Latitude, sunshine, and human lactase phenotype distributions may contribute to geographic patterns of modern disease: The inflammatory bowel disease model

Clinical Epidemiology

Volumn 6, Issue 1, 2014, Pages 183-198

  Szilagyi, Andrew ^a   Leighton, Henry ^b   Burstein, Barry ^a   Xue, Xiaoqing ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Evolution; Inflammatory bowel disease; Lactase; Latitude; Ultraviolet B exposure

Indexed keywords

LACTASE; LACTASE NON PERSISTENCE; UNCLASSIFIED DRUG;

ARTICLE; CROHN DISEASE; DAIRY PRODUCT; ENVIRONMENTAL FACTOR; ENZYME LOCALIZATION; FOOD INTAKE; GENE MUTATION; GEOGRAPHIC DISTRIBUTION; HUMAN; INFLAMMATORY BOWEL DISEASE; LATITUDE; LIFESTYLE; LONGITUDE; MATHEMATICAL ANALYSIS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHENOTYPE; POISSON DISTRIBUTION; RADIATION EXPOSURE; SIGNAL TRANSDUCTION; SOCIOECONOMICS; SUN EXPOSURE; ULCERATIVE COLITIS; ULTRAVIOLET B RADIATION;

EID: 84901641094     PISSN: None     EISSN: 11791349     Source Type: Journal    
DOI: 10.2147/CLEP.S59838     Document Type: Article

References (108)

1. Swallow DM. Genetics of lactase persistence and lactose intolerance. Ann Hum Genet. 2003;37(4):197-219.
2. Kruse TA, Bolund L, Grzeschik KH, etal. The human lactase-phlorizin gene is located on chromosome 2. FEBS Lett. 1988;240(1-2):123-126.
3. Enattah NS, Sahi T, Savilahti E, etal. Identification of a variant associated with adult-type hypolactasia. Nat Genet. 2002;30(2):233-237.
4. Tishkoff SA, Reed FA, Ranciaro A, etal. Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet. 2007;39(1):31-40.
5. Jones BL, Swallow DM. The impact of cis-acting polymorphisms on the human phenotype. Hugo J. 2011;5(1-4):13-23.
6. Forster P, Matsumura S. Did early humans go north or south? Science. 2005;308(5724):965-966.
7. Burger J, Kirchner M, Bramanti B, Haak W, Thomas MG. Absence of the lactase-persistence-associated allele in early Neolithic Europeans. Proc Natl Acad Sci U S A. 2007;104(10):3736-3741.
8. Itan Y, Powell A, Beaumont MA, Burger J, Thomas MG. The origins of lactase persistence in Europe. PLoS One Comput Biol. 2009;5(8): e1000491.
9. Gerbault P, Moret C, Currat M, Sanchez-Mazas A. Impact of selection and demography on the diffusion of lactase persistence. PLoS One. 2009;4(7):e6369.
10. Simoons FJ. Primary adult lactose intolerance and the milking habit: a problem in biologic and cultural interrelations. II. A culture historical hypothesis. Am J Dig Dis. 1970;15(8):695-710.
11. Cramer DW, Xu H. Lactase persistence, galactose metabolism and milk consumption as risk factors for ovarian cancer. In: Aurichio S, Semenza G, editors. Common Food Intolerances 2: Milk in Human Nutrition and Adult-Type Hypolactasia. Basel, Switzerland: Karger; 1993.
12. Nanji AA, Denardi FG. Primary adult lactose intolerance protects against development of inflammatory bowel disease. Med Hypotheses. 1986;19(1):1-6.
13. Shrier I, Szilagyi A, Correa JA. Impact of lactose containing foods and the genetics of lactase on diseases: an analytical review of population data. Nutr Cancer. 2008;60(3):292-300.
14. Grant WB. A meta-analysis of second cancers after a diagnosis of non-melanoma skin cancer: additional evidence that solar ultraviolet-B irradiance reduces the risk of internal cancers. J Steroid Biochem Mol Biol. 2007;103(3-5):668-674.
15. Grant WB. How strong is the evidence that solar ultraviolet B and vitamin D reduce the risk of cancer? Dermatoendocrinol. 2009;1(1): 17-24.
16. van Leeuwen MT, Turner JJ, Falster MO, etal. Latitude gradients for lymphoid neoplasm subtypes in Australia support an association with ultraviolet radiation exposure. Int J Cancer. 2013;133(4):944-951.
17. Mohr SB, Garland CF, Gorham ED, Grant WB, Garland FC. Ultraviolet light B and incidence rates of leukemia worldwide. Am J Prev Med. 2011;41(1):68-74.
18. Simpson S Jr, Blizzard L, Otahal P, Van der Mei I, Taylor B. Latitude is significantly associated with the prevalence of multiple sclerosis: a meta-analysis. J Neurol Neurosurg Psychiatry. 2011;82(10):1132-1141.
19. Ananathakrishnan AN, Khalili H, Higuchi LM, etal. Higher predicted vitamin D status is associated with reduced risk of Crohn's disease. Gastroenterology. 2012;142(3):482-489.
20. Peyrin-Biroulet L, Oussalah A, Bigard M-A. Crohn's disease: the hot hypothesis. Med Hypotheses. 2009;73(1):94-96.
21. Shivinanda S, Lennard-Jones J, Logan R, etal. Incidence of inflammatory bowel disease across Europe: is there a difference between north and south? Results of the European Collaborative Study on Inflammatory Bowel Disease (EC-IBD). Gut. 1996;39(5):690-697.
22. Juste RA. Crohn's disease and ruminant farming. Got lactase? Med Hypotheses. 2010;75(1):7-13.
23. Molodecky NA, Soon IS, Rabi D, etal. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on a systematic review. Gastroenterology. 2012;142(1):46-54.
24. Itan Y, Jones BL, Ingram CJE, Swallow DM, Thomas MG. A worldwide correlation of lactase persistence phenotype and genotypes. BMC Evol Biol. 2010;10:36.
25. Szilagyi A. Determinants of geographic patterns of diseases: interaction of lactose/lactase status and sunshine exposure. Med Hypotheses. 2010;75(5):466-470.
26. Bernstein CN, Shanahan F. Disorders of a modern lifestyle: reconciling the epidemiology of inflammatory bowel diseases. Gut. 2008;57(9): 1185-1191.
27. Economou M, Pappas G. New global map of Crohn's disease: genetic, environmental, and socioeconomic correlations. Inflamm Bowel Dis. 2008;14(5):709-720.
28. Thia KT, Loftus EV, Sandborn WJ, Yang S-K. An update on the epidemiology of inflammatory bowel disease in Asia. Am J Gastroenterol. 2008;103(12):3167-3182.
29. Lakatos L, Lakatos PL. Is the incidence and prevalence of inflammatory bowel diseases increasing in Eastern Europe? Postgrad Med J. 2006;82(967):332-337.
30. Sahi T. Genetics and epidemiology of adult-type hypolactasia. Scand J Gastroenterol. 1994;29 Suppl 202:S7-S20.
31. Scrimshaw N, Murray EB. The acceptability of milk and milk products in populations with a high prevalence of lactose intolerance. Am J Clin Nutr. 1988;48 Suppl 4:S1083-S1159.
32. Figueroa CC, Quera PR, Valenzuela EJ, Jensen BC. Enfermedades inflamatorias intestinales: Experiencia de dos centros chilenos. [Inflammatory bowel disease: experience of two Chilean centers]. Rev Med Chil. 2005;133(11):1295-1304. Spanish.
33. Hilmi I, Singh R, Ganesananthan S, etal. Demography and clinical course of ulcerative colitis in a multiracial Asian population: a nationwide study from Malaysia. J Dig Dis. 2009;10(1):15-20.
34. Chua KH, Hilmi I, Ng CC, etal. Identification of NOD2/CARD15 mutations in Malaysian patients with Crohn's disease. J Dig Dis. 2009;10(2):124-130.
35. Coelho M, Luiselli Bertorelle G, Lopes AI, Seixas S, Destro-Bisol G, Rocha J. Microsatellite variation and evolution of human lactase persistence. Hum Genet. 2005;117(4):329-339.
36. Blomme B, Gerlo E, Hauser B, Vandenplas Y. Disaccharidase activities in Belgian children: reference intervals and comparison with non-Belgian Caucasian children. Acta Pediatr. 2003;92(7):806-810.
37. Timpson NJ, Brennan P, Gaborieau V, etal. Can lactase persistence genotype be used to reassess the relationship between renal cell carcinoma and milk drinking? Potentials and problems in the application of Mendelian randomization. Cancer Epidemiol Biomarkers Prev. 2010;19(5):1341-1348.
38. Weinberg RB. Apolipoprotein A-IV-2 allele: association of its worldwide distribution with adult persistence of lactase and speculation on its function and origin. Genet Epidemiol. 1999;17(4):285-297.
39. Lee-Taylor J, Madronich S. Climatology of UV-A, UV-B, and Erythemal Radiation at the Earth's Surface, 1979-2000. Technical Note TN-474+STR. Boulder, CO, USA: National Center for Atmospheric Research; 2007.
40. Ennattah NS, Kuokkanen M, Forsblom C, etal. Correlation of intestinal disaccharidase activities with the C/T-13910 variant and age. World J Gastroenterol. 2007;13(25):3508-3512.
41. Marton A, Xue X, Szilagyi A. Meta-analysis: the diagnostic accuracy of lactose breath hydrogen or lactose tolerance tests for predicting the North European lactase polymorphism C/T-13910. Aliment Pharmacol Ther. 2012;35(4):429-440.
42. Vahedi H, Merat S, Momtahen S, etal. Epidemiologic characteristics of 500 patients with inflammatory bowel disease in Iran studied from 2004 through 2007. Arch Iran Med. 2009;12(5):454-460.
43. Zouiten-Mekki L, Zaouali H, Boubaker J, etal. Card15/Nod2 in a Tunisian population with Crohn's disease. Dig Dis Sci. 2005;50(1): 130-135.
44. Petritsch W, Fuchs S, Berghold A, etal. Incidence of inflammatory bowel disease in the province of Styria, Austria, from 1997 to 2007: a population-based study. J Crohns Colitis. 2013;7(1):58-69.
45. Jussila A, Virta LJ, Kautiainen H, etal. Increasing incidence of inflammatory bowel diseases between 2000 and 2007: a nationwide register study in Finland. Inflamm Bowel Dis. 2012;18(3):555-561.
46. Kiudelis G, Zvirbytiene A, Sventoraitye J, Kupecnikas L. Referral epidemiology of ulcerative colitis and Crohn's disease in Kaunas region Lithuania: one year prospective study. J Crohns Colitis. 2008;2 Suppl 1:S70.
47. Yammamoto-Furusho JK. Clinical epidemiology of ulcerative colitis in Mexico: a single hospital-based study in a 20-year period (1987-2006). J Clin Gastroenterol. 2009;43(3):221-224.
48. Fadda MA, Peedikayil MC, Kagevi I, Kahtani KA, Ben AA, Al HI. Inflammatory bowel disease in Saudi Arabia: a hospital-based clinical study of 312 patients. Ann Saudi Med. 2012;32(3):276-282.
49. Buenavida G, Casañias A, Vásquez C, etal. National Inflammatory Bowel Disease Registry. Acta Gastroenterol Latinoam. 2011;41(4): 281-287.
50. Wang YG, Yan YS, Xu JJ, Du RF, Kuhnau W, Flatz G. Prevalence of primary adult lactose malabsorption in three populations of northern China. Hum Genet. 1984;67(1):103-106.
51. Ladas S, Papanikos J, Arapakis G. Lactose malabsorption in Greek adults: correlation of small bowel transit time with the severity of lactose intolerance. Gut. 1982;23(11):968-973.
52. Sadre M, Karbasi K. Lactose intolerance in Iran. Am J Clin Nutr. 1979;32(9):1948-1954.
53. Nose O, Iida Y, Kai H, Harada T, Ogawa M, Yabuuchi H. Breath hydrogen test for detecting lactose malabsorption in infants and children. Prevalence of lactose malabsorption in Japanese children and adults. Arch Dis Child. 1979;54(6):436-440.
54. Nasrallah SM. Lactose intolerance in the Lebanese population and in Mediterranean lymphoma. Am J Clin Nutr. 1979;32(10):1994-1996.
55. Aswami MZ, Seppo L, Vapaatalo H, Korpela R. Hypolactasia and lactose intolerance among three ethnic groups of Malaysia. Indian J Med Res. 2006;124(6):697-704.
56. Senewiratne B, Thambipillai S, Pereira H. Intestinal lactase deficiency in Ceylon (Sri Lanka). Gastroenterology. 1977;72(6):1257-1259.
57. Filali A, Hassine B, Dhouib H, Matri S, Ben Ammar A, Garoui H. Study of malabsorption of lactose by the hydrogen breath test in a population of 70 Tunisian adults. Gastroenterol Clin Biol. 1987;11(8-9):554-557.
58. Flatz G, Henze HJ, Palabiyikoglu E, Dagalp K, Turkkan T. Distribution of the adult lactase phenotypes in Turkey. Trop Geogr Med. 1986;38(3): 255-258.
59. Bolin TD, Morrison RM, Steel JE, Davis AE. Lactose intolerance in Australia. Med J Aust. 1970;1(26):1289-1292.
60. Lember M, Torniainen S, Kull M, etal. Lactase non-persistence and milk consumption in Estonia. World J Gastroenterol. 2006;12(45): 7329-7331.
61. Abbott WG, Tasman-Jones C. Incidence of acquired primary hypolactasia in three New Zealand racial groups. N Z Med J. 1985;98(776):228-229.
62. Farup PG, Monsbakken KW, Vandvik PO. Lactose malabsorption in a population with irritable bowel syndrome: prevalence and symptoms. A case-control study. Scand J Gastroenterol. 2004;39(7):645-649.
63. Kuokkanen M, Butzow R, Rasinpera H, etal. Lactase and ovarian carcinoma risk in Finland, Poland and Sweden. Int J Cancer. 2005;117(1):90-94.
64. Mattar R, Monteiro MS, Villares CA, Santos AF, Silva JM, Carrilho FJ. Frequency of LCT-13910C. T single nucleotide polymorphism associated with adult-type hypolactasia/lactase persistence among Brazilians of different ethnic groups. Nutr J. 2009;8:46.
65. Czeizel A, Flatz G, Flatz SD. Prevalence of primary adult lactose malabsorption in Hungary. Hum Genet. 1983;64(4):398-401.
66. Babu J, Kumar S, Babu P, Prasad JH, Ghoshal UC. Frequency of lactose malabsorption among healthy southern and northern Indian populations by genetic analysis and lactose hydrogen breath and tolerance tests. Am J Clin Nutr. 2010;91(1):140-146.
67. Al-Sanae H, Saldanha W, Sugathan TN, Majid Molla A. Comparison of lactose intolerance in healthy Kuwaiti and Asian volunteers. Med Princ Pract. 2003;12(3):160-163.
68. Khabarova YA, Torniainen ST, Nurmi HA, Jarvela IE, Isokoski MK, Mattila KJ. Prevalence of lactase persistent/non-persistent genotypes and milk consumption in young population in north-west Russia. World J Gastroenterol. 2009;15(15):1849-1853.
69. Socha J, Ksiazyk J, Flatz G, Flatz SD. Prevalence of primary adult lactose malabsorption in Poland. Ann Hum Biol. 1984;11(4): 311-316.
70. Maggi R, Sayagues B, Fernandez A, etal. Lactose malabsorption and intolerance in Uruguayan population by breath hydrogen test (H2). J Pediatr Gastroenterol Nutr. 1987;6(3):373-376.
71. Ng SC, Bernstein CN, Vatn MH, etal. Geographical variability and environmental risk factors in inflammatory bowel disease. Gut. 2013;62(4):630-649.
72. Nerich V, Monnet E, Weill A, etal. Fine scale geographic variations of inflammatory bowel disease in France: correlation with socioeconomic and house equipment variables. Inflamm Bowel Dis. 2010;16(5):813-821.
73. Armitage EL, Aldhous MC, Anderson N, etal. Incidence of juvenile-onset Crohn's disease in Scotland: association with northern latitude and affluence. Gastroenterology. 2004;127(4):1051-1057.
74. Sonnenberg A, McCarty DJ, Jacobsen SJ. Geographic variation of inflammatory bowel disease within the United States. Gastroenterology. 1991;100(1):143-149.
75. Khalili H, Huang ES, Ananthakrishnan AN, etal. Geographical variation and incidence of inflammatory bowel disease among US women. Gut. 2012;61(12):1686-1692.
76. Bernstein CN, Wajda A, Svenson LW, etal. The epidemiology of inflammatory bowel disease in Canada: a population based study. Am J Gastroenterol. 2006;101(7):1559-1568.
77. Jussila A, Virta LJ, Salomaa V, Maki J, Jula A, Farkkila MA. High and increasing prevalence of inflammatory bowel disease in Finland with a clear north-south difference. J Crohns Colitis. 2013;7(7):e256-e262.
78. Sonnenberg A. Time trends of mortality from Crohn's disease and ulcerative colitis. Int J Epidemiol. 2007;36(4):890-899.
79. Garg M, Lubel JS, Sparrow MP, Holt SG, Gibson PR. Review article: vitamin D and inflammatory bowel disease-established concepts and future directions. Aliment Pharmacol Ther. 2012;36(4):324-344.
80. Jorgensen SP, Agnholt J, Glerup H, etal. Clinical trial: vitamin D3 treatment in Crohn's disease-a randomized double-blind placebo-controlled study. Aliment Pharmacol Ther. 2010;32(3):377-383.
81. Cantorna MT, Mahon BD. Mounting evidence for vitamin D as an environmental factor affecting autoimmune disease prevalence. Exp Biol Med (Maywood). 2004;229(11):1136-1142.
82. Holick MF, Chen TC, Lu Z, Sauter E. Vitamin D and skin physiology: a D-lightful story. J Bone Miner Res. 2007;22 Suppl 2:V28-V33.
83. Aamodt G, Bengtson MB, Vatn MH. Can temperature explain the latitudinal gradient of ulcerative colitis? Cohort of Norway. BMC Public Health. 2013;13:530.
84. Murdoch TB, Bernstein CN, El-Gabalawy H, etal. Prevalence of genetic variants associated with inflammatory bowel disease in a healthy First Nations cohort. CMAJ. 2012;184(8):E435-E441.
85. Shapira M, Tamir A. Crohn's disease in the Kinneret sub-district, Israel, 1960-1990. Incidence and prevalence in different ethnic subgroups. Eur J Epidemiol. 1994;10(2):231-233.
86. Gearry RB, Lea RA, Roberts RL, Chambers GK, Barclay ML, Kennedy MA. CARD15 allele frequency differences in New Zealand Maori: ancestry specific susceptibility to Crohn's disease in New Zealand? Gut. 2006;55(4):580.
87. Flatz G, Rotthauwe HW. Lactose nutrition and natural selection. Lancet. 1973;2(7820):76-77.
88. Heyer E, Brazier L, Segurel L, etal. Lactase persistence in central Asia: phenotype, genotype, and evolution. Hum Biol. 2011;83(3):379-392.
89. Gallego Romero I, Basu Mallick C, Liebert A, etal. Herders of Indian and European cattle share their predominant allele for lactase persistence. Mol Biol Evol. 2012;29(1):249-260.
90. Szilagyi A, Leighton H, Burstein B, Shrier I. Significant positive correlation between sunshine and lactase nonpersistence in Europe may implicate both in similarly altering risks for some diseases. Nutr Cancer. 2011;63(7):991-999.
91. Szilagyi A. Lactose: a potential prebiotic. Aliment Pharmacol Ther. 2002;16(9):1591-1602.
92. Szilagyi A, Nathwani U, Vinokuroff C, Correa JA, Shrier I. The effect of lactose maldigestion on the relationship between dairy food intake and colorectal cancer: a systematic review. Nutr Cancer. 2006;55(2): 141-150.
93. Spooren CE, Pierik MJ, Zeegers MP, Feskens EJ, Masclee AA, Jonkers DM. Review article: the association of diet with onset and relapse in patients with inflammatory bowel disease. Aliment Pharmacol Ther. 2013;38(10):1172-1187.
94. Abubakar I, Myhill DJ, Hart AR, etal. A case control study of drinking water and dairy products in Crohn's disease: further investigation of the possible role of Mycobacterium avium paratuberculosis. Am J Epidemiol. 2007;165(7):776-783.
95. Alfonso-Sanchez MA, Perez-Miranda AM, Garcia-Obregon S, Pena JA. An evolutionary approach to the high frequency of the delta F508 CFTR mutation in European populations. Med Hypotheses. 2010;74(6):989-992.
96. Gasche C, Nemeth M, Grundtner P, Willheim-Polli C, Ferenci P, Schwarzenbacher R. Evolution of Crohn's disease-associated Nod2 mutations. Immunogenetics. 2008;60(2):115-120.
97. Wang TT, Dabbas B, Laperriere D, etal. Direct and indirect induction by 1,25-dihydroxyvitamin D3 of the NOD2/CARD15-defensin β2 innate immune pathway defective in Crohn's disease. J Biol Chem. 2010;285(4):2227-2231.
98. Modiano G, Ciminellui BM, Pignatti PF. Cystic fibrosis and lactase persistence: a possible correlation. Eur J Hum Genet. 2007;15(3): 255-259.
99. Bresso F, Askling J, Astegiano M, etal. Potential role for the common cystic fibrosis ΔF508 mutation in Crohn's disease. Inflamm Bowel Dis. 2007;13(5):531-536.
100. Bahmanyar S, Ekbom A, Askling J, Johanneson M, Montgomery SM. Cystic fibrosis gene mutations and gastrointestinal disease. J Cyst Fibros. 2010;9(4):288-291.
101. Buning C, Ockenga JK, Jurga J, etal. The C/C(-13910) and G/G9-22018) genotypes for adult-type hypolactasia are not associated with inflammatory bowel disease. Scand J Gastroenterol. 2003;38(5): 538-542.
102. Elguezabal N, Chamorro S, Molina E, etal. Lactase persistence, NOD2 status and Mycobacterium avium subsp. Paratuberculosis infection associations to inflammatory bowel disease. Gut Pathog. 2012;4(1):6.
103. Nolan DJ, Han DY, Lam WJ, etal. Genetic adult lactase persistence is associated with risk of Crohn's disease in a New Zealand population. BMC Res Notes. 2010;3:339.
104. Juste RA, Elguezabal N, Chamorro S, etal. Associations between CARD15 polymorphisms, MAPDNA in blood and lactase persistence in a Crohn's disease case-control study in north Spain. Proceedings of the Tenth International Colloquium on Paratuberculosis. 2009; 269(2):9-14.
105. Lees CW, Barrett JC, Parkes M, Satsangi J. New IBD genetics: common pathways with other diseases. Gut. 2011;60(12):1739-1753.
106. Bernstein CN, Kraut A, Blanchard JF, Rawsthorne P, Yu N, Walld R. The relationship between inflammatory bowel disease and socioeconomic variables. Am J Gastroenterol. 2001;96(7):2117-2125.
107. Ross AG, Olds GR, Cripps AW, Farrar JJ, McManus DP. Enteropathogens and chronic illness in returning travelers. N Engl J Med. 2013;368(19):1817-1825.
108. Okada H, Kuhn C, Feillet H, Bach J-F. The 'hygiene hypothesis' for autoimmune and allergic diseases: an update. Clin Exp Immunol. 2010;160(1):1-9.