Skip to main content

Advertisement

Log in

The relationship between the severity of inflammatory bowel diseases and expirium air carbon monoxide levels

  • RESEARCH
  • Published:
International Journal of Colorectal Disease Aims and scope Submit manuscript

Abstract

Introduction

We investigated the relationship between expirium air carbon monoxide (E-CO) levels and disease severity in patients with ulcerative colitis (UC) and Crohn’s disease (CD).

Methods

After their first follow-ups, the E-CO levels of 162 patients with UC and 100 with CD were measured for four consecutive weeks. Blood samples were collected from all the patients, and their clinical severity was determined 1 month after their initial presentation. The clinical severity of CD was determined using the Harvey Bradshaw index (HBI), while the patients with UC completed the SEO clinical activity index (SEOI). The relationships between the disease severity and the means of these four E-CO readings were then compared.

Results

The mean age of the participants was 42.28 ± 14.9 years, and 158 (60.3%) were men. In addition, 27.2% of the UC group and 44% of the CD group were smokers. The mean SEOI score was 145.7 ± 42.0 (min = 90, max = 227), and the mean HBI score was 5.75 ± 3.3 (min = 1, max = 15). Increased CO ppm (OR = −9.047 to 7.654 95% CI) and the number of cigarettes smoked per day (OR = −0.161 to 1.157 95% CI) emerged as independent risk factors for lower SEO scores in the linear regression models (p < 0.001), while the number of cigarettes smoked per day (OR = 0.271 to 1.182% 95 CI) was a risk factor for higher HBI scores (p = 0.022).

Conclusion

UC severity decreased with higher E-CO levels and the mean number of cigarettes smoked, while CD severity increased in line with the mean number of cigarettes smoked.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Data availability

Datasets are available by corresponding author on reasonable request.

References

  1. Zhang L, Ren JW, Wong CC, Wu WK, Ren SX, Shen J et al (2012) Effects of cigarette smoke and its active components on ulcer formation and healing in the gastrointestinal mucosa. Curr Med Chem 19(1):63–69

    CAS  PubMed  Google Scholar 

  2. Calkins BM (1989) A meta-analysis of the role of smoking in inflammatory bowel disease. Dig Dis Sci 34(12):1841–1854

    CAS  PubMed  Google Scholar 

  3. Vessey M, Jewell D, Smith A, Yeates D, McPherson K (1986) Chronic inflammatory bowel disease, cigarette smoking, and use of oral contraceptives: findings in a large cohort study of women of childbearing age. Br Med J (Clin Res Ed) 292(6528):1101–1103

    CAS  PubMed  Google Scholar 

  4. Piovani D, Danese S, Peyrin-Biroulet L, Nikolopoulos GK, Lytras T, Bonovas S (2019) Environmental risk factors for inflammatory bowel diseases: an umbrella review of meta-analyses. Gastroenterology 157(3):647–659 e644

    PubMed  Google Scholar 

  5. Cottone M, Rosselli M, Orlando A, Oliva L, Puleo A, Cappello M et al (1994) Smoking habits and recurrence in Crohn’s disease. Gastroenterology 106(3):643–648

    CAS  PubMed  Google Scholar 

  6. To N, Gracie DJ, Ford AC (2016) Systematic review with meta-analysis: the adverse effects of tobacco smoking on the natural history of Crohn’s disease. Aliment Pharmacol Ther 43(5):549–561

    CAS  PubMed  Google Scholar 

  7. Lee S, Kuenzig ME, Ricciuto A, Zhang Z, Shim HH, Panaccione R et al (2021) Smoking may reduce the effectiveness of anti-TNF therapies to induce clinical response and remission in Crohn’s disease: a systematic review and meta-analysis. J Crohns Colitis 15(1):74–87

    PubMed  Google Scholar 

  8. Birrenbach T, Bocker U (2004) Inflammatory bowel disease and smoking: a review of epidemiology, pathophysiology, and therapeutic implications. Inflamm Bowel Dis 10(6):848–859

    PubMed  Google Scholar 

  9. Park JH, Peyrin-Biroulet L, Eisenhut M, Shin JI (2017) IBD immunopathogenesis: a comprehensive review of inflammatory molecules. Autoimmun Rev 16(4):416–426

    CAS  PubMed  Google Scholar 

  10. Marcilla A, Martinez I, Berenguer D, Gomez-Siurana A, Beltran MI (2012) Comparative study of the main characteristics and composition of the mainstream smoke of ten cigarette brands sold in Spain. Food Chem Toxicol 50(5):1317–1333

    CAS  PubMed  Google Scholar 

  11. Eliakim R, Karmeli F, Rachmilewitz D, Cohen P, Fich A (1998) Effect of chronic nicotine administration on trinitrobenzene sulphonic acid-induced colitis. Eur J Gastroenterol Hepatol 10(12):1013–1019

    CAS  PubMed  Google Scholar 

  12. Eliakim R, Karmeli F, Cohen P, Heyman SN, Rachmilewitz D (2001) Dual effect of chronic nicotine administration: augmentation of jejunitis and amelioration of colitis induced by iodoacetamide in rats. Int J Colorectal Dis 16(1):14–21

    CAS  PubMed  Google Scholar 

  13. Zhang W, Lin H, Zou M, Yuan Q, Huang Z, Pan X et al (2022) Nicotine in inflammatory diseases: anti-inflammatory and pro-inflammatory effects. Front Immunol 13:826889

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Takagi T, Naito Y, Uchiyama K, Yoshikawa T (2010) The role of heme oxygenase and carbon monoxide in inflammatory bowel disease. Redox Rep 15(5):193–201

    CAS  PubMed  Google Scholar 

  15. Sheikh SZ, Hegazi RA, Kobayashi T, Onyiah JC, Russo SM, Matsuoka K et al (2011) An anti-inflammatory role for carbon monoxide and heme oxygenase-1 in chronic Th2-mediated murine colitis. J Immunol 186(9):5506–5513

    CAS  PubMed  Google Scholar 

  16. Lashner BA, Hanauer SB, Silverstein MD (1990) Testing nicotine gum for ulcerative colitis patients. Experience with single-patient trials. Dig Dis Sci 35(7):827–832

    CAS  PubMed  Google Scholar 

  17. Lewis CM, Whitwell SC, Forbes A, Sanderson J, Mathew CG, Marteau TM (2007) Estimating risks of common complex diseases across genetic and environmental factors: the example of Crohn disease. J Med Genet 44(11):689–694

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Tozun N, Atug O, Imeryuz N, Hamzaoglu HO, Tiftikci A, Parlak E et al (2009) Clinical characteristics of inflammatory bowel disease in Turkey: a multicenter epidemiologic survey. J Clin Gastroenterol 43(1):51–57

    PubMed  Google Scholar 

  19. Irving JM, Clark EC, Crombie IK, Smith WC (1988) Evaluation of a portable measure of expired-air carbon monoxide. Prev Med 17(1):109–115

    CAS  PubMed  Google Scholar 

  20. Riaz M, Lewis S, Coleman T, Aveyard P, West R, Naughton F et al (2016) Which measures of cigarette dependence are predictors of smoking cessation during pregnancy? Analysis of data from a randomized controlled trial. Addiction 111(9):1656–1665

    PubMed  PubMed Central  Google Scholar 

  21. Seo M, Okada M, Yao T, Ueki M, Arima S, Okumura M (1992) An index of disease activity in patients with ulcerative colitis. Am J Gastroenterol 87(8):971–976

    CAS  PubMed  Google Scholar 

  22. Harvey RF, Bradshaw JM (1980) A simple index of Crohn’s-disease activity. Lancet 1(8167):514

    CAS  PubMed  Google Scholar 

  23. van der Heide F, Dijkstra A, Albersnagel FA, Kleibeuker JH, Dijkstra G (2010) Active and passive smoking behaviour and cessation plans of patients with Crohn’s disease and ulcerative colitis. J Crohns Colitis 4(2):125–131

    PubMed  Google Scholar 

  24. Khutoryanskiy VV (2015) Supramolecular materials: longer and safer gastric residence. Nat Mater 14(10):963–964

    CAS  PubMed  Google Scholar 

  25. Biedermann L, Brulisauer K, Zeitz J, Frei P, Scharl M, Vavricka SR et al (2014) Smoking cessation alters intestinal microbiota: insights from quantitative investigations on human fecal samples using FISH. Inflamm Bowel Dis 20(9):1496–1501

    PubMed  Google Scholar 

  26. de Souza HS, Fiocchi C (2016) Immunopathogenesis of IBD: current state of the art. Nat Rev Gastroenterol Hepatol 13(1):13–27

    PubMed  Google Scholar 

  27. Li LF, Chan RL, Lu L, Shen J, Zhang L, Wu WK et al (2014) Cigarette smoking and gastrointestinal diseases: the causal relationship and underlying molecular mechanisms (review). Int J Mol Med 34(2):372–380

    CAS  PubMed  Google Scholar 

  28. Puglisi F, Capuano P, Simone M, Verzillo F, Laurentaci C, Catalano G (1999) Immunogenetics of inflammatory bowel disease. Minerva Gastroenterol Dietol 45(1):5–9

    CAS  PubMed  Google Scholar 

  29. Eliakim R, Fan QX, Babyatsky MW (2002) Chronic nicotine administration differentially alters jejunal and colonic inflammation in interleukin-10 deficient mice. Eur J Gastroenterol Hepatol 14(6):607–614

    CAS  PubMed  Google Scholar 

  30. Lakhan SE, Kirchgessner A (2011) Anti-inflammatory effects of nicotine in obesity and ulcerative colitis. J Transl Med 9:129

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Saeed RW, Varma S, Peng-Nemeroff T, Sherry B, Balakhaneh D, Huston J et al (2005) Cholinergic stimulation blocks endothelial cell activation and leukocyte recruitment during inflammation. J Exp Med 201(7):1113–1123

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Mackern-Oberti JP, Riquelme SA, Llanos C, Schmidt CB, Simon T, Anegon I et al (2014) Heme oxygenase-1 as a target for the design of gene and pharmaceutical therapies for autoimmune diseases. Curr Gene Ther 14(3):218–235

    CAS  PubMed  Google Scholar 

  33. Berkowitz L, Schultz BM, Salazar GA, Pardo-Roa C, Sebastian VP, Alvarez-Lobos MM et al (2018) Impact of cigarette smoking on the gastrointestinal tract inflammation: opposing effects in Crohn’s disease and ulcerative colitis. Front Immunol 9:74

    PubMed  PubMed Central  Google Scholar 

  34. Lindell G, Farnebo LO, Chen D, Nexo E, Rask Madsen J, Bukhave K et al (1993) Acute effects of smoking during modified sham feeding in duodenal ulcer patients. An analysis of nicotine, acid secretion, gastrin, catecholamines, epidermal growth factor, prostaglandin E2, and bile acids. Scand J Gastroenterol 28(6):487–494

    CAS  PubMed  Google Scholar 

  35. Ingram JR, Thomas GA, Rhodes J, Green JT, Hawkes ND, Swift JL et al (2005) A randomized trial of nicotine enemas for active ulcerative colitis. Clin Gastroenterol Hepatol 3(11):1107–1114

    CAS  PubMed  Google Scholar 

  36. Sandborn WJ, Tremaine WJ, Offord KP, Lawson GM, Petersen BT, Batts KP et al (1997) Transdermal nicotine for mildly to moderately active ulcerative colitis. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 126(5):364–371

    CAS  PubMed  Google Scholar 

  37. Pullan RD, Rhodes J, Ganesh S, Mani V, Morris JS, Williams GT et al (1994) Transdermal nicotine for active ulcerative colitis. N Engl J Med 330(12):811–815

    CAS  PubMed  Google Scholar 

  38. Vermeire S, Van Assche G, Rutgeerts P (2006) Laboratory markers in IBD: useful, magic, or unnecessary toys? Gut 55(3):426–431

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Bridger S, Lee JC, Bjarnason I, Jones JE, Macpherson AJ (2002) In siblings with similar genetic susceptibility for inflammatory bowel disease, smokers tend to develop Crohn’s disease and non-smokers develop ulcerative colitis. Gut 51(1):21–25

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Cosnes J, Beaugerie L, Carbonnel F, Gendre JP (2001) Smoking cessation and the course of Crohn’s disease: an intervention study. Gastroenterology 120(5):1093–1099

    CAS  PubMed  Google Scholar 

  41. Pan KT, Leonardi GS, Ucci M, Croxford B (2021) Can exhaled carbon monoxide be used as a marker of exposure? A cross-sectional study in young adults. Int J Environ Res Public Health 18(22):11893

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Raiff BR, Faix C, Turturici M, Dallery J (2010) Breath carbon monoxide output is affected by speed of emptying the lungs: implications for laboratory and smoking cessation research. Nicotine Tob Res 12:834–838. https://doi.org/10.1093/ntr/ntq090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Meredith SE, Robinson A, Erb P, Spieler CA, Klugman N, Dutta P, Dallery J (2014) A mobile-phone-based breath carbon monoxide meter to detect cigarette smoking. Nicotine Tob Res. 16(6):766–73. https://doi.org/10.1093/ntr/ntt275. Epub 2014 Jan 27. PMID: 24470633; PMCID: PMC4031569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Carroll DM, Stepanov I, O’Connor R, Luo X, Cummings KM, Rees VW et al (2021) Impact of cigarette filter ventilation on U.S. smokers’ perceptions and biomarkers of exposure and potential harm. Cancer Epidemiol Biomarkers Prev 30(1):38–44

    CAS  PubMed  Google Scholar 

  45. Scherer G, Lee PN (2014) Smoking behavior and compensation: a review of the literature with meta-analysis. Regul Toxicol Pharmacol 70(3):615–628

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Bektas Murat Yalcin: study design, data analysis, and writing of first draft of manuscript. Yildiz Kirac: patient recruitment and data collection. Muge Ustaoglu: editing data, data collection, and the final edition of first draft of manuscript.

Corresponding author

Correspondence to Bektas Murat Yalcin.

Ethics declarations

Ethical approval

The study was approved by the Ethics Committee of the Ondokuz Mayis University Faculty of Medicine, and complied with the Declaration of Helsinki.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yalcin, B., Ustaoglu, M. & Kirac, Y. The relationship between the severity of inflammatory bowel diseases and expirium air carbon monoxide levels. Int J Colorectal Dis 38, 188 (2023). https://doi.org/10.1007/s00384-023-04468-9

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00384-023-04468-9

Keywords

Navigation