Early-Life Infections, Antibiotics and Later Risk of Childhood and Early Adult-Onset Inflammatory Bowel Disease: Pooled Analysis of Two Scandinavian Birth Cohorts.
Crohn's disease
penicillin
ulcerative colitis
Journal
Alimentary pharmacology & therapeutics
ISSN: 1365-2036
Titre abrégé: Aliment Pharmacol Ther
Pays: England
ID NLM: 8707234
Informations de publication
Date de publication:
25 Oct 2024
25 Oct 2024
Historique:
revised:
31
05
2024
received:
06
05
2024
accepted:
13
10
2024
medline:
25
10
2024
pubmed:
25
10
2024
entrez:
25
10
2024
Statut:
aheadofprint
Résumé
Childhood antibiotic use has been associated with inflammatory bowel disease (IBD), although the potential contribution of infection frequency remains uncertain. To explore the association between early-life infections, antibiotics and IBD development. We used population-based data from ABIS (Sweden) and MoBa (Norway) cohorts following children from birth (1997-2009) until 2021. Prospectively collected questionnaires identified infection frequency (any, gastrointestinal and respiratory) and antibiotics (any, penicillin and non-penicillin) until age 3. IBD diagnosis required ≥ 2 records in national health registries. Cohort-specific hazard ratios (aHR), adjusted for parental education, smoking and IBD were estimated and pooled using a random-effects model. Antibiotic analyses were adjusted for infection frequency. There were 103,046 children (11,872 ABIS and 91,174 MoBa), contributing to 1,663,898 person-years of follow-up, during which 395 were diagnosed with IBD. The frequency of any infection at 0 to < 1 and 1 to < 3 years showed a pooled aHR of 1.01 (95% confidence interval [CI] = 0.96-1.07) and 1.00 (95% CI = 0.99-1.01) per additional infection for IBD. Adjusting for infections, any versus no antibiotics in the first year was associated with IBD (pooled aHR = 1.33 [95% CI = 1.01-1.76]). The aHR for additional antibiotic course was 1.17 (95% CI = 0.96-1.44), driven by penicillin (per additional course, aHR = 1.28 [95% CI = 1.02-1.60]). Although antibiotics at 1 to < 3 years did not show an association with IBD or Crohn's disease, non-penicillin antibiotics were associated with ulcerative colitis (per additional course, aHR = 1.95 [95% CI = 1.38-2.75]). Early-life antibiotic use was, a significant risk factor for childhood and early adult-onset IBD, independent of infection frequency.
Sections du résumé
BACKGROUND
BACKGROUND
Childhood antibiotic use has been associated with inflammatory bowel disease (IBD), although the potential contribution of infection frequency remains uncertain.
AIMS
OBJECTIVE
To explore the association between early-life infections, antibiotics and IBD development.
METHODS
METHODS
We used population-based data from ABIS (Sweden) and MoBa (Norway) cohorts following children from birth (1997-2009) until 2021. Prospectively collected questionnaires identified infection frequency (any, gastrointestinal and respiratory) and antibiotics (any, penicillin and non-penicillin) until age 3. IBD diagnosis required ≥ 2 records in national health registries. Cohort-specific hazard ratios (aHR), adjusted for parental education, smoking and IBD were estimated and pooled using a random-effects model. Antibiotic analyses were adjusted for infection frequency.
RESULTS
RESULTS
There were 103,046 children (11,872 ABIS and 91,174 MoBa), contributing to 1,663,898 person-years of follow-up, during which 395 were diagnosed with IBD. The frequency of any infection at 0 to < 1 and 1 to < 3 years showed a pooled aHR of 1.01 (95% confidence interval [CI] = 0.96-1.07) and 1.00 (95% CI = 0.99-1.01) per additional infection for IBD. Adjusting for infections, any versus no antibiotics in the first year was associated with IBD (pooled aHR = 1.33 [95% CI = 1.01-1.76]). The aHR for additional antibiotic course was 1.17 (95% CI = 0.96-1.44), driven by penicillin (per additional course, aHR = 1.28 [95% CI = 1.02-1.60]). Although antibiotics at 1 to < 3 years did not show an association with IBD or Crohn's disease, non-penicillin antibiotics were associated with ulcerative colitis (per additional course, aHR = 1.95 [95% CI = 1.38-2.75]).
CONCLUSION
CONCLUSIONS
Early-life antibiotic use was, a significant risk factor for childhood and early adult-onset IBD, independent of infection frequency.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Forskningsrådet i Sydöstra Sverige
Organisme : JDRF Wallenberg Foundation
ID : K 98-99D-12813-01A
Organisme : LFoU grants from Region Östergötland and Linköping university
Organisme : Svenska Sällskapet för Medicinsk Forskning
Organisme : Birgitta och Göran Karlssons Stiftelse
Organisme : ALF funding
Organisme : Barndiabetesfonden
Organisme : Forskningsrådet för Arbetsliv och Socialvetenskap
ID : FAS2004-1775
Organisme : Vetenskapsrådet
ID : K2005-72X-11242-11A
Organisme : Vetenskapsrådet
ID : K2008-69X-20826-01-4
Organisme : Östgöta Brandstodsbolag
Informations de copyright
© 2024 The Author(s). Alimentary Pharmacology & Therapeutics published by John Wiley & Sons Ltd.
Références
M. Agrawal and T. Jess, “Implications of the Changing Epidemiology of Inflammatory Bowel Disease in a Changing World,” United European Gastroenterology Journal 10 (2022): 1113–1120.
M. E. Kuenzig, S. G. Fung, L. Marderfeld, et al., “Twenty‐First Century Trends in the Global Epidemiology of Pediatric‐Onset Inflammatory Bowel Disease: Systematic Review,” Gastroenterology 162 (2022): 1147–1159.
A. S. Faye, K. H. Allin, A. T. Iversen, et al., “Antibiotic Use as a Risk Factor for Inflammatory Bowel Disease Across the Ages: A Population‐Based Cohort Study,” Gut 72 (2023): 663–670.
R. B. Gearry, A. K. Richardson, C. M. Frampton, A. J. Dodgshun, and M. L. Barclay, “Population‐Based Cases Control Study of Inflammatory Bowel Disease Risk Factors,” Journal of Gastroenterology and Hepatology 25 (2010): 325–333.
D. Y. Han, A. G. Fraser, P. Dryland, and L. R. Ferguson, “Environmental Factors in the Development of Chronic Inflammation: A Case–Control Study on Risk Factors for Crohn's Disease Within New Zealand,” Mutation Research 690 (2010): 116–122.
A. Hviid, H. Svanstrom, and M. Frisch, “Antibiotic Use and Inflammatory Bowel Diseases in Childhood,” Gut 60 (2011): 49–54.
M. P. Kronman, T. E. Zaoutis, K. Haynes, R. Feng, and S. E. Coffin, “Antibiotic Exposure and IBD Development Among Children: A Population‐Based Cohort Study,” Pediatrics 130 (2012): e794–e803.
L. H. Nguyen, A. K. Ortqvist, Y. Cao, et al., “Antibiotic Use and the Development of Inflammatory Bowel Disease: A National Case–Control Study in Sweden,” Lancet Gastroenterology & Hepatology 5 (2020): 986–995.
A. K. Ortqvist, C. Lundholm, J. Halfvarson, et al., “Fetal and Early Life Antibiotics Exposure and Very Early Onset Inflammatory Bowel Disease: A Population‐Based Study,” Gut 68 (2019): 218–225.
S. Y. Shaw, J. F. Blanchard, and C. N. Bernstein, “Association Between the Use of Antibiotics in the First Year of Life and Pediatric Inflammatory Bowel Disease,” American Journal of Gastroenterology 105 (2010): 2687–2692.
J. Torres, C. Gomes, C. B. Jensen, et al., “Risk Factors for Developing Inflammatory Bowel Disease Within and Across Families With a Family History of IBD,” Journal of Crohn's & Colitis 17 (2023): 30–36.
L. Virta, A. Auvinen, H. Helenius, P. Huovinen, and K. L. Kolho, “Association of Repeated Exposure to Antibiotics With the Development of Pediatric Crohn's Disease–A Nationwide, Register‐Based Finnish Case‐Control Study,” American Journal of Epidemiology 175 (2012): 775–784.
C. Canova, J. F. Ludvigsson, R. Di Domenicantonio, et al., “Perinatal and Antibiotic Exposures and the Risk of Developing Childhood‐Onset Inflammatory Bowel Disease: A Nested Case–Control Study Based on a Population‐Based Birth Cohort,” International Journal of Environmental Research and Public Health 17 (2020): 2409.
S. J. Oh, H. J. Kim, C. K. Lee, and The Big Data Research Group (BDRG) of the Korean Society of Gastroenterology, “A Dose‐Dependent Increase in the Risk of Inflammatory Bowel Disease After Exposure to Broad‐Spectrum Antibiotics: A National Population Study in Korea,” Alimentary Pharmacology & Therapeutics 58 (2023): 191–206.
J. E. Axelrad, O. Olen, J. Askling, et al., “Gastrointestinal Infection Increases Odds of Inflammatory Bowel Disease in a Nationwide Case–Control Study,” Clinical Gastroenterology and Hepatology 17 (2019): 1311–1322.
L. A. Garcia Rodriguez, A. Ruigomez, and J. Panes, “Acute Gastroenteritis Is Followed by an Increased Risk of Inflammatory Bowel Disease,” Gastroenterology 130 (2006): 1588–1594.
K. O. Gradel, H. L. Nielsen, H. C. Schonheyder, et al., “Increased Short‐ and Long‐Term Risk of Inflammatory Bowel Disease After Salmonella or Campylobacter Gastroenteritis,” Gastroenterology 137 (2009): 495–501.
H. Hildebrand, P. Malmborg, J. Askling, A. Ekbom, and S. M. Montgomery, “Early‐Life Exposures Associated With Antibiotic Use and Risk of Subsequent Crohn's Disease,” Scandinavian Journal of Gastroenterology 43 (2008): 961–966.
T. Jess, J. Simonsen, N. M. Nielsen, et al., “Enteric Salmonella or Campylobacter Infections and the Risk of Inflammatory Bowel Disease,” Gut 60 (2011): 318–324.
C. K. Porter, D. R. Tribble, P. A. Aliaga, H. A. Halvorson, and M. S. Riddle, “Infectious Gastroenteritis and Risk of Developing Inflammatory Bowel Disease,” Gastroenterology 135 (2008): 781–786.
S. Y. Shaw, J. F. Blanchard, and C. N. Bernstein, “Association Between Early Childhood Otitis Media and Pediatric Inflammatory Bowel Disease: An Exploratory Population‐Based Analysis,” Journal of Pediatrics 162 (2013): 510–514.
J. F. Ludvigsson and Abis Study G, “Epidemiological Study of Constipation and Other Gastrointestinal Symptoms in 8000 Children,” Acta Paediatrica 95 (2006): 573–580.
P. Magnus, C. Birke, K. Vejrup, et al., “Cohort Profile Update: The Norwegian Mother and Child Cohort Study (MoBa),” International Journal of Epidemiology 45 (2016): 382–388.
I. J. Bakken, A. M. S. Ariansen, G. P. Knudsen, K. I. Johansen, and S. E. Vollset, “The Norwegian Patient Registry and the Norwegian Registry for Primary Health Care: Research Potential of Two Nationwide Health‐Care Registries,” Scandinavian Journal of Public Health 48 (2020): 49–55.
J. F. Ludvigsson, C. Almqvist, A. K. Bonamy, et al., “Registers of the Swedish Total Population and Their Use in Medical Research,” European Journal of Epidemiology 31 (2016): 125–136.
A. Welander, A. R. Tjernberg, S. M. Montgomery, J. Ludvigsson, and J. F. Ludvigsson, “Infectious Disease and Risk of Later Celiac Disease in Childhood,” Pediatrics 125 (2010): e530–e536.
J. H. Larsen, S. Andersen, G. Perminow, et al., “Higher Incidence of Paediatric Inflammatory Bowel Disease by Increasing Latitude in Norway, but Stable Incidence by Age,” Acta Paediatrica 113 (2024): 1720–1727.
M. Ostensson, O. Bjorkqvist, A. Guo, et al., “Epidemiology, Validation, and Clinical Characteristics of Inflammatory Bowel Disease: The ABIS Birth Cohort Study,” BMC Gastroenterology 23 (2023): 199.
A. H. Everhov, J. Halfvarson, P. Myrelid, et al., “Incidence and Treatment of Patients Diagnosed With Inflammatory Bowel Diseases at 60 Years or Older in Sweden,” Gastroenterology 154 (2018): 518–528.
G. L. Jakobsson, E. Sternegard, O. Olen, et al., “Validating Inflammatory Bowel Disease (IBD) in the Swedish National Patient Register and the Swedish Quality Register for IBD (SWIBREG),” Scandinavian Journal of Gastroenterology 52 (2017): 216–221.
M. Agrawal, J. Sabino, C. Frias‐Gomes, et al., “Early Life Exposures and the Risk of Inflammatory Bowel Disease: Systematic Review and Meta‐Analyses,” EClinicalMedicine 36 (2021): 100884.
N. Christensen, S. Bruun, J. Sondergaard, et al., “Breastfeeding and Infections in Early Childhood: A Cohort Study,” Pediatrics 146 (2020): e20191892.
K. Hashimoto, H. Maeda, H. Iwasa, et al., “Tobacco Exposure During Pregnancy and Infections in Infants up to 1 Year of Age: The Japan Environment and Children's Study,” Journal of Epidemiology 33 (2023): 489–497.
J. Liu, J. Ren, X. Gao, et al., “A Causal Relationship Between Educational Attainment and Risk of Infectious Diseases: A Mendelian Randomisation Study,” Journal of Global Health 14 (2024): 4089.
A. Meyer, M. Taine, J. Drouin, A. Weill, F. Carbonnel, and R. Dray‐Spira, “Serious Infections in Children Born to Mothers With Inflammatory Bowel Disease With in Utero Exposure to Thiopurines and Anti‐Tumor Necrosis Factor,” Clinical Gastroenterology and Hepatology 20 (2022): 1269–1281.
I. Sigvardsson, J. Ludvigsson, B. Andersson, K. Størdal, and K. Mårild, “Tobacco Smoke Exposure in Early Childhood and Later Risk of Inflammatory Bowel Disease: A Scandinavian Birth Cohort Study,” Journal of Crohn's & Colitis 18 (2024): 661–670.
I. Sigvardsson, K. Stordal, M. Ostensson, et al., “Childhood Socioeconomic Characteristics and Risk of Inflammatory Bowel Disease: A Scandinavian Birth Cohort Study,” Inflammatory Bowel Diseases 30 (2023): 1801–1811.
E. I. Benchimol, D. R. Mack, A. Guttmann, et al., “Inflammatory Bowel Disease in Immigrants to Canada and Their Children: A Population‐Based Cohort Study,” American Journal of Gastroenterology 110 (2015): 553–563.
N. H. Vissing, B. L. Chawes, M. A. Rasmussen, and H. Bisgaard, “Epidemiology and Risk Factors of Infection in Early Childhood,” Pediatrics 141 (2018): e20170933.
L. M. Irgens, “The Medical Birth Registry of Norway. Epidemiological Research and Surveillance Throughout 30 Years,” Acta Obstetricia et Gynecologica Scandinavica 79 (2000): 435–439.
D. Schoenfeld, “Partial Residuals for the Proportional Hazards Regression‐Model,” Biometrika 69 (1982): 239–241.
R. DerSimonian and N. Laird, “Meta‐Analysis in Clinical Trials,” Controlled Clinical Trials 7 (1986): 177–188.
S. van Buuren, “Multiple Imputation of Discrete and Continuous Data by Fully Conditional Specification,” Statistical Methods in Medical Research 16 (2007): 219–242.
M. M. Suttorp, B. Siegerink, K. J. Jager, C. Zoccali, and F. W. Dekker, “Graphical Presentation of Confounding in Directed Acyclic Graphs,” Nephrology, Dialysis, Transplantation 30 (2015): 1418–1423.
N. A. Bokulich, J. Chung, T. Battaglia, et al., “Antibiotics, Birth Mode, and Diet Shape Microbiome Maturation During Early Life,” Science Translational Medicine 8 (2016): 343ra82.
J. Ramirez, F. Guarner, L. Bustos Fernandez, A. Maruy, V. L. Sdepanian, and H. Cohen, “Antibiotics as Major Disruptors of Gut Microbiota,” Frontiers in Cellular and Infection Microbiology 10 (2020): 572912.
P. Brodin, “Immune‐Microbe Interactions Early in Life: A Determinant of Health and Disease Long Term,” Science 376 (2022): 945–950.
E. Kindgren and J. Ludvigsson, “Infections and Antibiotics During Fetal Life and Childhood and Their Relationship to Juvenile Idiopathic Arthritis: A Prospective Cohort Study,” Pediatric Rheumatology Online Journal 19 (2021): 145.
R. Ungaro, C. N. Bernstein, R. Gearry, et al., “Antibiotics Associated With Increased Risk of New‐Onset Crohn's Disease but Not Ulcerative Colitis: A Meta‐Analysis,” American Journal of Gastroenterology 109 (2014): 1728–1738.
C. Manichanh, N. Borruel, F. Casellas, and F. Guarner, “The Gut Microbiota in IBD,” Nature Reviews. Gastroenterology & Hepatology 9 (2012): 599–608.
T. Yatsunenko, F. E. Rey, M. J. Manary, et al., “Human Gut Microbiome Viewed Across Age and Geography,” Nature 486 (2012): 222–227.
L. Gehrt, I. Laake, H. Englund, et al., “Hospital Contacts for Infectious Diseases Among Children in Denmark, Finland, Norway, and Sweden, 2008–2017,” Clinical Epidemiology 14 (2022): 609–621.
B. Smith, L. K. Chu, T. C. Smith, et al., “Challenges of Self‐Reported Medical Conditions and Electronic Medical Records Among Members of a Large Military Cohort,” BMC Medical Research Methodology 8 (2008): 37.
B. Clark and M. McKendrick, “A Review of Viral Gastroenteritis,” Current Opinion in Infectious Diseases 17 (2004): 461–469.
C. A. Woodall, L. J. McGeoch, A. D. Hay, et al., “Respiratory Tract Infections and Gut Microbiome Modifications: A Systematic Review,” PLoS One 17 (2022): e0262057.
C. G. Alcazar, V. M. Paes, Y. Shao, et al., “The Association Between Early‐Life Gut Microbiota and Childhood Respiratory Diseases: A Systematic Review,” Lancet Microbe 3 (2022): e867–e880.
C. Petersen and J. L. Round, “Defining Dysbiosis and Its Influence on Host Immunity and Disease,” Cellular Microbiology 16 (2014): 1024–1033.
A. Sullivan, C. Edlund, and C. E. Nord, “Effect of Antimicrobial Agents on the Ecological Balance of Human Microflora,” Lancet Infectious Diseases 1 (2001): 101–114.
K. L. Glassner, B. P. Abraham, and E. M. M. Quigley, “The Microbiome and Inflammatory Bowel Disease,” Journal of Allergy and Clinical Immunology 145 (2020): 16–27.
J. Hurych, A. Mascellani Bergo, T. Lerchova, et al., “Faecal Bacteriome and Metabolome Profiles Associated With Decreased Mucosal Inflammatory Activity Upon Anti‐TNF Therapy in Paediatric Crohn's Disease,” Journal of Crohn's & Colitis 18 (2023): 106–120.
J. Li, H. Si, H. Du, et al., “Comparison of Gut Microbiota Structure and Actinobacteria Abundances in Healthy Young Adults and Elderly Subjects: A Pilot Study,” BMC Microbiology 21 (2021): 13.
J. Kelsen and R. N. Baldassano, “Inflammatory Bowel Disease: The Difference Between Children and Adults,” Inflammatory Bowel Diseases 14, no. Suppl 2 (2008): S9–S11.
R. E. Andersson, G. Olaison, C. Tysk, and A. Ekbom, “Appendectomy Is Followed by Increased Risk of Crohn's Disease,” Gastroenterology 124 (2003): 40–46.
R. M. Nilsen, S. E. Vollset, H. K. Gjessing, et al., “Self‐Selection and Bias in a Large Prospective Pregnancy Cohort in Norway,” Paediatric and Perinatal Epidemiology 23 (2009): 597–608.