Ambient and Traffic-Related Air Pollution Exposures as Novel Risk Factors for Metabolic Dysfunction and Type 2 Diabetes

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1. 1.
   GBD 2015 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388:1545–602.Google Scholar
2. 2.
   Dabelea D, Mayer-Davis EJ, Saydah S, Imperatore G, Linder B, Divers J, et al. Prevalence of type 1 and type 2 diabetes among children and adolescents from 2001 to 2009. JAMA. 2014;311:1778–86.CrossRefPubMedPubMedCentralGoogle Scholar
3. 3.
   Imperatore G, Boyle JP, Thompson TJ, Case D, Dabelea D, Hamman RF, et al. Projections of type 1 and type 2 diabetes burden in the U.S. population aged <20 years through 2050: dynamic modeling of incidence, mortality, and population growth. Am Diabetes Assoc Diabetes Care. 2012;35:2515–20.CrossRefGoogle Scholar
4. 4.
   Ljungman PL, Mittleman MA. Ambient air pollution and stroke. Stroke. 2014;45:3734–41.CrossRefPubMedPubMedCentralGoogle Scholar
5. 5.
   Koulova A, Frishman WH. Air pollution exposure as a risk factor for cardiovascular disease morbidity and mortality. Cardiol Rev. 2014;22:30–6.CrossRefPubMedGoogle Scholar
6. 6.
   Sava F, Carlsten C. Respiratory health effects of ambient air pollution: an update. Clin Chest Med. 2012;33:759–69.CrossRefPubMedGoogle Scholar
7. 7.
   Eze IC, Foraster M, Schaffner E, Vienneau D, Héritier H, Rudzik F, et al. Long-term exposure to transportation noise and air pollution in relation to incident diabetes in the SAPALDIA study. Int J Epidemiol. 2017;46:1115–25.CrossRefPubMedPubMedCentralGoogle Scholar
8. 8.
   Honda T, Pun VC, Manjourides J, Suh H. Associations between long-term exposure to air pollution, glycosylated hemoglobin and diabetes. Int J Hyg Environ Health. 2017;220:1124–32.CrossRefPubMedGoogle Scholar
9. 9.
   Jerrett M, Brook R, White LF, Burnett RT, Yu J, Su J, et al. Ambient ozone and incident diabetes: a prospective analysis in a large cohort of African American women. Environ Int. 2017;102:42–7.CrossRefPubMedGoogle Scholar
10. 10.
    Mazidi M, Speakman JR. Ambient particulate air pollution (PM2.5) is associated with the ratio of type 2 diabetes to obesity. Sci Rep. 2017;7(1):9144.Google Scholar
11. 11.
    O'Donovan G, Chudasama Y, Grocock S, Leigh R, Dalton AM, Gray LJ, et al. The association between air pollution and type 2 diabetes in a large cross-sectional study in Leicester: The CHAMPIONS study. Environ Int. 2017;104:41–7.CrossRefPubMedGoogle Scholar
12. 12.
    Requia WJ, Adams MD, Koutrakis P. Association of PM2.5 with diabetes, asthma, and high blood pressure incidence in Canada: a spatiotemporal analysis of the impacts of the energy generation and fuel sales. Sci Total Environ. 2017;584-585:1077–83.CrossRefPubMedGoogle Scholar
13. 13.
    Sohn D, Gender-dependent Differences OH. In the relationship between diabetes mellitus and ambient air pollution among adults in South Korean cities. Iran J Public Health. 2017;46:293–300.PubMedPubMedCentralGoogle Scholar
14. 14.
    Strak M, Janssen N, Beelen R, Schmitz O, Vaartjes I, Karssenberg D, et al. Long-term exposure to particulate matter, NO2 and the oxidative potential of particulates and diabetes prevalence in a large national health survey. Environ Int. 2017;108:228–36.CrossRefPubMedGoogle Scholar
15. 15.
    Coogan PF, White LF, Yu J, Burnett RT, Marshall JD, Seto E, et al. Long term exposure to NO2 and diabetes incidence in the Black Women’s Health Study. Environ Res. 2016;148:360–6.CrossRefPubMedPubMedCentralGoogle Scholar
16. 16.
    Dzhambov A, Dimitrova D. Exposures to road traffic, noise, and air pollution as risk factors for type 2 diabetes: a feasibility study in Bulgaria. Noise Health. 2016;18:133–11.CrossRefPubMedPubMedCentralGoogle Scholar
17. 17.
    •• Hansen AB, Ravnskjær L, Loft S, Andersen KK, Bräuner EV, Baastrup R, et al. Long-term exposure to fine particulate matter and incidence of diabetes in the Danish Nurse Cohort. Environ Int. 2016;91:243–50. Large prospective cohort study among 28,731 female nurses in Denmark. Results indicate that long-term exposures to PM _2.5 were associated with greater diabetes incidence from year 1993–2013. No significant associations were observed for NO ₂ , PM ₁₀ , and NO _x exposures. The associations with PM _2.5 were larger in nonsmokers and obese participants. CrossRefPubMedGoogle Scholar
18. 18.
    Lazarevic N, Dobson AJ, Barnett AG, Knibbs LD. Long-term ambient air pollution exposure and self-reported morbidity in the Australian Longitudinal Study on Women’s Health: a cross-sectional study. BMJ Open. 2015;5(10):e008714.CrossRefPubMedPubMedCentralGoogle Scholar
19. 19.
    • Liu C, Yang C, Zhao Y, Ma Z, Bi J, Liu Y, et al. Associations between long-term exposure to ambient particulate air pollution and type 2 diabetes prevalence, blood glucose and glycosylated hemoglobin levels in China. Environ Int. 2016;92–93:416–21. Large, cross-sectional study ( n =11,847) conducted in China with relatively high pollution levels. Results suggest that long-term exposures to ambient PM _2.5 were associated with higher risk of type 2 diabetes. These findings suggest that air pollution exposures impact type 2 diabetes risk in high polluted areas. Notably, similar findings were also observed in Europe and North America, where air pollution levels are relatively low. CrossRefPubMedPubMedCentralGoogle Scholar
20. 20.
    •• Park SK, Adar SD, O’Neill MS, Auchincloss AH, Szpiro A, Bertoni AG, et al. Long-term exposure to air pollution and type 2 diabetes mellitus in a multiethnic cohort. Am J Epidemiol. 2015;181:327–36. A large multiethnic, prospective study ( n =5,839) across six sites in the USA, which found long-term exposures to NO ₂ and PM _2.5 were associated with a higher prevalence of type 2 diabetes across all sites. However, the longitudinal associations between long-term exposures to NO ₂ and PM _2.5 and type 2 diabetes incidence were largely nonsignificant in across study sites . CrossRefPubMedPubMedCentralGoogle Scholar
21. 21.
    To T, Zhu J, Villeneuve PJ, Simatovic J, Feldman L, Gao C, et al. Chronic disease prevalence in women and air pollution—a 30-year longitudinal cohort study. Environ Int. 2015;80:26–32.CrossRefPubMedGoogle Scholar
22. 22.
    Weinmayr G, Hennig F, Fuks K, Nonnemacher M, Jakobs H, Möhlenkamp S, et al. Long-term exposure to fine particulate matter and incidence of type 2 diabetes mellitus in a cohort study: effects of total and traffic-specific air pollution. Environ Health. 2015;14:53.CrossRefPubMedPubMedCentralGoogle Scholar
23. 23.
    Chien L-C, Alamgir H, Yu H-L. Spatial vulnerability of fine particulate matter relative to the prevalence of diabetes in the United States. Sci Total Environ. 2015;508:136–44.CrossRefPubMedGoogle Scholar
24. 24.
    Eze IC, Schaffner E, Fischer E, Schikowski T, Adam M, Imboden M, et al. Long-term air pollution exposure and diabetes in a population-based Swiss cohort. Environ Int. 2014;70:95–105.CrossRefPubMedGoogle Scholar
25. 25.
    Chen H, Burnett RT, Kwong JC, Villeneuve PJ, Goldberg MS, Brook RD, et al. Risk of incident diabetes in relation to long-term exposure to fine particulate matter in Ontario, Canada. Environ Health Perspect. 2013;121:804–10.CrossRefPubMedPubMedCentralGoogle Scholar
26. 26.
    Andersen ZJ, Raaschou-Nielsen O, Ketzel M, Jensen SS, Hvidberg M, Loft S, et al. Diabetes incidence and long-term exposure to air pollution: a cohort study. Am Diabetes Assoc Diabetes Care. 2012;35:92–8.CrossRefGoogle Scholar
27. 27.
    Coogan PF, White LF, Jerrett M, Brook RD, Su JG, Seto E, et al. Air pollution and incidence of hypertension and diabetes mellitus in black women living in Los Angeles. Circulation. 2012;125:767–72.CrossRefPubMedPubMedCentralGoogle Scholar
28. 28.
    •• Chen Z, Salam MT, Toledo-Corral C, Watanabe RM, Xiang AH, Buchanan TA, et al. Ambient air pollutants have adverse effects on insulin and glucose homeostasis in Mexican Americans. Diabetes Care. 2016a;39:547–54. First adult study to examine ambient air pollution exposure with robust measures of insulin sensitivity estimated from a FSIVGTT. Results indicate that short-term and long-term exposures to PM _2.5 were associated with lower insulin sensitivity as well as higher fasting glucose and dyslipidemia. CrossRefPubMedPubMedCentralGoogle Scholar
29. 29.
    Wallwork RS, Colicino E, Zhong J, Kloog I, Coull BA, Vokonas P, et al. Ambient fine particulate matter, outdoor temperature, and risk of metabolic syndrome. Am J Epidemiol. 2017;185:30–9.CrossRefPubMedGoogle Scholar
30. 30.
    Brook RD, Sun Z, Brook JR, Zhao X, Ruan Y, Yan J, et al. Extreme air pollution conditions adversely affect blood pressure and insulin resistance: the Air Pollution and Cardiometabolic Disease Study. Hypertension. 2016;67:77–85.CrossRefPubMedGoogle Scholar
31. 31.
    • Chen L, Zhou Y, Li S, Williams G, Kan H, Marks GB, et al. Air pollution and fasting blood glucose: a longitudinal study in China. Sci Total Environ. 2016b;541:750–5. A large longitudinal study that shows that NO ₂ , PM ₁₀ , and SO ₂ were associated with fasting glucose, a clinical marker of glucose metabolism dysfunction. CrossRefPubMedGoogle Scholar
32. 32.
    Jiang S, Bo L, Gong C, Du X, Kan H, Xie Y, et al. Traffic-related air pollution is associated with cardio-metabolic biomarkers in general residents. Int Arch Occup Environ Health. 2016;89:911–21.CrossRefPubMedGoogle Scholar
33. 33.
    Peng C, Bind M-AC, Colicino E, Kloog I, Byun H-M, Cantone L, et al. Particulate air pollution and fasting blood glucose in nondiabetic individuals: associations and epigenetic mediation in the normative aging study, 2000–2011. Environ Health Perspect. 2016;124:1715–21.CrossRefPubMedPubMedCentralGoogle Scholar
34. 34.
    • Sade MY, Kloog I, Liberty IF, Katra I, Novack L, Novack V. Air pollution and serum glucose levels: a population-based study. Medicine (Baltimore). 2015;94:e1093. A large ( n =27,685) longitudinal study in China that indicates that acute exposures (prior 0–3 day average) to NO ₂ , PM ₁₀ , and SO ₂ were associated higher fasting glucose, a clinical marker of glucose metabolism dysfunction. CrossRefGoogle Scholar
35. 35.
    • Wolf K, Popp A, Schneider A, Breitner S, Hampel R, Rathmann W, et al. Association between long-term exposure to air pollution and biomarkers related to insulin resistance, subclinical inflammation, and adipokines. Diabetes. 2016;65:3314–26. Large cross-sectional study ( n =2,944) in German adults where air pollution levels are relatively low. Results show that higher long-term exposures to a wide spectrum of ambient and traffic-related air pollutants (e.g., NO ₂ , NOx, PM _2.5 , and PM ₁₀ ) were associated with higher fasting glucose, HOMA-IR, and leptin. Notably, the associations were strongest among prediabetic participants. CrossRefPubMedGoogle Scholar
36. 36.
    Eze IC, Schaffner E, Foraster M, Imboden M, von Eckardstein A, Gerbase MW, Rothe T, Rochat T, Künzli N, Schindler C, Probst-Hensch N. Long-Term Exposure to Ambient Air Pollution and Metabolic Syndrome in Adults. PLoS One. 2015;10(6):e0130337.Google Scholar
37. 37.
    Brook RD, Xu X, Bard RL, Dvonch JT, Morishita M, Kaciroti N, et al. Reduced metabolic insulin sensitivity following sub-acute exposures to low levels of ambient fine particulate matter air pollution. Sci Total Environ. 2013;448:66–71.CrossRefPubMedGoogle Scholar
38. 38.
    Teichert T, Vossoughi M, Vierkötter A, Sugiri D, Schikowski T, Schulte T, et al. Association between traffic-related air pollution, subclinical inflammation and impaired glucose metabolism: results from the SALIA Study. PLoS ONE. 2013;8:e83042.CrossRefPubMedPubMedCentralGoogle Scholar
39. 39.
    Yitshak Sade M, Kloog I, Liberty IF, Schwartz J, Novack V. The association between air pollution exposure and glucose and lipids levels. J Clin Endocrinol Metab. 2016;101:2460–7.CrossRefPubMedGoogle Scholar
40. 40.
    Bergman RN. Lilly lecture 1989. Toward physiological understanding of glucose tolerance. Minimal-model approach. Diabetes. 1989;38:1512–27.CrossRefPubMedGoogle Scholar
41. 41.
    Mayer-Davis EJ, Lawrence JM, Dabelea D, Divers J, Isom S, Dolan L, et al. Incidence trends of type 1 and type 2 diabetes among youths, 2002–2012. N Engl J Med. 2017;376:1419–29.CrossRefPubMedPubMedCentralGoogle Scholar
42. 42.
    Eppens MC, Craig ME, Cusumano J, Hing S, Chan AKF, Howard NJ, et al. Prevalence of diabetes complications in adolescents with type 2 compared with type 1 diabetes. Diabetes Care. 2006;29(6):1300–6.CrossRefPubMedGoogle Scholar
43. 43.
    •• Alderete TL, Habre R, Toledo-Corral CM, Berhane K, Chen Z, Lurmann FW, et al. Longitudinal associations between ambient air pollution with insulin sensitivity, β-cell function, and adiposity in Los Angeles Latino children. Diabetes. 2017a;66:1789–96. First longitudinal study to examine ambient air pollutants (NO ₂ and PM _2.5 ) with robust measures of insulin sensitivity and β-cell function estimated by FSIVGTT. Results indicate that long-term exposures to NO ₂ and PM _2.5 were associated with faster declines in insulin sensitivity and β-cell function among overweight and obese children. CrossRefPubMedGoogle Scholar
44. 44.
    • Ghosh R, Gauderman WJ, Minor H, Youn HA, Lurmann F, Cromar KR, et al. Air pollution, weight loss and metabolic benefits of bariatric surgery: a potential model for study of metabolic effects of environmental exposures. Pediatr Obes. 2017.  https://doi.org/10.1111/ijpo.12210. [Epub ahead of print]. The only current intervention study in children showing an attenuation of the metabolic benefits associated with bariatric surgery with increased air pollution exposure.
45. 45.
    Thiering E, Markevych I, Brüske I, Fuertes E, Kratzsch J, Sugiri D, et al. Associations of residential long-term air pollution exposures and satellite-derived greenness with insulin resistance in German adolescents. Environ Health Perspect. 2016;124:1291–8.CrossRefPubMedPubMedCentralGoogle Scholar
46. 46.
    • Toledo-Corral CM, Alderete TL, Habre R, Berhane K, Lurmann FW, Weigensberg MJ, et al. Effects of air pollution exposure on glucose metabolism in Los Angeles minority children. Pediatr Obes. 2016;312:1218. First cross-sectional study in children examining the associations of chronic exposures to ambient and traffic-related air pollutants with type 2 diabetes-related quantitative traits including robust measures of insulin sensitivity estimated from a FSIVGTT. Google Scholar
47. 47.
    Calderón-Garcidueñas L, Franco-Lira M, D'Angiulli A, Rodríguez-Díaz J, Blaurock-Busch E, Busch Y, et al. Mexico City normal weight children exposed to high concentrations of ambient PM2.5 show high blood leptin and endothelin-1, vitamin D deficiency, and food reward hormone dysregulation versus low pollution controls. Relevance for obesity and Alzheimer disease. Environ Res. 2015;140:579–92.CrossRefPubMedGoogle Scholar
48. 48.
    Thiering E, Cyrys J, Kratzsch J, Meisinger C, Hoffmann B, Berdel D, et al. Long-term exposure to traffic-related air pollution and insulin resistance in children: results from the GINIplus and LISAplus birth cohorts. Diabetologia. 2013;56:1696–704.CrossRefPubMedPubMedCentralGoogle Scholar
49. 49.
    Nemmar A. Passage of inhaled particles into the blood circulation in humans. Circulation. 2002;105:411–4.CrossRefPubMedGoogle Scholar
50. 50.
    Tamagawa E, Bai N, Morimoto K, Gray C, Mui T, Yatera K, et al. Particulate matter exposure induces persistent lung inflammation and endothelial dysfunction. Am J Physiol Lung Cell Mol Phys. 2008;295:L79–85.CrossRefGoogle Scholar
51. 51.
    Happo MS, Salonen RO, Hälinen AI, Jalava PI, Pennanen AS, Kosma VM, et al. Dose and time dependency of inflammatory responses in the mouse lung to urban air coarse, fine, and ultrafine particles from six European cities. Inhal Toxicol. 2007;19:227–46.CrossRefPubMedGoogle Scholar
52. 52.
    van Eeden SF, Tan WC, Suwa T, Mukae H, Terashima T, Fujii T, et al. Cytokines involved in the systemic inflammatory response induced by exposure to particulate matter air pollutants (PM(10)). Am J Respir Crit Care Med. 2001;164:826–30.CrossRefPubMedGoogle Scholar
53. 53.
    Dadvand P, Nieuwenhuijsen MJ, Agustí À, de Batlle J, Benet M, Beelen R, et al. Air pollution and biomarkers of systemic inflammation and tissue repair in COPD patients. Eur Respir J. 2014;44:603–13.CrossRefPubMedGoogle Scholar
54. 54.
    Fry RC, Rager JE, Zhou H, Zou B, Brickey JW, Ting J, et al. Individuals with increased inflammatory response to ozone demonstrate muted signaling of immune cell trafficking pathways. Respir Res. 2012;13:89.CrossRefPubMedPubMedCentralGoogle Scholar
55. 55.
    González-Guevara E, Martínez-Lazcano JC, Custodio V, Hernández-Cerón M, Rubio C, Paz C. Exposure to ozone induces a systemic inflammatory response: possible source of the neurological alterations induced by this gas. Inhal Toxicol. 2014;26:485–91.CrossRefPubMedGoogle Scholar
56. 56.
    Rajagopalan S, Brook RD. Air pollution and type 2 diabetes: mechanistic insights. Diabetes. 2012;61:3037–45.CrossRefPubMedPubMedCentralGoogle Scholar
57. 57.
    Xu X, Liu C, Xu Z, Tzan K, Zhong M, Wang A, et al. Long-term exposure to ambient fine particulate pollution induces insulin resistance and mitochondrial alteration in adipose tissue. Toxicol Sci. 2011;124:88–98.CrossRefPubMedPubMedCentralGoogle Scholar
58. 58.
    Xu X, Yavar Z, Verdin M, Ying Z, Mihai G, Kampfrath T, et al. Effect of early particulate air pollution exposure on obesity in mice: role of p47phox. Arterioscler Thromb Vasc Biol. 2010;30:2518–27.CrossRefPubMedPubMedCentralGoogle Scholar
59. 59.
    Irigaray P, Ogier V, Jacquenet S, Notet V, Sibille P, Mejean L, et al. Benzo[a]pyrene impairs beta-adrenergic stimulation of adipose tissue lipolysis and causes weight gain in mice. A novel molecular mechanism of toxicity for a common food pollutant. FEBS J. 2006;273:1362–72.CrossRefPubMedGoogle Scholar
60. 60.
    Sun Q, Yue P, Deiuliis JA, Lumeng CN, Kampfrath T, Mikolaj MB, et al. Ambient air pollution exaggerates adipose inflammation and insulin resistance in a mouse model of diet-induced obesity. Circulation. 2009;119:538–46.CrossRefPubMedGoogle Scholar
61. 61.
    Sas KM, Karnovsky A, Michailidis G, Pennathur S. Metabolomics and diabetes: analytical and computational approaches. Diabetes. 2015;64:718–32.CrossRefPubMedPubMedCentralGoogle Scholar
62. 62.
    Breitner S, Schneider A, Devlin RB, Ward-Caviness CK, Diaz-Sanchez D, Neas LM, et al. Associations among plasma metabolite levels and short-term exposure to PM2.5 and ozone in a cardiac catheterization cohort. Environ Int. 2016;97:76–84.CrossRefPubMedGoogle Scholar
63. 63.
    Sourij H, Meinitzer A, Pilz S, Grammer TB, Winkelmann BR, Boehm BO, et al. Arginine bioavailability ratios are associated with cardiovascular mortality in patients referred to coronary angiography. Atherosclerosis. 2011;218:220–5.CrossRefPubMedGoogle Scholar
64. 64.
    Schooneman MG, Vaz FM, Houten SM, Soeters MR. Acylcarnitines: reflecting or inflicting insulin resistance? Diabetes. 2013;62:1–8.CrossRefPubMedGoogle Scholar
65. 65.
    Menni C, Metrustry SJ, Mohney RP, Beevers S, Barratt B, Spector TD, et al. Circulating levels of antioxidant vitamins correlate with better lung function and reduced exposure to ambient pollution. Am J Respir Crit Care Med. 2015;191:1203–7.CrossRefPubMedPubMedCentralGoogle Scholar
66. 66.
    Wang-Sattler R, Yu Z, Herder C, Messias AC, Floegel A, He Y, et al. Novel biomarkers for pre-diabetes identified by metabolomics. Mol Syst Biol. 2012;8:615.CrossRefPubMedPubMedCentralGoogle Scholar
67. 67.
    Ferrannini E, Natali A, Camastra S, Nannipieri M, Mari A, Adam K-P, et al. Early metabolic markers of the development of dysglycemia and type 2 diabetes and their physiological significance. Diabetes. 2013;62:1730–7.CrossRefPubMedPubMedCentralGoogle Scholar
68. 68.
    Floegel A, Stefan N, Yu Z, Mühlenbruch K, Drogan D, Joost H-G, et al. Identification of serum metabolites associated with risk of type 2 diabetes using a targeted metabolomic approach. Diabetes. 2013;62:639–48.CrossRefPubMedPubMedCentralGoogle Scholar
69. 69.
    Zhao Y-Y, Wang H-L, Cheng X-L, Wei F, Bai X, Lin R-C, et al. Metabolomics analysis reveals the association between lipid abnormalities and oxidative stress, inflammation, fibrosis, and Nrf2 dysfunction in aristolochic acid-induced nephropathy. Sci Rep. 2015;5:12936.CrossRefPubMedPubMedCentralGoogle Scholar
70. 70.
    Miller DB, Karoly ED, Jones JC, Ward WO, Vallanat BD, Andrews DL, et al. Inhaled ozone (O3)-induces changes in serum metabolomic and liver transcriptomic profiles in rats. Toxicol Appl Pharmacol. 2015;286:65–79.CrossRefPubMedPubMedCentralGoogle Scholar
71. 71.
    Miller DB, Ghio AJ, Karoly ED, Bell LN, Snow SJ, Madden MC, et al. Ozone exposure increases circulating stress hormones and lipid metabolites in humans. Am J Respir Crit Care Med. 2016;193:1382–91.CrossRefPubMedPubMedCentralGoogle Scholar
72. 72.
    Kodavanti UP. Air pollution and insulin resistance: do all roads lead to Rome? Diabetes. 2015;64:712–4.CrossRefPubMedGoogle Scholar
73. 73.
    Vella RE, Pillon NJ, Zarrouki B, Croze ML, Koppe L, Guichardant M, et al. Ozone exposure triggers insulin resistance through muscle c-Jun N-terminal kinase activation. Diabetes. 2015;64:1011–24.CrossRefPubMedGoogle Scholar
74. 74.
    Wei Y, Zhang J, Li Z, Gow A, Chung KF, Hu M, et al. Chronic exposure to air pollution particles increases the risk of obesity and metabolic syndrome: findings from a natural experiment in Beijing. FASEB J. 2016;30:2115–22.CrossRefPubMedGoogle Scholar
75. 75.
    Bolton JL, Smith SH, Huff NC, Gilmour MI, Foster WM, Auten RL, et al. Prenatal air pollution exposure induces neuroinflammation and predisposes offspring to weight gain in adulthood in a sex-specific manner. FASEB J. 2012;26:4743–54.CrossRefPubMedGoogle Scholar
76. 76.
    Elmquist JK, Scherer PE. The cover. Neuroendocrine and endocrine pathways of obesity. JAMA. 2012;308:1070–1.CrossRefPubMedGoogle Scholar
77. 77.
    Kodavanti UP. Stretching the stress boundary: linking air pollution health effects to a neurohormonal stress response. Biochim Biophys Acta. 2016;1860:2880–90.CrossRefPubMedGoogle Scholar
78. 78.
    Gackière F, Saliba L, Baude A, Bosler O, Strube C. Ozone inhalation activates stress-responsive regions of the CNS. J Neurochem. 2011;117:961–72.CrossRefPubMedGoogle Scholar
79. 79.
    Beamish LA, Osornio-Vargas AR, Wine E. Air pollution: an environmental factor contributing to intestinal disease. J Crohns Colitis. 2011;5:279–86.CrossRefPubMedGoogle Scholar
80. 80.
    Möller W, Häussinger K, Winkler-Heil R, Stahlhofen W, Meyer T, Hofmann W, et al. Mucociliary and long-term particle clearance in the airways of healthy nonsmoker subjects. J Appl Physiol. 2004;97(6):2200–6.CrossRefPubMedGoogle Scholar
81. 81.
    Nemmar A, Hoet PM, Vanquickenborne B, Dinsdale D, Thomeer M, Hoylaerts MF, et al. Passage of inhaled particles into the blood circulation in humans. Circulation. 2002;105:411–4.CrossRefPubMedGoogle Scholar
82. 82.
    Salim SY, Kaplan GG, Madsen KL. Air pollution effects on the gut microbiota: a link between exposure and inflammatory disease. Gut Microbes. 2014;5:215–9.CrossRefPubMedGoogle Scholar
83. 83.
    Dybdahl M. DNA adduct formation and oxidative stress in colon and liver of Big Blue(R) rats after dietary exposure to diesel particles. Carcinogenesis. 2003;24:1759–66.CrossRefPubMedGoogle Scholar
84. 84.
    Kish L, Hotte N, Kaplan GG, Vincent R, Tso R, Gänzle M, et al. Environmental particulate matter induces murine intestinal inflammatory responses and alters the gut microbiome. PLoS ONE. 2013a;8:e62220.CrossRefPubMedPubMedCentralGoogle Scholar
85. 85.
    Mutlu EA, Engen PA, Soberanes S, Urich D, Forsyth CB, Nigdelioglu R, et al. Particulate matter air pollution causes oxidant-mediated increase in gut permeability in mice. Part Fibre Toxicol. 2011;8:19.CrossRefPubMedPubMedCentralGoogle Scholar
86. 86.
    Kish L, Hotte N, Kaplan GG, Vincent R, Tso R, Gänzle M, et al. Environmental particulate matter induces murine intestinal inflammatory responses and alters the gut microbiome. PLoS One. 2013b;8:e62220.CrossRefPubMedPubMedCentralGoogle Scholar
87. 87.
    Shen J, Obin MS, Zhao L. The gut microbiota, obesity and insulin resistance. Mol Asp Med. 2013;34:39–58.CrossRefGoogle Scholar
88. 88.
    Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31.CrossRefPubMedGoogle Scholar
89. 89.
    Amar J, Lange C, Payros G, Garret C, Chabo C, Lantieri O, et al. Blood microbiota dysbiosis is associated with the onset of cardiovascular events in a large general population: the D.E.S.I.R. study. PLoS One. 2013;8:e54461.CrossRefPubMedPubMedCentralGoogle Scholar
90. 90.
    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;105:2412–9.CrossRefPubMedPubMedCentralGoogle Scholar
91. 91.
    Kaplan GG, Szyszkowicz M, Fichna J, Rowe BH, Porada E, Vincent R, et al. Non-specific abdominal pain and air pollution: a novel association. PLoS One. 2012;7:e47669.CrossRefPubMedPubMedCentralGoogle Scholar
92. 92.
    Alderete TL, Jones RB, Chen Z, Kim JS, Habre R, Lurmann F, et al. Exposure to traffic-related air pollution and the composition of the gut microbiota in overweight and obese adolescents. Environ Res. 2017b;161:472–8.CrossRefGoogle Scholar
93. 93.
    Lerner A, Neidhöfer S, Matthias T. The gut microbiome feelings of the brain: a perspective for non-microbiologists. Microorganisms. 2017;12;5(4).  https://doi.org/10.3390/microorganisms.