Changing incidence of inflammatory bowel disease: Environmental influences and lessons learnt from the South Asian population

Frontiers in Pediatrics

Volumn 1, Issue NOV, 2013, Pages

  Foster, Alice ^a   Jacobson, Kevan ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Environmental factors; Inflammatory bowel disease; South Asian population

Indexed keywords

EID: 84993715808     PISSN: None     EISSN: 22962360     Source Type: Journal    
DOI: 10.3389/fped.2013.00034     Document Type: Review

References (89)

1. Crohn BB. Regional ileitis a pathologic and clinical entity. JAMA (1932) 99(16):1323. doi:10.1001/jama.1932.02740680019005
2. Kirsner JB. Historical aspects of inflammatory bowel disease. J Clin Gastroenterol (1988) 10(3):286-97. doi:10.1097/00004836-198806000-00012
3. Benchimol EI, Fortinsky KJ, Gozdyra P, Van den Heuvel M, Van Limbergen J, Griffiths AM. Epidemiology of pediatric inflammatory bowel disease: a systematic review of international trends. Inflamm Bowel Dis (2011) 17(1):423-39. doi:10.1002/ibd.21349
4. Soon IS, Molodecky NA, Rabi DM, Ghali WA, Barkema HW, Kaplan GG. The relationship between urban environment and the inflammatory bowel diseases: a systematic review and meta-analysis. BMC Gastroenterol (2012) 12(1):51. doi:10.1186/1471-230X-12-51
5. Carr I, Mayberry JF. The effects of migration on ulcerative colitis: a three-year prospective study among Europeans and first-and second-generation South Asians in Leicester (1991-1994). Am J Gastroenterol (1999) 94(10):2918-22. doi:10.1016/S0002-9270(99)00494-3
6. Tsironi E, Feakins RM, Probert CSJ, Roberts CSJ, Rampton DS, Phil D. Incidence of inflammatory bowel disease is rising and abdominal tuberculosis is falling in Bangladeshis in East London, United Kingdom. Am J Gastroenterol (2004) 99(9):1749-55. doi:10.1111/j.1572-0241.2004.30445.x
7. Pinsk V, Lemberg DA, Grewal K, Barker CC, Schreiber RA, Jacobson K. Inflammatory bowel disease in the South Asian pediatric population of British Columbia. Am J Gastroenterol (2007) 102(5):1077-83. doi:10.1111/j.1572-0241.2007.01124.x
8. Fellows IW, Freeman JG, Holmes GK. Crohn's disease in the city of Derby, 1951-85. Gut (1990) 31(11):1262-5. doi:10.1136/gut.31.11.1262
9. Probert CS, Jayanthi V, Pinder D, Wicks AC, Mayberry JF. Epidemiological study of ulcerative proctocolitis in Indian migrants and the indigenous population of Leicestershire. Gut (1992) 33(5):687-93. doi:10.1136/gut.33.5.687
10. Jayanthi V, Probert CS, Pinder D, Wicks AC, Mayberry JF. Epidemiology of Crohn's disease in Indian migrants and the indigenous population in Leicestershire. Q J Med (1992) 82(298):125-38
11. Sood A. Incidence and prevalence of ulcerative colitis in Punjab, North India. Gut (2003) 52(11):1587-90. doi:10.1136/gut.52.11.1587
12. Khosla SN, Girdhar NK, Lal S, Mishra DS. Epidemiology of ulcerative colitis in hospital and select general population of northern India. J Assoc Physicians India (1986) 34(6):405-7
13. Rubin GP, Hungin APS, Kelly PJ, Ling J. Inflammatory bowel disease: epidemiology and management in an English general practice population. Aliment Pharmacol Ther (2000) 14(12):1553-9. doi:10.1046/j.1365-2036.2000.00886.x
14. Loftus CG, Loftus EV Jr, Harmsen WS, Zinsmeister AR, Tremaine WJ, Melton LJ III, 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(3):254-61. doi:10.1002/ibd.20029
15. Bernstein CN, Wajda A, Svenson LW, MacKenzie A, Koehoorn M, Jackson M, et al. The epidemiology of inflammatory bowel disease in Canada: a population-based study. Am J Gastroenterol (2006) 101(7):1559-68. doi:10.1111/j.1572-0241.2006.00603.x
16. Satia JA. Dietary acculturation and the nutrition transition: an overview. Appl Physiol Nutr Metab (2010) 35(2):219-23. doi:10.1139/H10-007
17. Misra A, Rastogi K, Joshi SR. Whole grains and health: perspective for Asian Indians. J Assoc Physicians India (2009) 57:155-62
18. Holmboe-Ottesen G, Wandel M. Changes in dietary habits after migration and consequences for health: a focus on South Asians in Europe. Food Nutr Res (2012) 56:18891. doi:10.3402/fnr.v56i0.18891
19. Sakamoto N, Kono S, Wakai K, Fukuda Y, Satomi M, Shimoyama T, et al. Dietary risk factors for inflammatory bowel disease: a multicenter case-control study in Japan. Inflamm Bowel Dis (2005) 11(2):154-63. doi:10.1097/00054725-200502000-00009
20. Hou JK, Abraham B, El-Serag H. Dietary intake and risk of developing inflammatory bowel disease: a systematic review of the literature. Am J Gastroenterol (2011) 106(4):563-73. doi:10.1038/ajg.2011.44
21. Wandel M, Råberg M, Kumar B, Holmboe-Ottesen G. Changes in food habits after migration among South Asians settled in Oslo: the effect of demographic, socio-economic and integration factors. Appetite (2008) 50(2-3):376-85. doi:10.1016/j.appet.2007.09.003
22. Mellin-Olsen T, Wandel M. Changes in food habits among Pakistani immigrant women in Oslo, Norway. Ethn Health (2005) 10(4):311-39. doi:10.1080/13557850500145238
23. Sevak L, McKeigue PM, Marmot MG. Relationship of hyperinsulinemia to dietary intake in south Asian and European men. Am J Clin Nutr (1994) 59(5):1069-74
24. Lovegrove JA, Lovegrove SS, Lesauvage SV, Brady LM, Saini N, Minihane AM, et al. Moderate fish-oil supplementation reverses low-platelet, long-chain n-3 polyunsaturated fatty acid status and reduces plasma triacylglycerol concentrations in British Indo-Asians. Am J Clin Nutr (2004) 79(6):974-82
25. Donin AS, Nightingale CM, Owen CG, Rudnicka AR, McNamara MC, Prynne CJ, et al. Nutritional composition of the diets of South Asian, black African-Caribbean and white European children in the United Kingdom: the Child Heart and Health Study in England (CHASE). Br J Nutr (2010) 104(2):276-85. doi:10.1017/S000711451000070X
26. Vilaseca J, Salas A, Guarner F, Rodríguez R, Martínez M, Malagelada JR. Dietary fish oil reduces progression of chronic inflammatory lesions in a rat model of granulomatous colitis. Gut (1990) 31(5):539-44. doi:10.1136/gut.31.5.539
27. Monk JM, Hou TY, Turk HF, Weeks B, Wu C, McMurray DN, et al. Dietary n-3 polyunsaturated fatty acids (PUFA) decrease obesity-associated Th17 cell-mediated inflammation during colitis. PLoS One (2012) 7(11):e49739. doi:10.1371/journal.pone.0049739
28. Andoh A, Tsujikawa T, Ishizuka I, Araki Y, Sasaki M, Koyama S, et al. N-3 fatty acid-rich diet prevents early response of interleukin-6 elevation in trinitrobenzene sulfonic acid-induced enteritis. Int J Mol Med (2003) 12(5):721-5
29. Hekmatdoost A, Wu X, Morampudi V, Innis SM, Jacobson K. Dietary oils modify the host immune response and colonic tissue damage following Citrobacter rodentium infection in mice. Am J Physiol Gastrointest Liver Physiol (2013) 304(10):G917-28. doi:10.1152/ajpgi.00292.2012
30. Satish Kumar R, Kanmani P, Yuvaraj N, Paari KA, Pattukumar V, Arul V. Traditional Indian fermented foods: a rich source of lactic acid bacteria. Int J Food Sci Nutr (2013) 64(4):415-28. doi:10.3109/09637486.2012.746288
31. Ceapa C, Wopereis H, Rezaïki L, Kleerebezem M, Knol J, Oozeer R. Influence of fermented milk products, prebiotics and probiotics on microbiota composition and health. Best Pract Res Clin Gastroenterol (2013) 27(1):139-55. doi:10.1016/j.bpg.2013.04.004
32. Ananthakrishnan AN. Environmental risk factors for inflammatory bowel disease. Gastroenterol Hepatol (N Y) (2013) 9(6):367-74
33. Klement E, Cohen RV, Boxman J, Joseph A, Reif S. Breastfeeding and risk of inflammatory bowel disease: a systematic review with meta-analysis. Am J Clin Nutr (2004) 80(5):1342-52
34. Twamley K, Puthussery S, Harding S, Baron M, Macfarlane A. UK-born ethnic minority women and their experiences of feeding their newborn infant. Midwifery (2011) 27(5):595-602. doi:10.1016/j.midw.2010.06.016
35. Innis SM, Dai C, Wu X, Buchan AM, Jacobson K. Perinatal lipid nutrition alters early intestinal development and programs the response to experimental colitis in young adult rats. Am J Physiol Gastrointest Liver Physiol (2010) 299(6):G1376-85. doi:10.1152/ajpgi.00258.2010
36. Innis SM. Polyunsaturated fatty acids in human milk: an essential role in infant development. Adv Exp Med Biol (2004) 554:27-43. doi:10.1007/978-1-4757-4242-8_5
37. Innis SM. Essential fatty acid transfer and fetal development. Placenta (2005) 26(Suppl A):S70-5. doi:10.1016/j.placenta.2005.01.005
38. Jacobson K, Mundra H, Innis SM. Intestinal responsiveness to experimental colitis in young rats is altered by maternal diet. Am J Physiol Gastrointest Liver Physiol (2005) 289(1):G13-20. doi:10.1152/ajpgi.00459.2004
39. Bowen L, Ebrahim S, De Stavola B, Ness A, Kinra S, Bharathi AV, et al. Dietary intake and rural-urban migration in India: a cross-sectional study. PLoS One (2011) 6(6):e14822. doi:10.1371/journal.pone.0014822
40. Ponder A, Long MD. A clinical review of recent findings in the epidemiology of inflammatory bowel disease. Clin Epidemiol (2013) 5:237-47. doi:10.2147/CLEP.S33961
41. Kaplan GG, Hubbard J, Korzenik J, Sands BE, Panaccione R, Ghosh S, et al. The inflammatory bowel diseases and ambient air pollution: a novel association. Am J Gastroenterol (2010) 105(11):2412-9. doi:10.1038/ajg.2010.252
42. Ananthakrishnan AN, McGinley EL, Binion DG, Saeian K. Ambient air pollution correlates with hospitalizations for inflammatory bowel disease: an ecologic analysis. Inflamm Bowel Dis (2011) 17(5):1138-45. doi:10.1002/ibd.21455
43. Strachan DP. Hay fever, hygiene, and household size. BMJ (1989) 299(6710):1259-60. doi:10.1136/bmj.299.6710.1259
44. Yazdanbakhsh M, Matricardi PM. Parasites and the hygiene hypothesis: regulating the immune system? Clin Rev Allergy Immunol (2004) 26(1):15-24. doi:10.1385/CRIAI:26:1:15
45. Feillet H, Bach JF. Increased incidence of inflammatory bowel disease: the price of the decline of infectious burden? Curr Opin Gastroenterol (2004) 20(6):560-4. doi:10.1097/00001574-200411000-00010
46. Bernstein CN, Rawsthorne P, Cheang M, Blanchard JF. A population-based case control study of potential risk factors for IBD. Am J Gastroenterol (2006) 101(5):993-1002. doi:10.1111/j.1572-0241.2006.00381.x
47. Gent AE, Hellier MD, Grace RH, Swarbrick ET, Coggon D. Inflammatory bowel disease and domestic hygiene in infancy. Lancet (1994) 343(8900):766-7. doi:10.1016/S0140-6736(94)91841-4
48. Wang TT, Dabbas B, Laperriere D, Bitton AJ, Soualhine H, Tavera-Mendoza LE, et al. Direct and indirect induction by 1,25-dihydroxyvitamin D3 of the NOD2/CARD15-defensin beta2 innate immune pathway defective in Crohn disease. J Biol Chem (2010) 285(4):2227-31. doi:10.1074/jbc.C109.071225
49. Lim W-C, Hanauer SB, Li YC. Mechanisms of disease: vitamin D and inflammatory bowel disease. Nat Clin Pract Gastroenterol Hepatol (2005) 2(7):308-15. doi:10.1038/ncpgasthep0215
50. Pappa HM, Grand RJ, Gordon CM. Report on the vitamin D status of adult and pediatric patients with inflammatory bowel disease and its significance for bone health and disease. Inflamm Bowel Dis (2006) 12(12):1162-74. doi:10.1097/01.mib.0000236929.74040.b0
51. Katz S. Osteoporosis in patients with inflammatory bowel disease: risk factors, prevention, and treatment. Rev Gastroenterol Disord (2006) 6(2):63-71
52. Fu YT, Chatur N, Cheong-Lee C, Salh B. Hypovitaminosis D in adults with inflammatory bowel disease: potential role of ethnicity. Dig Dis Sci (2012) 57(8):2144-8. doi:10.1007/s10620-012-2130-7
53. Froicu M, Weaver V, Wynn TA, McDowell MA, Welsh JE, Cantorna MT. A crucial role for the vitamin D receptor in experimental inflammatory bowel diseases. Mol Endocrinol (2003) 17(12):2386-92. doi:10.1210/me.2003-0281
54. Bhalla AK, Amento EP, Clemens TL, Holick MF, Krane SM. Specific high-affinity receptors for 1,25-dihydroxyvitamin D3 in human peripheral blood mononuclear cells: presence in monocytes and induction in T lymphocytes following activation. J Clin Endocrinol Metab (1983) 57(6):1308-10. doi:10.1210/jcem-57-6-1308
55. Provvedini DM, Tsoukas CD, Deftos LJ, Manolagas SC. 1,25-Dihydroxyvitamin D3 receptors in human leukocytes. Science (1983) 221(4616):1181-3. doi:10.1126/science.6310748
56. Manolagas SC, Provvedini DM, Murray EJ, Tsoukas CD, Deftos LJ. The antiproliferative effect of calcitriol on human peripheral blood mononuclear cells. J Clin Endocrinol Metab (1986) 63(2):394-400. doi:10.1210/jcem-63-2-394
57. Brennan A, Katz DR, Nunn JD, Barker S, Hewison M, Fraher LJ, et al. Dendritic cells from human tissues express receptors for the immunoregulatory vitamin D3 metabolite, dihydroxycholecalciferol. Immunology (1987) 61(4):457-61
58. Veldman CM, Cantorna MT, DeLuca HF. Expression of 1,25-dihydroxyvitamin D(3) receptor in the immune system. Arch Biochem Biophys (2000) 374(2):334-8. doi:10.1006/abbi.1999.1605
59. D'Ambrosio D, Cippitelli M, Cocciolo MG, Mazzeo D, Di Lucia P, Lang R, et al. Inhibition of IL-12 production by 1,25-dihydroxyvitamin D3. Involvement of NF-kappaB downregulation in transcriptional repression of the p40 gene. J Clin Invest (1998) 101(1):252-62. doi:10.1172/JCI1050
60. Rigby WF, Stacy T, Fanger MW. Inhibition of T lymphocyte mitogenesis by 1,25-dihydroxyvitamin D3 (calcitriol). J Clin Invest (1984) 74(4):1451-5. doi:10.1172/JCI111557
61. Jørgensen SP, Agnholt J, Glerup H, Lyhne S, Villadsen GE, Hvas CL, et al. Clinical trial: vitamin D3 treatment in Crohn's disease-a randomized double-blind placebo-controlled study. Aliment Pharmacol Ther (2010) 32(3):377-83. doi:10.1111/j.1365-2036.2010.04355.x
62. Cantorna MT, Munsick C, Bemiss C, Mahon BD. 1,25-Dihydroxycholecalciferol prevents and ameliorates symptoms of experimental murine inflammatory bowel disease. J Nutr (2000) 130(11):2648-52
63. Denson LA, Long MD, McGovern DP, Kugathasan S, Wu GD, Young VB, et al. Challenges in IBD research: update on progress and prioritization of the CCFA's research agenda. Inflamm Bowel Dis (2013) 19(4):677-82. doi:10.1097/MIB.0b013e31828134b3
64. Ventham NT, Kennedy NA, Nimmo ER, Satsangi J. Beyond gene discovery in inflammatory bowel disease: the emerging role of epigenetics. Gastroenterology (2013) 145(2):293-308. doi:10.1053/j.gastro.2013.05.050
65. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature (2012) 491(7422):119-24. doi:10.1038/nature11582
66. Brant SR. Promises, delivery, and challenges of inflammatory bowel disease risk gene discovery. Clin Gastroenterol Hepatol (2013) 11(1):22-6. doi:10.1016/j.cgh.2012.11.001
67. Luther J, Dave M, Higgins PDR, Kao JY. Association between Helicobacter pylori infection and inflammatory bowel disease: a meta-analysis and systematic review of the literature. Inflamm Bowel Dis (2010) 16(6):1077-84. doi:10.1002/ibd.21116
68. Feeney MA, Murphy F, Clegg AJ, Trebble TM, Sharer NM, Snook JA. A case-control study of childhood environmental risk factors for the development of inflammatory bowel disease. Eur J Gastroenterol Hepatol (2002) 14(5):529-34. doi:10.1097/00042737-200205000-00010
69. Koloski NA. Hygiene hypothesis in inflammatory bowel disease: a critical review of the literature. World J Gastroenterol (2008) 14(2):165. doi:10.3748/wjg.14.165
70. Hunter MM, McKay DM. Review article: helminths as therapeutic agents for inflammatory bowel disease. Aliment Pharmacol Ther (2004) 19(2):167-77. doi:10.1111/j.0269-2813.2004.01803.x
71. Summers RW, Elliott DE, Urban JF, Thompson RA, Weinstock JV. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology (2005) 128(4):825-32. doi:10.1053/j.gastro.2005.01.005
72. Cornish JA, Tan E, Simillis C, Clark SK, Teare J, Tekkis PP. The risk of oral contraceptives in the etiology of inflammatory bowel disease: a meta-analysis. Am J Gastroenterol (2008) 103(9):2394-400. doi:10.1111/j.1572-0241.2008.02064.x
73. Khalili H, Higuchi LM, Ananthakrishnan AN, Richter JM, Feskanich D, Fuchs CS, et al. Oral contraceptives, reproductive factors and risk of inflammatory bowel disease. Gut (2013) 62(8):1153-9. doi:10.1136/gutjnl-2012-302362
74. Cutolo M, Capellino S, Montagna P, Ghiorzo P, Sulli A, Villaggio B. Sex hormone modulation of cell growth and apoptosis of the human monocytic/macrophage cell line. Arthritis Res Ther (2005) 7(5):R1124-32. doi:10.1186/ar1791
75. Williamson LM, Parkes A, Wight D, Petticrew M, Hart GJ. Limits to modern contraceptive use among young women in developing countries: a systematic review of qualitative research. Reprod Health (2009) 6:3. doi:10.1186/1742-4755-6-3
76. Schultsz C, Van Den Berg FM, Ten Kate FW, Tytgat GN, Dankert J. The intestinal mucus layer from patients with inflammatory bowel disease harbors high numbers of bacteria compared with controls. Gastroenterology (1999) 117(5):1089-97. doi:10.1016/S0016-5085(99)70393-8
77. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut (2006) 55(2):205-11. doi:10.1136/gut.2005.073817
78. Pils MC, Bleich A, Prinz I, Fasnacht N, Bollati-Fogolin M, Schippers A, et al. Commensal gut flora reduces susceptibility to experimentally induced colitis via T-cell-derived interleukin-10. Inflamm Bowel Dis (2011) 17(10):2038-46. doi:10.1002/ibd.21587
79. Sellon RK, Tonkonogy S, Schultz M, Dieleman LA, Grenther W, Balish E, et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun (1998) 66(11):5224-31
80. Yang I, Eibach D, Kops F, Brenneke B, Woltemate S, Schulze J, et al. Intestinal microbiota composition of interleukin-10 deficient C57BL/6J mice and susceptibility to Helicobacter hepaticus-induced colitis. PLoS One (2013) 8(8):e70783. doi:10.1371/journal.pone.0070783
81. Card T. Antibiotic use and the development of Crohn's disease. Gut (2004) 53(2):246-50. doi:10.1136/gut.2003.025239
82. Shaw SY, Blanchard JF, Bernstein CN. Association between the use of antibiotics in the first year of life and pediatric inflammatory bowel disease. Am J Gastroenterol (2010) 105(12):2687-92. doi:10.1038/ajg.2010.398
83. Shaw SY, Blanchard JF, Bernstein CN. Association between the use of antibiotics and new diagnoses of Crohn's disease and ulcerative colitis. Am J Gastroenterol (2011) 106(12):2133-42. doi:10.1038/ajg.2011.304
84. Albenberg LG, Lewis JD, Wu GD. Food and the gut microbiota in inflammatory bowel diseases: a critical connection. Curr Opin Gastroenterol (2012) 28(4):314-20. doi:10.1097/MOG.0b013e328354586f
85. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature (2012) 489(7415):220-30. doi:10.1038/nature11550
86. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A (2010) 107(33):14691-6. doi:10.1073/pnas.1005963107
87. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science (2011) 334(6052):105-8. doi:10.1126/science.1208344
88. Hehemann JH, Kelly AG, Pudlo NA, Martens EC, Boraston AB. Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc Natl Acad Sci U S A (2012) 109(48):19786-91. doi:10.1073/pnas.1211002109
89. Deatherage Kaiser BL, Li J, Sanford JA, Kim YM, Kronewitter SR, Jones MB, et al. A multi-omic view of host-pathogen-commensal interplay in Salmonella-mediated intestinal infection. PLoS One (2013) 8(6):e67155. doi:10.1371/journal.pone.0067155