Association of Lifecourse Socioeconomic Status with Chronic Inflammation and Type 2 Diabetes Risk: The Whitehall II Prospective Cohort Study

English version České info

Background:
Socioeconomic adversity in early life has been hypothesized to “program” a vulnerable phenotype with exaggerated inflammatory responses, so increasing the risk of developing type 2 diabetes in adulthood. The aim of this study is to test this hypothesis by assessing the extent to which the association between lifecourse socioeconomic status and type 2 diabetes incidence is explained by chronic inflammation.

Methods and Findings:
We use data from the British Whitehall II study, a prospective occupational cohort of adults established in 1985. The inflammatory markers C-reactive protein and interleukin-6 were measured repeatedly and type 2 diabetes incidence (new cases) was monitored over an 18-year follow-up (from 1991–1993 until 2007–2009). Our analytical sample consisted of 6,387 non-diabetic participants (1,818 women), of whom 731 (207 women) developed type 2 diabetes over the follow-up. Cumulative exposure to low socioeconomic status from childhood to middle age was associated with an increased risk of developing type 2 diabetes in adulthood (hazard ratio [HR] = 1.96, 95% confidence interval: 1.48–2.58 for low cumulative lifecourse socioeconomic score and HR = 1.55, 95% confidence interval: 1.26–1.91 for low-low socioeconomic trajectory). 25% of the excess risk associated with cumulative socioeconomic adversity across the lifecourse and 32% of the excess risk associated with low-low socioeconomic trajectory was attributable to chronically elevated inflammation (95% confidence intervals 16%–58%).

Conclusions:
In the present study, chronic inflammation explained a substantial part of the association between lifecourse socioeconomic disadvantage and type 2 diabetes. Further studies should be performed to confirm these findings in population-based samples, as the Whitehall II cohort is not representative of the general population, and to examine the extent to which social inequalities attributable to chronic inflammation are reversible.

Please see later in the article for the Editors' Summary

Vyšlo v časopise: Association of Lifecourse Socioeconomic Status with Chronic Inflammation and Type 2 Diabetes Risk: The Whitehall II Prospective Cohort Study. PLoS Med 10(7): e32767. doi:10.1371/journal.pmed.1001479
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pmed.1001479

Souhrn

Zdroje

1. AgardhE, AllebeckP, HallqvistJ, MoradiT, SidorchukA (2011) Type 2 diabetes incidence and socio-economic position: a systematic review and meta-analysis. Int J Epidemiol 40: 804–818.

2. StringhiniS, TabakAG, AkbaralyTN, SabiaS, ShipleyMJ, et al. (2012) Contribution of modifiable risk factors to social inequalities in type 2 diabetes: prospective Whitehall II cohort study. BMJ 345: e5452.

3. AlbertiKG, ZimmetPZ (1998) Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 15: 539–553.

4. DabeleaD, HansonRL, LindsayRS, PettittDJ, ImperatoreG, et al. (2000) Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships. Diabetes 49: 2208–2211.

5. GluckmanPD, HansonMA, CooperC, ThornburgKL (2008) Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359: 61–73.

6. VaagAA, GrunnetLG, AroraGP, BronsC (2012) The thrifty phenotype hypothesis revisited. Diabetologia 55: 2085–2088.

7. MatySC, Everson-RoseSA, HaanMN, RaghunathanTE, KaplanGA (2005) Education, income, occupation, and the 34-year incidence (1965–99) of Type 2 diabetes in the Alameda County Study. Int J Epidemiol 34: 1274–1281.

8. MatySC, LynchJW, RaghunathanTE, KaplanGA (2008) Childhood socioeconomic position, gender, adult body mass index, and incidence of type 2 diabetes mellitus over 34 years in the Alameda County Study. Am J Public Health 98: 1486–1494.

9. LucoveJC, KaufmanJS, JamesSA (2007) Association between adult and childhood socioeconomic status and prevalence of the metabolic syndrome in African Americans: the Pitt County Study. Am J Public Health 97: 234–236.

10. LangenbergC, KuhD, WadsworthME, BrunnerE, HardyR (2006) Social circumstances and education: life course origins of social inequalities in metabolic risk in a prospective national birth cohort. Am J Public Health 96: 2216–2221.

11. LawlorDA, Davey SmithG, EbrahimS (2003) Life course influences on insulin resistance: findings from the British Women's Heart and Health Study. Diabetes Care 26: 97–103.

12. LehmanBJ, TaylorSE, KiefeCI, SeemanTE (2005) Relation of childhood socioeconomic status and family environment to adult metabolic functioning in the CARDIA study. Psychosom Med 67: 846–854.

13. ImkampeAK, GullifordMC (2011) Increasing socio-economic inequality in type 2 diabetes prevalence–repeated cross-sectional surveys in England 1994–2006. Eur J Public Health 21: 484–490.

14. EspeltA, KunstAE, PalenciaL, GnaviR, BorrellC (2012) Twenty years of socio-economic inequalities in type 2 diabetes mellitus prevalence in Spain, 1987–2006. Eur J Public Health 22: 765–771.

15. Circulation (1999) Diabetes mellitus: a major risk factor for cardiovascular disease. A joint editorial statement by the American Diabetes Association; The National Heart, Lung, and Blood Institute; The Juvenile Diabetes Foundation International; The National Institute of Diabetes and Digestive and Kidney Diseases; and The American Heart Association. Circulation 100: 1132–1133.

16. PanA, LucasM, SunQ, van DamRM, FrancoOH, et al. (2010) Bidirectional association between depression and type 2 diabetes mellitus in women. Arch Intern Med 170: 1884–1891.

17. HaffnerSM, LehtoS, RonnemaaT, PyoralaK, LaaksoM (1998) Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 339: 229–234.

18. ParkerL, LamontDW, UnwinN, PearceMS, BennettSM, et al. (2003) A lifecourse study of risk for hyperinsulinaemia, dyslipidaemia and obesity (the central metabolic syndrome) at age 49–51 years. Diabet Med 20: 406–415.

19. TelamaR, YangX, ViikariJ, ValimakiI, WanneO, et al. (2005) Physical activity from childhood to adulthood: a 21-year tracking study. Am J Prev Med 28: 267–273.

20. MillerGE, ChenE, FokAK, WalkerH, LimA, et al. (2009) Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proc Natl Acad Sci U S A 106: 14716–14721.

21. BorgholN, SudermanM, McArdleW, RacineA, HallettM, et al. (2012) Associations with early-life socio-economic position in adult DNA methylation. Int J Epidemiol 41: 62–74.

22. HertzmanC (1999) The biological embedding of early experience and its effects on health in adulthood. Ann N Y Acad Sci 896: 85–95.

23. HanselA, HongS, CamaraRJ, von KanelR (2010) Inflammation as a psychophysiological biomarker in chronic psychosocial stress. Neurosci Biobehav Rev 35: 115–121.

24. Ziol-GuestKM, DuncanGJ, KalilA, BoyceWT (2012) Early childhood poverty, immune-mediated disease processes, and adult productivity. Proc Natl Acad Sci U S A 109 Suppl 2: 17289–17293.

25. TungJ, BarreiroLB, JohnsonZP, HansenKD, MichopoulosV, et al. (2012) Social environment is associated with gene regulatory variation in the rhesus macaque immune system. Proc Natl Acad Sci U S A 109: 6490–6495.

26. HemingwayH, ShipleyM, MullenMJ, KumariM, BrunnerE, et al. (2003) Social and psychosocial influences on inflammatory markers and vascular function in civil servants (the Whitehall II study). Am J Cardiol 92: 984–987.

27. JousilahtiP, SalomaaV, RasiV, VahteraE, PalosuoT (2003) Association of markers of systemic inflammation, C reactive protein, serum amyloid A, and fibrinogen, with socioeconomic status. J Epidemiol Community Health 57: 730–733.

28. KivimakiM, LawlorDA, JuonalaM, SmithGD, ElovainioM, et al. (2005) Lifecourse socioeconomic position, C-reactive protein, and carotid intima-media thickness in young adults: the cardiovascular risk in Young Finns Study. Arterioscler Thromb Vasc Biol 25: 2197–2202.

29. AlleyDE, SeemanTE, Ki KimJ, KarlamanglaA, HuP, et al. (2006) Socioeconomic status and C-reactive protein levels in the US population: NHANES IV. Brain Behav Immun 20: 498–504.

30. LoucksEB, PiloteL, LynchJW, RichardH, AlmeidaND, et al. (2010) Life course socioeconomic position is associated with inflammatory markers: the Framingham Offspring Study. Soc Sci Med 71: 187–195.

31. GalobardesB, SmithGD, LynchJW (2006) Systematic review of the influence of childhood socioeconomic circumstances on risk for cardiovascular disease in adulthood. Ann Epidemiol 16: 91–104.

32. HotamisligilGS (2006) Inflammation and metabolic disorders. Nature 444: 860–867.

33. DonathMY, EhsesJA, MaedlerK, SchumannDM, EllingsgaardH, et al. (2005) Mechanisms of beta-cell death in type 2 diabetes. Diabetes 54 Suppl 2: S108–113.

34. PradhanAD, MansonJE, RifaiN, BuringJE, RidkerPM (2001) C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 286: 327–334.

35. DuncanBB, SchmidtMI, PankowJS, BallantyneCM, CouperD, et al. (2003) Low-grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes 52: 1799–1805.

36. Mohamed-AliV, GoodrickS, RaweshA, KatzDR, MilesJM, et al. (1997) Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-alpha, in vivo. J Clin Endocrinol Metab 82: 4196–4200.

37. ReidDD, BrettGZ, HamiltonPJ, JarrettRJ, KeenH, et al. (1974) Cardiorespiratory disease and diabetes among middle-aged male Civil Servants. A study of screening and intervention. Lancet 1: 469–473.

38. MarmotMG, SmithGD, StansfeldS, PatelC, NorthF, et al. (1991) Health inequalities among British civil servants: the Whitehall II study. Lancet 337: 1387–1393.

39. GalobardesB, LynchJW, SmithGD (2004) Childhood socioeconomic circumstances and cause-specific mortality in adulthood: systematic review and interpretation. Epidemiol Rev 26: 7–21.

40. GalobardesB, LynchJ, SmithGD (2007) Measuring socioeconomic position in health research. Br Med Bull 81–82: 21–37.

41. StringhiniS, DugravotA, KivimakiM, ShipleyM, ZinsM, et al. (2011) Do different measures of early life socioeconomic circumstances predict adult mortality? Evidence from the British Whitehall II and French GAZEL studies. J Epidemiol Community Health 65: 1097–1103.

42. GalobardesB, ShawM, LawlorDA, LynchJW, Davey SmithG (2006) Indicators of socioeconomic position (part 1). J Epidemiol Community Health 60: 7–12.

43. GalobardesB, ShawM, LawlorDA, LynchJW, Davey SmithG (2006) Indicators of socioeconomic position (part 2). J Epidemiol Community Health 60: 95–101.

44. Ben-ShlomoY, KuhD (2002) A life course approach to chronic disease epidemiology: conceptual models, empirical challenges and interdisciplinary perspectives. Int J Epidemiol 31: 285–293.

45. SmithBT, LynchJW, FoxCS, HarperS, AbrahamowiczM, et al. (2011) Life-course socioeconomic position and type 2 diabetes mellitus: The Framingham Offspring Study. Am J Epidemiol 173: 438–447.

46. TabakAG, JokelaM, AkbaralyTN, BrunnerEJ, KivimakiM, et al. (2009) Trajectories of glycaemia, insulin sensitivity, and insulin secretion before diagnosis of type 2 diabetes: an analysis from the Whitehall II study. Lancet 373: 2215–2221.

47. BrunnerEJ, KivimakiM, WitteDR, LawlorDA, Davey SmithG, et al. (2008) Inflammation, insulin resistance, and diabetes–Mendelian randomization using CRP haplotypes points upstream. PLoS Med 5: e155 doi:10.1371/journal.pmed.0050155

48. GimenoD, KivimakiM, BrunnerEJ, ElovainioM, De VogliR, et al. (2009) Associations of C-reactive protein and interleukin-6 with cognitive symptoms of depression: 12-year follow-up of the Whitehall II study. Psychol Med 39: 413–423.

49. SabiaS, DugravotA, KivimakiM, BrunnerE, ShipleyMJ, et al. (2012) Effect of intensity and type of physical activity on mortality: results from the Whitehall II Cohort Study. Am J Public Health 102: 698–704.

50. McCulloughML, FeskanichD, StampferMJ, GiovannucciEL, RimmEB, et al. (2002) Diet quality and major chronic disease risk in men and women: moving toward improved dietary guidance. Am J Clin Nutr 76: 1261–1271.

51. AkbaralyTN, FerrieJE, BerrC, BrunnerEJ, HeadJ, et al. (2011) Alternative Healthy Eating Index and mortality over 18 y of follow-up: results from the Whitehall II cohort. Am J Clin Nutr 94: 247–253.

52. StringhiniS, SabiaS, ShipleyM, BrunnerE, NabiH, et al. (2010) Association of socioeconomic position with health behaviors and mortality. JAMA 303: 1159–1166.

53. World Health Organisation (2007) The challenge of obesity in the WHO European Region and the strategies for response. Geneva: WHO. 73 p.

54. DemissieS, LaValleyMP, HortonNJ, GlynnRJ, CupplesLA (2003) Bias due to missing exposure data using complete-case analysis in the proportional hazards regression model. Stat Med 22: 545–557.

55. CoxDR (1972) Regression models and life-tables. Journal of the Royal Statistical Society Series B (Methodological) 34: 187–220.

56. ShulmanGI (2000) Cellular mechanisms of insulin resistance. J Clin Invest 106: 171–176.

57. AgardhEE, AhlbomA, AnderssonT, EfendicS, GrillV, et al. (2007) Socio-economic position at three points in life in association with type 2 diabetes and impaired glucose tolerance in middle-aged Swedish men and women. Int J Epidemiol 36: 84–92.

58. LidfeldtJ, LiTY, HuFB, MansonJE, KawachiI (2007) A prospective study of childhood and adult socioeconomic status and incidence of type 2 diabetes in women. Am J Epidemiol 165: 882–889.

59. DemakakosP, MarmotM, SteptoeA (2012) Socioeconomic position and the incidence of type 2 diabetes: the ELSA study. Eur J Epidemiol 27: 367–378.

60. RanjitN, Diez-RouxAV, SheaS, CushmanM, NiH, et al. (2007) Socioeconomic position, race/ethnicity, and inflammation in the multi-ethnic study of atherosclerosis. Circulation 116: 2383–2390.

61. CarrollJE, CohenS, MarslandAL (2011) Early childhood socioeconomic status is associated with circulating interleukin-6 among mid-life adults. Brain Behav Immun 25: 1468–1474.

62. GimenoD, BrunnerEJ, LoweGD, RumleyA, MarmotMG, et al. (2007) Adult socioeconomic position, C-reactive protein and interleukin-6 in the Whitehall II prospective study. Eur J Epidemiol 22: 675–683.

63. LoucksEB, SullivanLM, HayesLJ, D'AgostinoRBSr, LarsonMG, et al. (2006) Association of educational level with inflammatory markers in the Framingham Offspring Study. Am J Epidemiol 163: 622–628.

64. O'ReillyDS, UptonMN, CaslakeMJ, RobertsonM, NorrieJ, et al. (2006) Plasma C reactive protein concentration indicates a direct relation between systemic inflammation and social deprivation. Heart 92: 533–535.

65. GimenoD, FerrieJE, ElovainioM, Pulkki-RabackL, Keltikangas-JarvinenL, et al. (2008) When do social inequalities in C-reactive protein start? A life course perspective from conception to adulthood in the Cardiovascular Risk in Young Finns Study. Int J Epidemiol 37: 290–298.

66. AbramsonJL, VaccarinoV (2002) Relationship between physical activity and inflammation among apparently healthy middle-aged and older US adults. Arch Intern Med 162: 1286–1292.

67. FranksPW (2006) Obesity, inflammatory markers and cardiovascular disease: distinguishing causality from confounding. J Hum Hypertens 20: 837–840.

68. van der VaartH, PostmaDS, TimensW, HylkemaMN, WillemseBW, et al. (2005) Acute effects of cigarette smoking on inflammation in healthy intermittent smokers. Respir Res 6: 22.

69. O'ConnorMF, BowerJE, ChoHJ, CreswellJD, DimitrovS, et al. (2009) To assess, to control, to exclude: effects of biobehavioral factors on circulating inflammatory markers. Brain Behav Immun 23: 887–897.

70. HamerM, SabiaS, BattyGD, ShipleyMJ, TabakAG, et al. (2012) Physical activity and inflammatory markers over 10 years: follow-up in men and women from the Whitehall II cohort study. Circulation 126: 928–933.

71. ScottKA, MelhornSJ, SakaiRR (2012) Effects of chronic social stress on obesity. Curr Obes Rep 1: 16–25.

72. DalstraJA, KunstAE, BorrellC, BreezeE, CamboisE, et al. (2005) Socioeconomic differences in the prevalence of common chronic diseases: an overview of eight European countries. Int J Epidemiol 34: 316–326.

73. LawlorDA, SmithGD, EbrahimS (2004) Socioeconomic position and hormone replacement therapy use: explaining the discrepancy in evidence from observational and randomized controlled trials. Am J Public Health 94: 2149–2154.

74. FilippiniM, MasieroG, MoschettiK (2006) Socioeconomic determinants of regional differences in outpatient antibiotic consumption: evidence from Switzerland. Health Policy 78: 77–92.

75. BattyGD, LawlorDA, MacintyreS, ClarkH, LeonDA (2005) Accuracy of adults' recall of childhood social class: findings from the Aberdeen children of the 1950s study. J Epidemiol Community Health 59: 898–903.

76. KauhanenL, LakkaHM, LynchJW, KauhanenJ (2006) Social disadvantages in childhood and risk of all-cause death and cardiovascular disease in later life: a comparison of historical and retrospective childhood information. Int J Epidemiol 35: 962–968.

77. ElovainioM, FerrieJE, Singh-ManouxA, ShipleyM, BattyGD, et al. (2011) Socioeconomic differences in cardiometabolic factors: social causation or health-related selection? Evidence from the Whitehall II Cohort Study, 1991–2004. Am J Epidemiol 174: 779–789.

78. PrinceSA, AdamoKB, HamelME, HardtJ, GorberSC, et al. (2008) A comparison of direct versus self-report measures for assessing physical activity in adults: a systematic review. Int J Behav Nutr Phys Act 5: 56.

79. HatziandreuEJ, PierceJP, FioreMC, GriseV, NovotnyTE, et al. (1989) The reliability of self-reported cigarette consumption in the United States. Am J Public Health 79: 1020–1023.

80. BrunnerE, StalloneD, JunejaM, BinghamS, MarmotM (2001) Dietary assessment in Whitehall II: comparison of 7 d diet diary and food-frequency questionnaire and validity against biomarkers. Br J Nutr 86: 405–414.

81. RichardsonMT, LeonAS, JacobsDRJr, AinsworthBE, SerfassR (1994) Comprehensive evaluation of the Minnesota Leisure Time Physical Activity Questionnaire. J Clin Epidemiol 47: 271–281.

82. OlivieriM, PoliA, ZuccaroP, FerrariM, LamprontiG, et al. (2002) Tobacco smoke exposure and serum cotinine in a random sample of adults living in Verona, Italy. Arch Environ Health 57: 355–359.

83. RothwellPM, PriceJF, FowkesFG, ZanchettiA, RoncaglioniMC, et al. (2012) Short-term effects of daily aspirin on cancer incidence, mortality, and non-vascular death: analysis of the time course of risks and benefits in 51 randomised controlled trials. Lancet 379: 1602–1612.

84. RothwellPM, WilsonM, PriceJF, BelchJF, MeadeTW, et al. (2012) Effect of daily aspirin on risk of cancer metastasis: a study of incident cancers during randomised controlled trials. Lancet 379: 1591–1601.

85. SilvaMT, GalvaoTF, ZimmermanIR, PereiraMG, LopesLC (2012) Non-aspirin non-steroidal anti-inflammatory drugs for the primary chemoprevention of non-gastrointestinal cancer: summary of evidence. Curr Pharm Des 18: 4047–4070.