Yael R. Nobel, Jordan Axelrad, Suzanne K. Lewis, Susan Whittier, Garrett Lawlor, Simon Lichtiger, Peter H. R. Green, Benjamin Lebwohl

Published in: Digestive Diseases and Sciences | Issue 4/2018

Login to get access

Abstract

Background

Patients with celiac disease and inflammatory bowel disease, two immune-mediated luminal conditions, have higher rates of certain infections than healthy counterparts. The prevalence of many gastrointestinal infections in these patients, however, is unknown.

Aims

Using a novel clinical stool pathogen PCR test, we investigated the hypothesis that patients with celiac disease/inflammatory bowel disease had different distributions of diarrheal pathogens than other patients.

Methods

We performed a retrospective cohort study of outpatients who underwent stool pathogen testing with the FilmArray Gastrointestinal PCR Panel (BioFire Diagnostics, Salt Lake City, UT) at our institution from January 1 to December 31, 2015. Rates of pathogens were measured in patients with or without celiac disease/inflammatory bowel disease.

Results

Of 955 patients, 337 had positive test for any pathogen, with 465 bacterial, parasitic, or viral pathogens identified. One hundred and twenty-seven patients (13.3%) had celiac disease or inflammatory bowel disease, of which 29/127 (22.8%) had a positive test, compared to 308/828 other patients (37.2%) (p = 0.002). Patients with celiac disease/inflammatory bowel disease had significantly fewer viruses (1.6 vs. 8.1% of patients; p = 0.008) and parasites (0 vs. 3.3%; p = 0.039), with nonsignificant trend toward fewer bacteria (21.3 vs. 29.2%; p = 0.063). Escherichia coli species were most common in both populations.

Conclusions

Stool PCR identified numerous pathogens in patients with or without celiac disease/inflammatory bowel disease. Patients with celiac disease/inflammatory bowel disease were significantly less likely to have any pathogen identified, and had significantly fewer viruses and parasites. In this population, knowledge of common pathogens can guide diagnostic evaluation and offer opportunities for treatment.
Literature
1.
go back to reference Ludvigsson JF, Wahlstrom J, Grunewald J, Ekbom A, Montgomery SM. Coeliac disease and risk of tuberculosis: a population based cohort study. Thorax. 2007;62:23–28.CrossRefPubMedPubMedCentral Ludvigsson JF, Wahlstrom J, Grunewald J, Ekbom A, Montgomery SM. Coeliac disease and risk of tuberculosis: a population based cohort study. Thorax. 2007;62:23–28.CrossRefPubMedPubMedCentral
2.
go back to reference Peters U, Askling J, Gridley G, Ekbom A, Linet M. Causes of death in patients with celiac disease in a population-based swedish cohort. Arch Intern Med. 2003;163:1566–1572.CrossRefPubMed Peters U, Askling J, Gridley G, Ekbom A, Linet M. Causes of death in patients with celiac disease in a population-based swedish cohort. Arch Intern Med. 2003;163:1566–1572.CrossRefPubMed
3.
go back to reference Thomas HJ, Wotton CJ, Yeates D, Ahmad T, Jewell DP, Goldacre MJ. Pneumococcal infection in patients with coeliac disease. Eur J Gastroenterol Hepatol. 2008;20:624–628.CrossRefPubMed Thomas HJ, Wotton CJ, Yeates D, Ahmad T, Jewell DP, Goldacre MJ. Pneumococcal infection in patients with coeliac disease. Eur J Gastroenterol Hepatol. 2008;20:624–628.CrossRefPubMed
4.
go back to reference Marild K, Fredlund H, Ludvigsson JF. Increased risk of hospital admission for influenza in patients with celiac disease: a nationwide cohort study in Sweden. Am J Gastroenterol. 2010;105:2465–2473.CrossRefPubMed Marild K, Fredlund H, Ludvigsson JF. Increased risk of hospital admission for influenza in patients with celiac disease: a nationwide cohort study in Sweden. Am J Gastroenterol. 2010;105:2465–2473.CrossRefPubMed
5.
go back to reference Lawson PA, Citron DM, Tyrrell KL, Finegold SM. Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O’Toole 1935) Prevot 1938. Anaerobe. 2016;40:95–99.CrossRefPubMed Lawson PA, Citron DM, Tyrrell KL, Finegold SM. Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O’Toole 1935) Prevot 1938. Anaerobe. 2016;40:95–99.CrossRefPubMed
6.
go back to reference Nguyen GC, Kaplan GG, Harris ML, Brant SR. A national survey of the prevalence and impact of Clostridium difficile infection among hospitalized inflammatory bowel disease patients. Am J Gastroenterol. 2008;103:1443–1450.CrossRefPubMed Nguyen GC, Kaplan GG, Harris ML, Brant SR. A national survey of the prevalence and impact of Clostridium difficile infection among hospitalized inflammatory bowel disease patients. Am J Gastroenterol. 2008;103:1443–1450.CrossRefPubMed
7.
go back to reference Saidel-Odes L, Borer A, Odes S. Clostridium difficile infection in patients with inflammatory bowel disease. Ann Gastroenterol. 2011;24:263–270.PubMedPubMedCentral Saidel-Odes L, Borer A, Odes S. Clostridium difficile infection in patients with inflammatory bowel disease. Ann Gastroenterol. 2011;24:263–270.PubMedPubMedCentral
8.
go back to reference Pascarella F, Martinelli M, Miele E, Del Pezzo M, Roscetto E, Staiano A. The impact of Clostridium difficile infection on pediatric inflammatory bowel disease. J Pediatr. 2009;154:854–858.CrossRefPubMed Pascarella F, Martinelli M, Miele E, Del Pezzo M, Roscetto E, Staiano A. The impact of Clostridium difficile infection on pediatric inflammatory bowel disease. J Pediatr. 2009;154:854–858.CrossRefPubMed
9.
go back to reference Khare R, Espy MJ, Cebelinski E, et al. Comparative evaluation of two commercial multiplex panels for detection of gastrointestinal pathogens by use of clinical stool specimens. J Clin Microbiol. 2014;52:3667–3673.CrossRefPubMedPubMedCentral Khare R, Espy MJ, Cebelinski E, et al. Comparative evaluation of two commercial multiplex panels for detection of gastrointestinal pathogens by use of clinical stool specimens. J Clin Microbiol. 2014;52:3667–3673.CrossRefPubMedPubMedCentral
10.
go back to reference Buss SN, Leber A, Chapin K, et al. Multicenter evaluation of the BioFire FilmArray gastrointestinal panel for etiologic diagnosis of infectious gastroenteritis. J Clin Microbiol. 2015;53:915–925.CrossRefPubMedPubMedCentral Buss SN, Leber A, Chapin K, et al. Multicenter evaluation of the BioFire FilmArray gastrointestinal panel for etiologic diagnosis of infectious gastroenteritis. J Clin Microbiol. 2015;53:915–925.CrossRefPubMedPubMedCentral
11.
go back to reference Ananthakrishnan AN, McGinley EL, Binion DG. Excess hospitalisation burden associated with Clostridium difficile in patients with inflammatory bowel disease. Gut. 2008;57:205–210.CrossRefPubMed Ananthakrishnan AN, McGinley EL, Binion DG. Excess hospitalisation burden associated with Clostridium difficile in patients with inflammatory bowel disease. Gut. 2008;57:205–210.CrossRefPubMed
12.
go back to reference Lebwohl B, Nobel YR, Green PHR, Blaser MJ, Ludvigsson JF. Risk of Clostridium difficile infection in patients with celiac disease: a population-based study. Am J Gastroenterol. 2017;112:1878–1884.CrossRefPubMed Lebwohl B, Nobel YR, Green PHR, Blaser MJ, Ludvigsson JF. Risk of Clostridium difficile infection in patients with celiac disease: a population-based study. Am J Gastroenterol. 2017;112:1878–1884.CrossRefPubMed
13.
go back to reference Al-Toma A, Goerres MS, Meijer JW, Pena AS, Crusius JB, Mulder CJ. Human leukocyte antigen-DQ2 homozygosity and the development of refractory celiac disease and enteropathy-associated T-cell lymphoma. Clin Gastroenterol Hepatol. 2006;4:315–319.CrossRefPubMed Al-Toma A, Goerres MS, Meijer JW, Pena AS, Crusius JB, Mulder CJ. Human leukocyte antigen-DQ2 homozygosity and the development of refractory celiac disease and enteropathy-associated T-cell lymphoma. Clin Gastroenterol Hepatol. 2006;4:315–319.CrossRefPubMed
14.
go back to reference Rieck M, Arechiga A, Onengut-Gumuscu S, Greenbaum C, Concannon P, Buckner JH. Genetic variation in PTPN22 corresponds to altered function of T and B lymphocytes. J Immunol. 2007;179:4704–4710.CrossRefPubMed Rieck M, Arechiga A, Onengut-Gumuscu S, Greenbaum C, Concannon P, Buckner JH. Genetic variation in PTPN22 corresponds to altered function of T and B lymphocytes. J Immunol. 2007;179:4704–4710.CrossRefPubMed
15.
go back to reference Jarry A, Malard F, Bou-Hanna C, et al. Interferon-alpha promotes Th1 response and epithelial apoptosis via inflammasome activation in human intestinal mucosa. Cell Mol Gastroenterol Hepatol. 2016;3:72–81.CrossRefPubMedPubMedCentral Jarry A, Malard F, Bou-Hanna C, et al. Interferon-alpha promotes Th1 response and epithelial apoptosis via inflammasome activation in human intestinal mucosa. Cell Mol Gastroenterol Hepatol. 2016;3:72–81.CrossRefPubMedPubMedCentral
16.
go back to reference Park SD, Markowitz J, Pettei M, et al. Failure to respond to hepatitis B vaccine in children with celiac disease. Pediatr Gastroenterol Nutr.. 2007;44:431–435.CrossRef Park SD, Markowitz J, Pettei M, et al. Failure to respond to hepatitis B vaccine in children with celiac disease. Pediatr Gastroenterol Nutr.. 2007;44:431–435.CrossRef
17.
go back to reference Nemes É, Lefler É, Szegedi L, et al. Gluten intake interferes with the humoral immune response to recombinant hepatitis B vaccine in patients with celiac disease. Pediatrics. 2008;121:e1570–e1576.CrossRefPubMed Nemes É, Lefler É, Szegedi L, et al. Gluten intake interferes with the humoral immune response to recombinant hepatitis B vaccine in patients with celiac disease. Pediatrics. 2008;121:e1570–e1576.CrossRefPubMed
18.
go back to reference Noh KW, Poland GA, Murray JA. Hepatitis B vaccine nonresponse and celiac disease. Am J Gastroenterol. 2003;98:2289–2292.CrossRefPubMed Noh KW, Poland GA, Murray JA. Hepatitis B vaccine nonresponse and celiac disease. Am J Gastroenterol. 2003;98:2289–2292.CrossRefPubMed
19.
go back to reference Di Sabatino A, Rosado MM, Cazzola P, et al. Splenic hypofunction and the spectrum of autoimmune and malignant complications in celiac disease. Clin Gastroenterol Hepatol. 2006;4:179–186.CrossRefPubMed Di Sabatino A, Rosado MM, Cazzola P, et al. Splenic hypofunction and the spectrum of autoimmune and malignant complications in celiac disease. Clin Gastroenterol Hepatol. 2006;4:179–186.CrossRefPubMed
20.
go back to reference Girbovan A, Sur G, Samasca G, Lupan I. Dysbiosis a risk factor for celiac disease. Med Microbiol Immunol. 2017;206:83–91.CrossRefPubMed Girbovan A, Sur G, Samasca G, Lupan I. Dysbiosis a risk factor for celiac disease. Med Microbiol Immunol. 2017;206:83–91.CrossRefPubMed
21.
go back to reference Wlodarska M, Kostic AD, Xavier RJ. An integrative view of microbiome-host interactions in inflammatory bowel disease. Cell Host Microbe. 2015;17:577–591.CrossRefPubMedPubMedCentral Wlodarska M, Kostic AD, Xavier RJ. An integrative view of microbiome-host interactions in inflammatory bowel disease. Cell Host Microbe. 2015;17:577–591.CrossRefPubMedPubMedCentral
22.
go back to reference Fyderek K, Strus M, Kowalsa-Duplaga K, et al. Mucosal bacterial microflora and mucus later thickness in adolescents with inflammatory bowel disease. World J Gastroenterol. 2009;15:5287–5294.CrossRefPubMedPubMedCentral Fyderek K, Strus M, Kowalsa-Duplaga K, et al. Mucosal bacterial microflora and mucus later thickness in adolescents with inflammatory bowel disease. World J Gastroenterol. 2009;15:5287–5294.CrossRefPubMedPubMedCentral
Metadata
Title
Stool PCR for Gastrointestinal Pathogens in Patients With and Without Immune-Mediated Intestinal Diseases
Authors
Yael R. Nobel
Jordan Axelrad
Suzanne K. Lewis
Susan Whittier
Garrett Lawlor
Simon Lichtiger
Peter H. R. Green
Benjamin Lebwohl
Publication date
01-04-2018
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 4/2018
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-018-4959-x

Other articles of this Issue 4/2018

Digestive Diseases and Sciences 4/2018 Go to the issue