Advertisement

European Journal of Nutrition

, Volume 49, Issue 3, pp 141–146 | Cite as

Associations between lactase persistence and the metabolic syndrome in a cross-sectional study in the Canary Islands

  • Ricardo Almon
  • Eva E. Álvarez-Leon
  • Peter Engfeldt
  • Lluís Serra-Majem
  • Anders Magnuson
  • Torbjörn K. Nilsson
Original Contribution

Abstract

Background

The single nucleotide polymorphism (SNP) LCT −13910 C>T, associated with genetically determined phenotypes of lactase persistence (LP) or non-persistence (LNP), was studied in relation to the metabolic syndrome (MS).

Aim of the study

The aim was to determine if milk intake and MS are associated. We applied Mendelian randomization (MR). The SNP, LCT −13910 C>T, with the genotypes LP (TT/CT) and LNP (CC), was taken as a proxy for milk consumption.

Methods

A representative sample of adults belonging to the Canary Islands Nutrition Survey (ENCA) in Spain aged 18–75 years (n = 551) was genotyped for the LCT −13910 C>T polymorphism. We used the International Diabetes Federation (IDF) criteria to define MS.

Results

60% of the population was LP and 40% LNP. One hundred seven LP subjects (35.0%) and 53 LNP subjects (25.6%) showed MS (χ 2 = 5.04, p = 0.025). LP subjects showed a significantly higher odds ratio (OR) for MS than LNP subjects computed for the whole population: both the crude OR (1.56; 95% CI 1.06–2.31) and adjusted OR for sex, age, daily energy intake, physical activity and educational level (1.57; 95% CI 1.02–2.43). Adjusted OR for women with LP was 1.93; 95% CI 1.06–3.52.

Conclusions

The T allele of the SNP might constitute a nutrigenetic factor increasing the susceptibility of LP subjects, especially women, to develop MS in the Canary Islands.

Keywords

LCT −13910 C>T polymorphism Metabolic syndrome Milk Mendelian randomization Nutrigenetics 

Notes

Acknowledgments

The Spanish Canarian Health Service supported the Canary Islands Nutrition Survey (ENCA). The present work was also supported by the Örebro County Council, Sweden. We are thankful to Lewis Burgess, Ph.D., applied anthropologist in New York City, for revising the manuscript.

References

  1. 1.
    Adebamowo CA, Spiegelman D, Berkey CS, Danby FW, Rockett HH, Colditz GA, Willett WC, Holmes MD (2008) Milk consumption and acne in teenaged boys. J Am Acad Dermatol 58:794–795CrossRefGoogle Scholar
  2. 2.
    Alberti KG, Zimmet P, Shaw J (2006) Metabolic syndrome—a new world-wide definition. A consensus statement from the International Diabetes Federation. Diabet Med 23:469–480CrossRefGoogle Scholar
  3. 3.
    Almon R, Engfeldt P, Tysk C, Sjostrom M, Nilsson TK (2007) Prevalence and trends in adult-type hypolactasia in different age cohorts in Central Sweden diagnosed by genotyping for the adult-type hypolactasia-linked LCT −13910C>T mutation. Scand J Gastroenterol 42:165–170CrossRefGoogle Scholar
  4. 4.
    Alvarez Leon EE, Ribas Barba L, Serra Majem L (2003) Prevalence of the metabolic syndrome in the population of Canary Islands, Spain. Med Clin (Barc) 120:172–174CrossRefGoogle Scholar
  5. 5.
    Alvarez-Leon EE, Roman-Vinas B, Serra-Majem L (2006) Dairy products and health: a review of the epidemiological evidence. Br J Nutr 96(Suppl 1):S94–99Google Scholar
  6. 6.
    Aranceta J (2005) La leche y los lácteos en la alimentación de los españoles. In: Arancenta J, Serra-Majem L (eds) Leche, lácteos y salud. Médica-Panamericana, Madrid, pp 31–41Google Scholar
  7. 7.
    Berkey CS, Colditz GA, Rockett HR, Frazier AL, Willett WC (2009) Dairy consumption and female height growth: prospective cohort study. Cancer Epidemiol Biomarkers Prev 18:1881–1887CrossRefGoogle Scholar
  8. 8.
    Berkey CS, Rockett HR, Willett WC, Colditz GA (2005) Milk, dairy fat, dietary calcium, and weight gain: a longitudinal study of adolescents. Arch Pediatr Adolesc Med 159:543–550CrossRefGoogle Scholar
  9. 9.
    Brismar K, Nilsson SE (2009) Interrelations and associations of serum levels of steroids and pituitary hormones with markers of insulin resistance, inflammatory activity, and renal function in men and women aged >70 years in an 8-year longitudinal study of opposite-sex twins. Gend Med 6(Suppl 1):123–136CrossRefGoogle Scholar
  10. 10.
    Cornier MA, Dabelea D, Hernandez TL, Lindstrom RC, Steig AJ, Stob NR, Van Pelt RE, Wang H, Eckel RH (2008) The metabolic syndrome. Endocr Rev 29:777–822CrossRefGoogle Scholar
  11. 11.
    Denise Robertson M (2007) Metabolic cross talk between the colon and the periphery: implications for insulin sensitivity. Proc Nutr Soc 66:351–361CrossRefGoogle Scholar
  12. 12.
    Ding EL, Song Y, Malik VS, Liu S (2006) Sex differences of endogenous sex hormones and risk of type 2 diabetes: a systematic review and meta-analysis. JAMA 295:1288–1299CrossRefGoogle Scholar
  13. 13.
    Elwood PC, Pickering JE, Fehily AM (2007) Milk and dairy consumption, diabetes and the metabolic syndrome: the Caerphilly prospective study. J Epidemiol Community Health 61:695–698CrossRefGoogle Scholar
  14. 14.
    Enattah NS, Trudeau A, Pimenoff V, Maiuri L, Auricchio S, Greco L, Rossi M, Lentze M, Seo JK, Rahgozar S, Khalil I, Alifrangis M, Natah S, Groop L, Shaat N, Kozlov A, Verschubskaya G, Comas D, Bulayeva K, Mehdi SQ, Terwilliger JD, Sahi T, Savilahti E, Perola M, Sajantila A, Jarvela I, Peltonen L (2007) Evidence of still-ongoing convergence evolution of the lactase persistence T-13910 alleles in humans. Am J Hum Genet 81:615–625CrossRefGoogle Scholar
  15. 15.
    Erlingsson S, Herard S, Dahlqvist Leinhard O, Lindstrom T, Lanne T, Borga M, Nystrom FH (2009) Men develop more intraabdominal obesity and signs of the metabolic syndrome after hyperalimentation than women. Metabolism 58:995–1001CrossRefGoogle Scholar
  16. 16.
    FitzGerald RJ, Murray BA, Walsh DJ (2004) Hypotensive peptides from milk proteins. J Nutr 134:980S–988SGoogle Scholar
  17. 17.
    Ford ES (2005) Risks for all-cause mortality, cardiovascular disease, and diabetes associated with the metabolic syndrome: a summary of the evidence. Diabetes Care 28:1769–1778CrossRefGoogle Scholar
  18. 18.
    Ganmaa D, Sato A (2005) The possible role of female sex hormones in milk from pregnant cows in the development of breast, ovarian and corpus uteri cancers. Med Hypotheses 65:1028–1037CrossRefGoogle Scholar
  19. 19.
    Ganmaa D, Wang PY, Qin LQ, Hoshi K, Sato A (2001) Is milk responsible for male reproductive disorders? Med Hypotheses 57:510–514CrossRefGoogle Scholar
  20. 20.
    Giovannucci E, Pollak M, Liu Y, Platz EA, Majeed N, Rimm EB, Willett WC (2003) Nutritional predictors of insulin-like growth factor I and their relationships to cancer in men. Cancer Epidemiol Biomarkers Prev 12:84–89Google Scholar
  21. 21.
    Henriquez Sanchez P, Diaz Romero C, Rodriguez Rodriguez E, Lopez Blanco F, Alvarez Leon E, Diaz Cremades J, Pastor Ferrer MC, Serra Majem L (2000) Biochemical assessment of nutritional status in the Canary Islands population (1998). Arch Latinoam Nutr 50:43–54Google Scholar
  22. 22.
    Hjartaker A, Lagiou A, Slimani N, Lund E, Chirlaque MD, Vasilopoulou E, Zavitsanos X, Berrino F, Sacerdote C, Ocke MC, Peeters PH, Engeset D, Skeie G, Aller A, Amiano P, Berglund G, Nilsson S, McTaggart A, Spencer EA, Overvad K, Tjonneland A, Clavel-Chapelon F, Linseisen J, Schulz M, Hemon B, Riboli E (2002) Consumption of dairy products in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort: data from 35,955 24-h dietary recalls in 10 European countries. Public Health Nutr 5:1259–1271CrossRefGoogle Scholar
  23. 23.
    Hoppe C, Molgaard C, Juul A, Michaelsen KF (2004) High intakes of skimmed milk, but not meat, increase serum IGF-I and IGFBP-3 in eight-year-old boys. Eur J Clin Nutr 58:1211–1216CrossRefGoogle Scholar
  24. 24.
    Ingram CJ, Elamin MF, Mulcare CA, Weale ME, Tarekegn A, Raga TO, Bekele E, Elamin FM, Thomas MG, Bradman N, Swallow DM (2007) A novel polymorphism associated with lactose tolerance in Africa: multiple causes for lactase persistence? Hum Genet 120:779–788CrossRefGoogle Scholar
  25. 25.
    Joy T, Lahiry P, Pollex RL, Hegele RA (2008) Genetics of metabolic syndrome. Curr Diab Rep 8:141–148CrossRefGoogle Scholar
  26. 26.
    Lanou AJ, Barnard ND (2008) Dairy and weight loss hypothesis: an evaluation of the clinical trials. Nutr Rev 66:272–279CrossRefGoogle Scholar
  27. 27.
    Lawlor DA, Ebrahim S, Timpson N, Davey Smith G (2005) Avoiding milk is associated with a reduced risk of insulin resistance and the metabolic syndrome: findings from the British Women’s Heart and Health Study. Diabet Med 22:808–811CrossRefGoogle Scholar
  28. 28.
    Levesque J, Lamarche B (2008) The metabolic syndrome: definitions, prevalence and management. J Nutrigenet Nutrigenomics 1:100–108CrossRefGoogle Scholar
  29. 29.
    Livingstone C, Collison M (2002) Sex steroids and insulin resistance. Clin Sci (Lond) 102:151–166CrossRefGoogle Scholar
  30. 30.
    Nilsson TK, Johansson CA (2004) A novel method for diagnosis of adult hypolactasia by genotyping of the −13910 C/T polymorphism with Pyrosequencing technology. Scand J Gastroenterol 39:287–290CrossRefGoogle Scholar
  31. 31.
    Nishizawa H, Shimomura I, Kishida K, Maeda N, Kuriyama H, Nagaretani H, Matsuda M, Kondo H, Furuyama N, Kihara S, Nakamura T, Tochino Y, Funahashi T, Matsuzawa Y (2002) Androgens decrease plasma adiponectin, an insulin-sensitizing adipocyte-derived protein. Diabetes 51:2734–2741CrossRefGoogle Scholar
  32. 32.
    Ostman EM, Liljeberg Elmstahl HG, Bjorck IM (2001) Inconsistency between glycemic and insulinemic responses to regular and fermented milk products. Am J Clin Nutr 74:96–100Google Scholar
  33. 33.
    Pfeuffer M, Schrezenmeir J (2007) Milk and the metabolic syndrome. Obes Rev 8:109–118CrossRefGoogle Scholar
  34. 34.
    Rajpathak SN, Rimm EB, Rosner B, Willett WC, Hu FB (2006) Calcium and dairy intakes in relation to long-term weight gain in US men. Am J Clin Nutr 83:559–566Google Scholar
  35. 35.
    Regitz-Zagrosek V, Lehmkuhl E, Mahmoodzadeh S (2007) Gender aspects of the role of the metabolic syndrome as a risk factor for cardiovascular disease. Gend Med 4(Suppl B):S162–177CrossRefGoogle Scholar
  36. 36.
    Sahi T (1994) Genetics and epidemiology of adult-type hypolactasia. Scand J Gastroenterol Suppl 202:7–20CrossRefGoogle Scholar
  37. 37.
    Serra Majem L, Cabrera Leon A, Sierra Lopez A (2000) Conclusions of the Canary Islands Nutrition Survey (1997–1998). Foundations for a nutrition policy in Canary Islands. Arch Latinoam Nutr 50:62–70Google Scholar
  38. 38.
    Serra Majem L, Ribas Barba L, Armas Navarro A, Alvarez Leon E, Sierra A (2000) Energy and nutrient intake and risk of inadequate intakes in Canary Islands (1997–1998). Arch Latinoam Nutr 50:7–22Google Scholar
  39. 39.
    Serra-Majem L, Aranceta J (2002) Alimentación infantil y juvenil. Masson S.A., BarcelonaGoogle Scholar
  40. 40.
    Suarez FL, Savaiano D, Arbisi P, Levitt MD (1997) Tolerance to the daily ingestion of two cups of milk by individuals claiming lactose intolerance. Am J Clin Nutr 65:1502–1506Google Scholar
  41. 41.
    Swallow DM (2003) Genetics of lactase persistence and lactose intolerance. Annu Rev Genet 37:197–219CrossRefGoogle Scholar
  42. 42.
    Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Babbitt CC, Silverman JS, Powell K, Mortensen HM, Hirbo JB, Osman M, Ibrahim M, Omar SA, Lema G, Nyambo TB, Ghori J, Bumpstead S, Pritchard JK, Wray GA, Deloukas P (2007) Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet 39:31–40CrossRefGoogle Scholar
  43. 43.
    Wiley AS (2005) Does milk make children grow? Relationships between milk consumption and height in NHANES 1999–2002. Am J Hum Biol 17:425–441CrossRefGoogle Scholar
  44. 44.
    Zemel MB (2003) Role of dietary calcium and dairy products in modulating adiposity. Lipids 38:139–146CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Ricardo Almon
    • 1
  • Eva E. Álvarez-Leon
    • 2
    • 3
  • Peter Engfeldt
    • 1
  • Lluís Serra-Majem
    • 2
    • 3
  • Anders Magnuson
    • 4
  • Torbjörn K. Nilsson
    • 5
  1. 1.Family Medicine Research Centre, School of Health and Medical SciencesÖrebro UniversityÖrebroSweden
  2. 2.Department of Clinical Sciences, Faculty of Health SciencesUniversity of Las Palmas de Gran CanariaCanary IslandsSpain
  3. 3.Service of Preventive MedicineUniversity Hospital Insular of Gran Canaria, Canarian Health ServiceCanary IslandsSpain
  4. 4.Statistical and Epidemiology UnitÖrebro University HospitalÖrebroSweden
  5. 5.Department of Clinical ChemistryÖrebro University HospitalÖrebroSweden

Personalised recommendations