Systematic review with meta-analysis: The adverse effects of tobacco smoking on the natural history of Crohn's disease

Alimentary Pharmacology and Therapeutics

Volumn 43, Issue 5, 2016, Pages 549-561

  To, N ^a,b   Gracie, D J ^a,b   Ford, A C ^a,b  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CROHN DISEASE; DISEASE ACTIVITY; DISEASE COURSE; DISEASE EXACERBATION; HUMAN; INTESTINE SURGERY; META ANALYSIS; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SECOND LOOK SURGERY; SMOKING; SMOKING CESSATION; SYSTEMATIC REVIEW; ADVERSE EFFECTS; PATHOPHYSIOLOGY; RISK FACTOR;

CROHN DISEASE; DISEASE PROGRESSION; HUMANS; RISK FACTORS; SMOKING;

EID: 84953888856     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/apt.13511     Document Type: Article

References (81)

1. Loftus CG, Loftus EV, Harmsen WS, et al,. Update on the incidence and prevalence of Crohn's disease and ulcerative colitis in Olmsted County, Minnesota, 1940-2000. Inflamm Bowel Dis 2007; 13: 254-61.
2. Loftus EV, Silverstein MD, Sandborn WJ, Tremaine WJ, Harmsen WS, Zinsmeister AR,. Crohn's disease in Olmsted County, Minnesota, 1940-1993: incidence, prevalence, and survival. Gastroenterology 1998; 114: 1161-8.
3. Kappelman MD, Rifas-Shiman SL, Kleinman K, et al,. The prevalence and geographic distribution of Crohn's disease and ulcerative colitis in the United States. Clin Gastroenterol Hepatol 2007; 5: 1424-9.
4. Molodecky NA, Soon IS, Rabi DM, et al,. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012; 142: 46-54. e42; quiz e30.
5. Floyd D, Langham S, Severac H, Leveseque B,. The economic and quality-of-life burden of Crohn's disease in Europe and the United States, 2000 to 2013: a systematic review. Dig Dis Sci 2015; 60: 299-312.
6. Yu AP, Cabanilla LA, Wu EQ, Mulani PM, Chao J,. The costs of Crohn's disease in the United States and other Western countries: a systematic review. Curr Med Res Opin 2008; 24: 319-28.
7. Bassi A, Dodd S, Williamson P, Bodger K,. Cost of illness of inflammatory bowel disease in the UK: a single centre retrospective study. Gut 2004; 53: 1471-8.
8. Xavier RJ, Podolsky DK,. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007; 448: 427-34.
9. Somerville KW, Logan RF, Edmond M, Langman MJ,. Smoking and Crohn's disease. Br Med J (Clin Res Ed) 1984; 289: 954-6.
10. Holdstock G, Savage D, Harman M, Wright R,. Should patients with inflammatory bowel disease smoke? Br Med J (Clin Res Ed) 1984; 288: 362.
11. Birrenbach T, Böcker U,. Inflammatory bowel disease and smoking: a review of epidemiology, pathophysiology, and therapeutic implications. Inflamm Bowel Dis 2004; 10: 848-59.
12. Cosnes J, Beaugerie L, Carbonnel F, Gendre JP,. Smoking cessation and the course of Crohn's disease: an intervention study. Gastroenterology 2001; 120: 1093-9.
13. Lawrance IC, Murray K, Batman B, et al,. Crohn's disease and smoking: is it ever too late to quit? J Crohns Colitis 2013; 7: e665-71.
14. Cosnes J, Carbonnel F, Carrat F, Beaugerie L, Cattan S, Gendre J,. Effects of current and former cigarette smoking on the clinical course of Crohn's disease. Aliment Pharmacol Ther 1999; 13: 1403-11.
15. Russel MG, Volovics A, Schoon EJ, et al,. Inflammatory bowel disease: is there any relation between smoking status and disease presentation? European Collaborative IBD Study Group. Inflamm Bowel Dis 1998; 4: 182-6.
16. Timmer A, Sutherland LR, Martin F,. Oral contraceptive use and smoking are risk factors for relapse in Crohn's disease. The Canadian Mesalamine for Remission of Crohn's Disease Study Group. Gastroenterology 1998; 114: 1143-50.
17. Sands BE, Arsenault JE, Rosen MJ, et al,. Risk of early surgery for Crohn's disease: implications for early treatment strategies. Am J Gastroenterol 2003; 98: 2712-8.
18. Fornaro R, Caratto E, Caratto M, et al,. Post-operative recurrence in Crohn's disease. Critical analysis of potential risk factors. An update. Surgeon 2015; 13: 330-47.
19. Reese GE, Nanidis T, Borysiewicz C, Yamamoto T, Orchard T, Tekkis PP,. The effect of smoking after surgery for Crohn's disease: a meta-analysis of observational studies. Int J Colorectal Dis 2008; 23: 1213-21.
20. Buisson A, Chevaux JB, Allen PB, Bommelaer G, Peyrin-Biroulet L,. Review article: the natural history of postoperative Crohn's disease recurrence. Aliment Pharmacol Ther 2012; 35: 625-33.
21. Yamamoto T,. Factors affecting recurrence after surgery for Crohn's disease. World J Gastroenterol 2005; 11: 3971-9.
22. Mahid SS, Minor KS, Soto RE, Hornung CA, Galandiuk S,. Smoking and inflammatory bowel disease: a meta-analysis. Mayo Clin Proc 2006; 81: 1462-71.
23. Inamdar S, Volfson A, Rosen L, Sunday S, Katz S, Sultan K,. Smoking and early infliximab response in Crohn's disease: a meta-analysis. J Crohns Colitis 2015; 9: 140-6.
24. Song YN, Zheng P, Xiao JH, Lu ZJ,. Efficacy and safety of adalimumab for the Crohn's disease: a systematic review and meta-analysis of published randomized placebo-controlled trials. Eur J Clin Pharmacol 2014; 70: 907-14.
25. Johnson GJ, Cosnes J, Mansfield JC,. Review article: smoking cessation as primary therapy to modify the course of Crohn's disease. Aliment Pharmacol Ther 2005; 21: 921-31.
26. Wells GA, Shea B, O'Connell D, et al,. The Newcastle-Ottawa Scale (NOS) for assessing the quality of non-randomised studies in meta-analyses. Available at: http://www.ohri.ca/programs/clinical-epidemiology/oxford.asp (Accessed July 2015)
27. Higgins JP, Thompson SG, Deeks JJ, Altman DG,. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557-60.
28. DerSimonian R, Laird N,. Meta-analysis in clinical trials. Control Clin Trials 1986; 7: 177-88.
29. Egger M, Davey Smith G, Schneider M, Minder C,. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315: 629-34.
30. Sterne JA, Sutton AJ, Ioannidis JP, et al,. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ 2011; 343: d4002.
31. Fidder HH, Avidan B, Lahav M, Bar-Meir S, Chowers Y,. Clinical and demographic characterization of Jewish Crohn's disease patients in Israel. J Clin Gastroenterol 2003; 36: 8-12.
32. Seksik P, Nion-Larmurier I, Sokol H, Beaugerie L, Cosnes J,. Effects of light smoking consumption on the clinical course of Crohn's disease. Inflamm Bowel Dis 2009; 15: 734-41.
33. Harper JW, Welch MP, Sinanan MN, Wahbeh GT, Lee SD,. Co-morbid diabetes in patients with Crohn's disease predicts a greater need for surgical intervention. Aliment Pharmacol Ther 2012; 35: 126-32.
34. Zabana Y, Garcia-Planella E, Van Domselaar M, et al,. Does active smoking really influence the course of Crohn's disease? A retrospective observational study. J Crohns Colitis 2013; 7: 280-5.
35. Lindberg E, Järnerot G, Huitfeldt B,. Smoking in Crohn's disease: effect on localisation and clinical course. Gut 1992; 33: 779-82.
36. Duffy LC, Zielezny MA, Marshall JR, et al,. Cigarette smoking and risk of clinical relapse in patients with Crohn's disease. Am J Prev Med 1990; 6: 161-6.
37. Solberg IC, Vatn MH, Høie O, et al,. Clinical course in Crohn's disease: results of a Norwegian population-based ten-year follow-up study. Clin Gastroenterol Hepatol 2007; 5: 1430-8.
38. Radwan-Kwiatek K, Wójtowicz-Chomicz K, Radwan P, Skrzydło-Radomska B, Borzecki A,. Impact of cigarette smoking on the clinical outcome of Crohn's disease. Przegl Lek 2009; 66: 567-70.
39. Szamosi T, Banai J, Lakatos L, et al,. Early azathioprine/biological therapy is associated with decreased risk for first surgery and delays time to surgery but not reoperation in both smokers and nonsmokers with Crohn's disease, while smoking decreases the risk of colectomy in ulcerative colitis. Eur J Gastroenterol Hepatol 2010; 22: 872-9.
40. Song XM, Gao X, Li MZ, et al,. Clinical features and risk factors for primary surgery in 205 patients with Crohn's disease: analysis of a South China cohort. Dis Colon Rectum 2011; 54: 1147-54.
41. Renda MC, Orlando A, Civitavecchia G, et al,. The role of CARD15 mutations and smoking in the course of Crohn's disease in a Mediterranean area. Am J Gastroenterol 2008; 103: 649-55.
42. Picco MF, Zubiaurre I, Adluni M, Cangemi JR, Shelton D,. Immunomodulators are associated with a lower risk of first surgery among patients with non-penetrating non-stricturing Crohn's disease. Am J Gastroenterol 2009; 104: 2754-9.
43. Moon CM, Park DI, Kim ER, et al,. Clinical features and predictors of clinical outcomes in Korean patients with Crohn's disease: a Korean association for the study of intestinal diseases multicenter study. J Gastroenterol Hepatol 2014; 29: 74-82.
44. Karczewski J, Poniedziałek B, Rzymski P, Rychlewska-Hańczewska A, Adamski Z, Wiktorowicz K,. The effect of cigarette smoking on the clinical course of inflammatory bowel disease. Prz Gastroenterol 2014; 9: 153-9.
45. Sutherland LR, Ramcharan S, Bryant H, Fick G,. Effect of cigarette smoking on recurrence of Crohn's disease. Gastroenterology 1990; 98: 1123-8.
46. Moskovitz D, McLeod RS, Greenberg GR, Cohen Z,. Operative and environmental risk factors for recurrence of Crohn's disease. Int J Colorectal Dis 1999; 14: 224-6.
47. Yamamoto T, Keighley MR,. The association of cigarette smoking with a high risk of recurrence after ileocolonic resection for ileocecal Crohn's disease. Surg Today 1999; 29: 579-80.
48. Cullen G, O'toole A, Keegan D, Sheahan K, Hyland JM, O'donoghue DP,. Long-term clinical results of ileocecal resection for Crohn's disease. Inflamm Bowel Dis 2007; 13: 1369-73.
49. Breuer-Katschinski BD, Holländer N, Goebell H,. Effect of cigarette smoking on the course of Crohn's disease. Eur J Gastroenterol Hepatol 1996; 8: 225-8.
50. Cottone M, Rosselli M, Orlando A, et al,. Smoking habits and recurrence in Crohn's disease. Gastroenterology 1994; 106: 643-8.
51. Wright JP,. Factors influencing first relapse in patients with Crohn's disease. J Clin Gastroenterol 1992; 15: 12-6.
52. Bernstein CN, Singh S, Graff LA, Walker JR, Miller N, Cheang M,. A prospective population-based study of triggers of symptomatic flares in IBD. Am J Gastroenterol 2010; 105: 1994-2002.
53. Kane SV, Flicker M, Katz-Nelson F,. Tobacco use is associated with accelerated clinical recurrence of Crohn's disease after surgically induced remission. J Clin Gastroenterol 2005; 39: 32-5.
54. Kurer MA, Stamou KM, Wilson TR, Bradford IM, Leveson SH,. Early symptomatic recurrence after intestinal resection in Crohn's disease is unpredictable. Colorectal Dis 2007; 9: 567-71.
55. de Diego C, Alcántara M, Valle J, Repiso A, Carrobles JM, Martínez-Castro P,. Influence of smoking habits and CARD15 mutations on the onset of Crohn's disease. Scand J Gastroenterol 2006; 41: 1209-11.
56. Ryan WR, Allan RN, Yamamoto T, Keighley MR,. Crohn's disease patients who quit smoking have a reduced risk of reoperation for recurrence. Am J Surg 2004; 187: 219-25.
57. Cheikh I, Ben Ammar A, Essid M, Azzouz M, Ettahri N, Krichene M, et al,. Treatment and outcome of Crohn's disease without initial complications. Results of a retrospective, multicenter Tunisian study. Tunis Med 2002; 80: 193-8.
58. Lunney PC, Kariyawasam VC, Wang RR, et al,. Smoking prevalence and its influence on disease course and surgery in Crohn's disease and ulcerative colitis. Aliment Pharmacol Ther 2015; 42: 61-70.
59. Mittermaier C, Dejaco C, Waldhoer T, et al,. Impact of depressive mood on relapse in patients with inflammatory bowel disease: a prospective 18-month follow-up study. Psychosom Med 2004; 66: 79-84.
60. Dam AN, Berg AM, Farraye FA,. Environmental influences on the onset and clinical course of Crohn's disease-part 1: an overview of external risk factors. Gastroenterol Hepatol (N Y) 2013; 9: 711-7.
61. Kouvonen A, Kivimäki M, Virtanen M, Pentti J, Vahtera J,. Work stress, smoking status, and smoking intensity: an observational study of 46, 190 employees. J Epidemiol Community Health 2005; 59: 63-9.
62. Khan KJ, Dubinsky MC, Ford AC, Ullman TA, Talley NJ, Moayyedi P,. Efficacy of immunosuppressive therapy for inflammatory bowel disease: a systematic review and meta-analysis. Am J Gastroenterol 2011; 106: 630-42.
63. Ford AC, Sandborn WJ, Khan KJ, Hanauer SB, Talley NJ, Moayyedi P,. Efficacy of biological therapies in inflammatory bowel disease: systematic review and meta-analysis. Am J Gastroenterol 2011a; 106: 644-59, quiz 60.
64. Ramadas AV, Gunesh S, Thomas GA, Williams GT, Hawthorne AB,. Natural history of Crohn's disease in a population-based cohort from Cardiff (1986-2003): a study of changes in medical treatment and surgical resection rates. Gut 2010; 59: 1200-6.
65. Ford AC, Kane SV, Khan KJ, et al,. Efficacy of 5-aminosalicylates in Crohn's disease: systematic review and meta-analysis. Am J Gastroenterol 2011b; 106: 617-29.
66. Ford AC, Bernstein CN, Khan KJ, et al,. Glucocorticosteroid therapy in inflammatory bowel disease: systematic review and meta-analysis. Am J Gastroenterol 2011c; 106: 590-9; quiz 600.
67. Ford AC, Khan KJ, Talley NJ, Moayyedi P,. 5-aminosalicylates prevent relapse of Crohn's disease after surgically induced remission: systematic review and meta-analysis. Am J Gastroenterol 2011d; 106: 413-20.
68. Benjamin JL, Hedin CR, Koutsoumpas A, et al,. Smokers with active Crohn's disease have a clinically relevant dysbiosis of the gastrointestinal microbiota. Inflamm Bowel Dis 2012; 18: 1092-100.
69. Bergeron V, Grondin V, Rajca S, et al,. Current smoking differentially affects blood mononuclear cells from patients with Crohn's disease and ulcerative colitis: relevance to its adverse role in the disease. Inflamm Bowel Dis 2012; 18: 1101-11.
70. Sopori M,. Effects of cigarette smoke on the immune system. Nat Rev Immunol 2002; 2: 372-7.
71. Alegría-Torres JA, Baccarelli A, Bollati V,. Epigenetics and lifestyle. Epigenomics 2011; 3: 267-77.
72. Da Bie C, Hendriks N, Coenen S, et al,. Smoking behaviour and knowledge of the health effects of smoking in patients with inflammatory bowel disease. Aliment Pharmacol Ther 2015; 42: 1294-302.
73. Kennelly RP, Subramaniam T, Egan LJ, Joyce MR,. Smoking and Crohn's disease: active modification of an independent risk factor (education alone is not enough). J Crohns Colitis 2013; 7: 631-5.
74. England PH. Smokefree NHS. Available at: http://www.nhs.uk/smokefree2015 (Accessed July 2015).
75. Das SK,. Harmful health effects of cigarette smoking. Mol Cell Biochem 2003; 253: 159-65.
76. Biedermann L, Fournier N, Misselwitz B, et al,. High rates of smoking especially in female Crohn's disease patients and low use of supportive measures to achieve smoking cessation-data from the Swiss IBD cohort study. J Crohns Colitis 2015; 9: 819-29.
77. Hughes JR, Stead LF, Hartmann-Boyce J, Cahill K, Lancaster T,. Antidepressants for smoking cessation. Cochrane Database Syst Rev 2014; 1: CD000031.
78. Stead LF, Hartmann-Boyce J, Perera R, Lancaster T,. Telephone counselling for smoking cessation. Cochrane Database Syst Rev 2013a; 8: CD002850.
79. Cahill K, Stevens S, Perera R, Lancaster T,. Pharmacological interventions for smoking cessation: an overview and network meta-analysis. Cochrane Database Syst Rev 2013; 5: CD009329.
80. Stead LF, Buitrago D, Preciado N, Sanchez G, Hartmann-Boyce J, Lancaster T,. Physician advice for smoking cessation. Cochrane Database Syst Rev 2013b; 5: CD000165.
81. Coward S, Heitman SJ, Clement F, et al,. Funding a smoking cessation program for Crohn's disease: an economic evaluation. Am J Gastroenterol 2015; 110: 368-77.