Prevalence, Risk Factors, and Outcomes of Irritable Bowel Syndrome After Infectious Enteritis: A Systematic Review and Meta-analysis

Fabiane Klem, Akhilesh Wadhwa, Larry J Prokop, Wendy J Sundt, Gianrico Farrugia, Michael Camilleri, Siddharth Singh, Madhusudan Grover, Fabiane Klem, Akhilesh Wadhwa, Larry J Prokop, Wendy J Sundt, Gianrico Farrugia, Michael Camilleri, Siddharth Singh, Madhusudan Grover

Abstract

Background & aims: Foodborne illness affects 15% of the US population each year, and is a risk factor for irritable bowel syndrome (IBS). We evaluated risk of, risk factors for, and outcomes of IBS after infectious enteritis.

Methods: We performed a systematic review of electronic databases from 1994 through August 31, 2015 to identify cohort studies of the prevalence of IBS 3 months or more after infectious enteritis. We used random-effects meta-analysis to calculate the summary point prevalence of IBS after infectious enteritis, as well as relative risk (compared with individuals without infectious enteritis) and host- and enteritis-related risk factors.

Results: We identified 45 studies, comprising 21,421 individuals with enteritis, followed for 3 months to 10 years for development of IBS. The pooled prevalence of IBS at 12 months after infectious enteritis was 10.1% (95% confidence interval [CI], 7.2-14.1) and at more than 12 months after infectious enteritis was 14.5% (95% CI, 7.7-25.5). Risk of IBS was 4.2-fold higher in patients who had infectious enteritis in the past 12 months than in those who had not (95% CI, 3.1-5.7); risk of IBS was 2.3-fold higher in individuals who had infectious enteritis more than 12 months ago than in individuals who had not (95% CI, 1.8-3.0). Of patients with enteritis caused by protozoa or parasites, 41.9% developed IBS, and of patients with enteritis caused by bacterial infection, 13.8% developed IBS. Risk of IBS was significantly increased in women (odds ratio [OR], 2.2; 95% CI, 1.6-3.1) and individuals with antibiotic exposure (OR, 1.7; 95% CI, 1.2-2.4), anxiety (OR, 2; 95% CI, 1.3-2.9), depression (OR, 1.5; 95% CI, 1.2-1.9), somatization (OR, 4.1; 95% CI, 2.7-6.0), neuroticism (OR, 3.3; 95% CI, 1.6-6.5), and clinical indicators of enteritis severity. There was a considerable level of heterogeneity among studies.

Conclusions: In a systematic review and meta-analysis, we found >10% of patients with infectious enteritis develop IBS later; risk of IBS was 4-fold higher than in individuals who did not have infectious enteritis, although there was heterogeneity among studies analyzed. Women-particularly those with severe enteritis-are at increased risk for developing IBS, as are individuals with psychological distress and users of antibiotics during the enteritis.

Keywords: Functional Gastrointestinal Disorders; Gastrointestinal Infections; Microbes; Post-Infectious Irritable Bowel Syndrome.

Conflict of interest statement

Conflicts of interest: None to declare for any authors.

Copyright © 2017 AGA Institute. Published by Elsevier Inc. All rights reserved.

Figures

Figure 1
Figure 1
Study selection flow-diagram
Figure 2
Figure 2
Summary point prevalence of PI-IBS with bacterial, protozoal/parasitic and viral infectious enteritis. Considerable heterogeneity (I2>95%) was observed for all analyses.
Figure 3
Figure 3
Pooled odds ratio for host- and infectious enteritis-episode related risk factors for PI-IBS development. Moderate to considerable heterogeneity was observed for most estimates (I2 values for abdominal pain = 86%, antibiotic exposure = 32%, anxiety = 90%, bloody stool = 65%, depression = 48%, duration of initial enteritis >7 days = 86%, female sex = 72%, fever at time of enteritis = 69%, neuroticism – 0%, somatization = 0%, smoking = 8%, weight loss = 75%).

References

    1. Chey WD, Kurlander J, Eswaran S. Irritable bowel syndrome: a clinical review. JAMA. 2015;313:949–958.
    1. Spiller R, Garsed K. Postinfectious irritable bowel syndrome. Gastroenterology. 2009;136:1979–1988.
    1. Chaudhary NA, Truelove SC. The irritable colon syndrome. A study of the clinical features, predisposing causes, and prognosis in 130 cases. Q J Med. 1962;31:307–322.
    1. Neal KR, Hebden J, Spiller R. Prevalence of gastrointestinal symptoms six months after bacterial gastroenteritis and risk factors for development of the irritable bowel syndrome: postal survey of patients. BMJ. 1997;314:779–782.
    1. Gwee KA, Leong YL, Graham C, et al. The role of psychological and biological factors in postinfective gut dysfunction. Gut. 1999;44:400–406.
    1. Thabane M, Kottachchi DT, Marshall JK. Systematic review and meta-analysis: The incidence and prognosis of post-infectious irritable bowel syndrome. Aliment Pharmacol Ther. 2007;26:535–544.
    1. Porter CK, Faix DJ, Shiau D, et al. Postinfectious gastrointestinal disorders following norovirus outbreaks. Clin Infect Dis. 2012;55:915–922.
    1. Zanini B, Ricci C, Bandera F, et al. Incidence of post-infectious irritable bowel syndrome and functional intestinal disorders following a water-borne viral gastroenteritis outbreak. Am J Gastroenterol. 2012;107:891–899.
    1. Saps M, Pensabene L, Turco R, et al. Rotavirus gastroenteritis: precursor of functional gastrointestinal disorders? J Pediatr Gastroenterol Nutr. 2009;49:580–583.
    1. Marshall JK, Thabane M, Borgaonkar MR, et al. Postinfectious irritable bowel syndrome after a food-borne outbreak of acute gastroenteritis attributed to a viral pathogen. Clin Gastroenterol Hepatol. 2007;5:457–460.
    1. Hanevik K, Dizdar V, Langeland N, et al. Development of functional gastrointestinal disorders after Giardia lamblia infection. BMC Gastroenterol. 2009;9:27.
    1. Hanevik K, Wensaas KA, Rortveit G, et al. Irritable bowel syndrome and chronic fatigue 6 years after giardia infection: a controlled prospective cohort study. Clin Infect Dis. 2014;59:1394–1400.
    1. Wensaas KA, Langeland N, Hanevik K, et al. Irritable bowel syndrome and chronic fatigue 3 years after acute giardiasis: historic cohort study. Gut. 2012;61:214–219.
    1. Marshall JK, Thabane M, Garg AX, et al. Eight year prognosis of postinfectious irritable bowel syndrome following waterborne bacterial dysentery. Gut. 2010;59:605–611.
    1. Schwille-Kiuntke J, Enck P, Zendler C, et al. Postinfectious irritable bowel syndrome: follow-up of a patient cohort of confirmed cases of bacterial infection with Salmonella or Campylobacter. Neurogastroenterol Motil. 2011;23:e479–e488.
    1. Rodriguez LA, Ruigomez A. Increased risk of irritable bowel syndrome after bacterial gastroenteritis: cohort study. BMJ. 1999;318:565–566.
    1. Ruigomez A, Garcia Rodriguez LA, Panes J. Risk of irritable bowel syndrome after an episode of bacterial gastroenteritis in general practice: influence of comorbidities. Clin Gastroenterol Hepatol. 2007;5:465–469.
    1. Center for Disease Control and Prevention. Estimates of foodborne illness in the United States. [Accessed November 18, 2016];
    1. Schwille-Kiuntke J, Mazurak N, Enck P. Systematic review with meta-analysis: post-infectious irritable bowel syndrome after travellers' diarrhoea. Aliment Pharmacol Ther. 2015;41:1029–1037.
    1. Marshall JK, Thabane M, Garg AX, et al. Incidence and epidemiology of irritable bowel syndrome after a large waterborne outbreak of bacterial dysentery. Gastroenterology. 2006;131:445–450.
    1. Garg AX, Marshall J, Salvadori M, et al. A gradient of acute gastroenteritis was characterized, to assess risk of long-term health sequelae after drinking bacterial-contaminated water. J Clin Epidemiol. 2006;59:421–428.
    1. Thabane M, Simunovic M, Akhtar-Danesh N, et al. Development and validation of a risk score for post-infectious irritable bowel syndrome. Am J Gastroenterol. 2009;104:2267–2274.
    1. Pitzurra R, Fried M, Rogler G, et al. Irritable bowel syndrome among a cohort of European travelers to resource-limited destinations. J Travel Med. 2011;18:250–256.
    1. Shea BJ, Hamel C, Wells GA, et al. AMSTAR is a reliable and valid measurement tool to assess the methodological quality of systematic reviews. J Clin Epidemiol. 2009;62:1013–1020.
    1. Wells G, Shea BJ, O'Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. .
    1. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–188.
    1. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–560.
    1. Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634.
    1. Schwille-Kiuntke J, Enck P, Polster AV, et al. Postinfectious irritable bowel syndrome after travelers' diarrhea--a cohort study. Neurogastroenterol Motil. 2015;27:1147–1155.
    1. Pensabene L, Talarico V, Concolino D, et al. Postinfectious functional gastrointestinal disorders in children: a multicenter prospective study. J Pediatr. 2015;166:903–907.
    1. Nielsen HL, Engberg J, Ejlertsen T, et al. Psychometric scores and persistence of irritable bowel after Campylobacter concisus infection. Scand J Gastroenterol. 2014;49:545–551.
    1. Nair P, Okhuysen PC, Jiang ZD, et al. Persistent abdominal symptoms in US adults after short-term stay in Mexico. J Travel Med. 2014;21:153–158.
    1. Kowalcyk BK, Smeets HM, Succop PA, et al. Relative risk of irritable bowel syndrome following acute gastroenteritis and associated risk factors. Epidemiol Infect. 2014;142:1259–1268.
    1. Cremon C, Stanghellini V, Pallotti F, et al. Salmonella gastroenteritis during childhood is a risk factor for irritable bowel syndrome in adulthood. Gastroenterology. 2014;147:69–77.
    1. Bettes N, Griffith J, Camilleri M, et al. Risk and predictors of post-infectious irritable bowel syndrome among community-acquired cases of bacterial enteritis. Gastroenterology. 2014;146:S-538.
    1. Lalani T, Tribble D, Ganesan A, et al. Travelers' diarrhea risk factors and incidence of postinfectious irritable bowel syndrome (PI-IBS) in a large prospective cohort of Department of Defense beneficiaries (TRAVMIL) Am J Trop Hyg. 2012;89:223.
    1. Van Wanrooij S, Wouters M, Mondelaers S, et al. Postinfectious irritable bowel syndrome and functional dyspepsia following an outbreak of tap water contamination. Gastroenterology. 2013;144:S536–S537.
    1. Youn Y, Park S, Park C, et al. The clinical course of postinfectious irritable bowel syndrome (IBS) after shigellosis: A 10-year follow-up study. Neurogastroenterol Motil. 2012;24:102.
    1. Koh SJ, Lee DH, Lee SH, et al. Incidence and risk factors of irritable bowel syndrome in community subjects with culture-proven bacterial gastroenteritis. Korean J Gastroenterol. 2012;60:13–18.
    1. Thabane M, Simunovic M, Akhtar-Danesh N, et al. An outbreak of acute bacterial gastroenteritis is associated with an increased incidence of irritable bowel syndrome in children. Am J Gastroenterol. 2010;105:933–939.
    1. Lim H, Kim H, Youn Y, et al. The clinical course of post-infectious irritable bowel syndrome: an eight-year follow-up study. Gastroenterology. 2010;138:S623.
    1. Jung IS, Kim HS, Park H, et al. The clinical course of postinfectious irritable bowel syndrome: a five-year follow-up study. J Clin Gastroenterol. 2009;43:534–540.
    1. Saps M, Pensabene L, Di Martino L, et al. Post-infectious functional gastrointestinal disorders in children. J Pediatr. 2008;152:812–816. 816.
    1. Spence MJ, Moss-Morris R. The cognitive behavioural model of irritable bowel syndrome: a prospective investigation of patients with gastroenteritis. Gut. 2007;56:1066–1071.
    1. Tornblom H, Holmvall P, Svenungsson B, et al. Gastrointestinal symptoms after infectious diarrhea: a five-year follow-up in a Swedish cohort of adults. Clin Gastroenterol Hepatol. 2007;5:461–464.
    1. Soyturk M, Akpinar H, Gurler O, et al. Irritable bowel syndrome in persons who acquired trichinellosis. Am J Gastroenterol. 2007;102:1064–1069.
    1. Piche T, Vanbiervliet G, Pipau FG, et al. Low risk of irritable bowel syndrome after Clostridium difficile infection. Can J Gastroenterol. 2007;21:727–731.
    1. Cumberland P, Sethi D, Roderick PJ, et al. The infectious intestinal disease study of England: a prospective evaluation of symptoms and health care use after an acute episode. Epidemiol Infect. 2003;130:453–460.
    1. Ilnyckyj A, Balachandra B, Elliott L, et al. Post-traveler's diarrhea irritable bowel syndrome: a prospective study. Am J Gastroenterol. 2003;98:596–599.
    1. Ji S, Park H, Lee D, et al. Post-infectious irritable bowel syndrome in patients with Shigella infection. J Gastroenterol Hepatol. 2005;20:381–386.
    1. Mearin F, Perez-Oliveras M, Perello A, et al. Dyspepsia and irritable bowel syndrome after a Salmonella gastroenteritis outbreak: one-year follow-up cohort study. Gastroenterology. 2005;129:98–104.
    1. Okhuysen PC, Jiang ZD, Carlin L, et al. Post-diarrhea chronic intestinal symptoms and irritable bowel syndrome in North American travelers to Mexico. Am J Gastroenterol. 2004;99:1774–1778.
    1. Parry SD, Stansfield R, Jelley D, et al. Does bacterial gastroenteritis predispose people to functional gastrointestinal disorders? A prospective, community-based, case-control study. Am J Gastroenterol. 2003;98:1970–1975.
    1. Wang LH, Fang XC, Pan GZ. Bacillary dysentery as a causative factor of irritable bowel syndrome and its pathogenesis. Gut. 2004;53:1096–1101.
    1. McKendrick MW, Read NW. Irritable bowel syndrome--post salmonella infection. J Infect. 1994;29:1–3.
    1. Gwee KA, Graham JC, McKendrick MW, et al. Psychometric scores and persistence of irritable bowel after infectious diarrhoea. Lancet. 1996;347:150–153.
    1. Dunlop SP, Jenkins D, Neal KR, et al. Relative importance of enterochromaffin cell hyperplasia, anxiety, and depression in postinfectious IBS. Gastroenterology. 2003;125:1651–1659.
    1. Borgaonkar MR, Ford DC, Marshall JK, et al. The incidence of irritable bowel syndrome among community subjects with previous acute enteric infection. Dig Dis Sci. 2006;51:1026–1032.
    1. Stermer E, Lubezky A, Potasman I, et al. Is traveler's diarrhea a significant risk factor for the development of irritable bowel syndrome? A prospective study. Clin Infect Dis. 2006;43:898–901.
    1. Kendall ME, Crim S, Fullerton K, et al. Travel-associated enteric infections diagnosed after return to the United States, Foodborne Diseases Active Surveillance Network (FoodNet), 2004–2009. Clin Infect Dis. 2012;54(Suppl 5):S480–S487.
    1. LaRocque RC, Rao SR, Lee J, et al. Global TravEpiNet: a national consortium of clinics providing care to international travelers--analysis of demographic characteristics, travel destinations, and pretravel healthcare of high-risk US international travelers, 2009–2011. Clin Infect Dis. 2012;54:455–462.
    1. Riddle MS, Welsh M, Porter CK, et al. The epidemiology of irritable bowel syndrome in the US Military: Findings from the Millennium Cohort Study. Am J Gastroenterol. 2016;111:93–104.
    1. Shah ED, Riddle MS, Chang C, et al. Estimating the contribution of acute gastroenteritis to the overall prevalence of irritable bowel syndrome. J Neurogastroenterol Motil. 2012;18:200–204.
    1. Halvorson HA, Schlett CD, Riddle MS. Postinfectious irritable bowel syndrome--a meta-analysis. Am J Gastroenterol. 2006;101:1894–1899. quiz 1942.
    1. Jalanka-Tuovinen J, Salojarvi J, Salonen A, et al. Faecal microbiota composition and host-microbe cross-talk following gastroenteritis and in postinfectious irritable bowel syndrome. Gut. 2014;63:1737–1745.
    1. Lackner JM, Quigley BM, Blanchard EB. Depression and abdominal pain in IBS patients: the mediating role of catastrophizing. Psychosom Med. 2004;66:435–441.
    1. Drossman DA. Do psychosocial factors define symptom severity and patient status in irritable bowel syndrome? Am J Med. 1999;107:41S–50S.
    1. Bansal T, Englert D, Lee J, et al. Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect Immun. 2007;75:4597–4607.
    1. Bailey MT. Psychological stress, immunity, and the effects on indigenous microflora. Adv Exp Med Biol. 2016;874:225–246.
    1. Halder SL, Locke GR, 3rd, Schleck CD, et al. Natural history of functional gastrointestinal disorders: a 12-year longitudinal population-based study. Gastroenterology. 2007;133:799–807.
    1. Olafsdottir LB, Gudjonsson H, Jonsdottir HH, et al. Stability of the irritable bowel syndrome and subgroups as measured by three diagnostic criteria - a 10-year follow-up study. Aliment Pharmacol Ther. 2010;32:670–680.

Source: PubMed

3
Se inscrever