Investigating the spill-over hypothesis: Analysis of the association between local inflammatory markers in sputum and systemic inflammatory mediators in plasma

Environmental Research

Volumn 134, Issue , 2014, Pages 24-32

  Teichert, Tom ^a   Vossoughi, Mohammad ^b   Vierkötter, Andrea ^b   Sugiri, Dorothea ^b   Schikowski, Tamara ^b,c,d   Hoffmann, Barbara ^b,e   Schulte, Thomas ^e   Roden, Michael ^a,f   Raulf Heimsoth, Monika ^g   Luckhaus, Christian ^e   Krämer, Ursula ^b   Herder, Christian ^a  

^a LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

^b IUF LEIBNIZ RESEARCH INSTITUTE FOR ENVIRONMENTAL MEDICINE   (Germany)

^c SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^d UNIVERSITY OF BASEL   (Switzerland)

^e HEINRICH HEINE UNIVERSITY   (Germany)

^f UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^g RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Airway inflammation; Cytokines; Induced sputum; Subclinical inflammation; Systemic inflammation

Indexed keywords

ADIPONECTIN; BIOLOGICAL MARKER; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; EOSINOPHIL CATIONIC PROTEIN; GAMMA INTERFERON; GELATINASE B; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 8; LEPTIN; LEUKOTRIENE B4; LEUKOTRIENE C4; LEUKOTRIENE D4; LEUKOTRIENE E4; MATRIX METALLOPROTEINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRITE; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; ADIPOCYTOKINE; CELL ADHESION MOLECULE; CHEMOKINE; CYTOKINE; LEUKOTRIENE; LEUKOTRIENE C; LEUKOTRIENE D; UNCLASSIFIED DRUG; AUTACOID;

AGED; AGING; AIR POLLUTANT; AIR POLLUTION; ANTHROPOMETRY; ARTICLE; BODY MASS; CHRONIC OBSTRUCTIVE LUNG DISEASE; CROSS-SECTIONAL STUDY; EXPOSURE; FEMALE; HUMAN; LUNG FUNCTION; MOLECULAR WEIGHT; PASSIVE SMOKING; PHENOTYPE; PLASMA; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN SPUTUM LEVEL; SPUTUM; SPUTUM LEVEL; BLOOD SAMPLING; COHORT ANALYSIS; CONFOUNDING VARIABLE; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE ASSOCIATION; ENVIRONMENTAL EXPOSURE; HISTOPATHOLOGY; HYPOTHESIS; MAJOR CLINICAL STUDY; MEDIATOR; RESPIRATORY TRACT INFLAMMATION; SPUTUM ANALYSIS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; BLOOD; METABOLISM;

ATMOSPHERIC POLLUTION; BIOASSAY; BIOMARKER; CANCER; CARDIOVASCULAR DISEASE; CORRELATION; ELDERLY POPULATION; MUCUS; PLASMA; POLLUTION EXPOSURE; RESPIRATORY DISEASE; RISK ASSESSMENT; RISK FACTOR; WOMENS HEALTH;

AGED; BIOLOGICAL MARKERS; CROSS-SECTIONAL STUDIES; HUMANS; INFLAMMATION MEDIATORS; SPUTUM;

EID: 84904507699     PISSN: 00139351     EISSN: 10960953     Source Type: Journal    
DOI: 10.1016/j.envres.2014.06.021     Document Type: Article

References (62)

1. Agustí A., Edwards L.D., Rennard S.I., MacNee W., Tal-Singer R., Miller B.E., Vestbo J., Lomas D.A., Calverley P.M.A., Wouters E., Crim C., Yates J.C., Silverman E.K., Coxson H.O., Bakke P., Mayer R.J., Celli B. Persistent systemic inflammation is associated with poor clinical outcomes in COPD: a novel phenotype. PLoS One 2012, 7:e37483. 10.1371/journal.pone.0037483.s009.
2. Baeza-Squiban A., Bonvallot V., Boland S., Marano F. Airborne particles evoke an inflammatory response in human airway epithelium. Activation of transcription factors. Cell Biol. Toxicol. 1999, 15:375-380. 10.1023/A:1007653900063.
3. Bai N., Khazaei M., van Eeden S.F., Laher I. The pharmacology of particulate matter air pollution-induced cardiovascular dysfunction. Pharmacol. Ther. 2007, 113:16-29. 10.1016/j.pharmthera.2006.06.005.
4. Becker S., Mundandhara S., Devlin R., Madden M. Regulation of cytokine production in human alveolar macrophages and airway epithelial cells in response to ambient air pollution particles: further mechanistic studies. Toxicol. Appl. Pharmacol. 2005, 207:269-275. 10.1016/j.taap.2005.01.023.
5. Broekhuizen R., Vernooy J., Schols A., Dentener M., Wouters E. Leptin as local inflammatory marker in COPD. Respir. Med. 2005, 99:70-74. 10.1016/j.rmed.2004.03.029.
6. Brook R.D., Rajagopalan S., Pope C.A., Brook J.R., Bhatnagar A., Diez-Roux A.V., Holguin F., Hong Y., Luepker R.V., Mittleman M.A., Peters A., Siscovick D., Smith S.C., Whitsel L., Kaufman J.D. Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association. Circulation 2010, 121:2331-2378. 10.1161/CIR.0b013e3181dbece1.
7. Brunekreef B., Holgate S. Air pollution and health. Lancet 2002, 360:1233-1242. 10.1016/S0140-6736(02)11274-8.
8. Carstensen M., Herder C., Kivimäki M., Jokela M., Roden M., Shipley M.J., Witte D.R., Brunner E.J., Tabák A.G. Accelerated increase in serum interleukin-1 receptor antagonist starts 6 years before diagnosis of type 2 diabetes-Whitehall II prospective cohort study. Diabetes 2010, 59:1222-1227. 10.2337/db09-1199.
9. Danesh J., Kaptoge S., Mann A., Sarwar N., Wood A., Angleman S., Wensley F., Higgins J., Lennon L., Eiriksdottir G., Rumley A., Whincup P., Lowe G.D., Gudnason V. Long-term interleukin-6 levels and subsequent risk of coronary heart disease: two new prospective studies and a systematic review. PLoS Med. 2008, 5:e78. 10.1371/journal.pmed.
10. Decramer M., Janssens W., Miravitlles M. Chronic obstructive pulmonary disease. Lancet 2012, 379:1341-1351. 10.1016/S0140-6736(11)60968-9.
11. Eagan T.M.L., Ueland T., Wagner P.D., Hardie J.A., Mollnes T.E., Damas J.K., Aukrust P., Bakke P.S. Systemic inflammatory markers in COPD: results from the Bergen COPD cohort study. Eur. Respir. J. 2010, 35:540-548. 10.1183/09031936.00088209.
12. Fujii T., Hayashi S., Hogg J., Vincent R., van Eeden S. Particulate matter induces cytokine expression in human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 2001, 25:265-271. 10.1165/ajrcmb.25.3.4445.
13. Garcia-Rio F., Miravitlles M., Soriano J., Muñoz L., Duran-Tauleria E., Sánchez G. Systemic inflammation in chronic obstructive pulmonary disease: a population-based study. Respir. Res. 2010, 11:63. 10.1186/1465-9921-11-63.
14. Ghio A., Kim C., Devlin R. Concentrated ambient air particles induce mild pulmonary inflammation in healthy human volunteers. Am. J. Respir. Crit. Care Med. 2000, 162:981-988. 10.1164/ajrccm.162.3.9911115.
15. Gilmour P., Rahman I., Hayashi S., Hogg J., Donaldson K., MacNee W. Adenoviral e1a primes alveolar epithelial cells to PM10-induced transcription of interleukin-8. Am. J. Physiol.-Lung C 2001, 281:L598-L606.
16. Gilmour P., Ziesenis A., Morrison E., Vickers M., Drost E., Ford I., Karg E., Mossa C., Schroeppel A., Ferron G. Pulmonary and systemic effects of short-term inhalation exposure to ultrafine carbon black particles. Toxicol. Appl. Pharmacol. 2004, 195:35-44. 10.1016/j.taap.2003.10.003.
17. Glantz S., Gonzalez M. Effective tobacco control is key to rapid progress in reduction of non-communicable diseases. Lancet 2012, 379:1269-1271. 10.1016/S0140-6736(11)60615-6.
18. GOLD Scientific Committee, 2013. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: Gold executive summary - updated 2013. Available at: (accessed 11.03.13). http://www.goldcopd.org.
19. Hancox R.J., Poulton R., Greene J.M., Filsell S., Mclachlan C.R., Rasmussen F., Taylor D.R., Williams M.J.A., Williamson A., Sears M.R. Systemic inflammation and lung function in young adults. Thorax 2007, 62:1064-1068. 10.1136/thx.2006.076877.
20. Herder C., Baumert J., Zierer A., Roden M., Meisinger C., Karakas M., Chambless L., Rathmann W., Peters A., Koenig W. Immunological and cardiometabolic risk factors in the prediction of type 2 diabetes and coronary events: MONICA/KORA Augsburg case-cohort study. PLoS One 2011, 6:e19852. 10.1371/journal.pone.0019852.
21. Herder C., Carstensen M., Ouwens D. Anti-inflammatory cytokines and risk of type 2 diabetes. Diabetes Obes. Metab. 2013, 3(Suppl.):S39-S50. 10.1111/dom.12155.
22. Herder C., Peltonen M., Svensson P.-A., Carstensen M., Jacobson P., Roden M., Sjörström L., Carlsson L. Adiponectin and bariatric surgery: associations with diabetes and cardiovascular disease in the swedish obese subjects study. Diabetes Care 2014, 37:1401-1409. 10.2337/dc13-1362.
23. Hetland R., Cassee F., Refsnes M., Schwarze P., Låg M., Boere A., Dybing E. Release of inflammatory cytokines, cell toxicity and apoptosis in epithelial lung cells after exposure to ambient air particles of different size fractions. Toxicol. in vitro 2004, 18:203-212. 10.1016/S0887-2333(03)00142-5.
24. Hoffmann B., Moebus S., Dragano N., Stang A., Mohlenkamp S., Schmermund A., Memmesheimer M., Brocker-Preuss M., Mann K., Erbel R., Jockel K.H. Chronic residential exposure to particulate matter air pollution and systemic inflammatory markers. Environ. Health Perspect. 2009, 117:1302-1308. 10.1289/ehp.0800362.
25. Huertas A., Palange P. COPD: a multifactorial systemic disease. Ther. Adv. Respir. Dis. 2011, 5:217-224. 10.1177/1753465811400490.
26. Hurst J.R., Donaldson G.C., Perera W.R., Wilkinson T.M.A., Bilello J.A., Hagan G.W., Vessey R.S., Wedzicha J.A. Use of plasma biomarkers at exacerbation of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2006, 174:867-874. 10.1164/rccm.200604-506OC.
27. Krämer U., Herder C., Sugiri D., Strassburger K., Schikowski T., Ranft U., Rathmann W. Traffic-related air pollution and incident type 2 diabetes: results from the SALIA cohort study. Environ. Health Perspect. 2010, 118:1273-1279. 10.1289/ehp.0901689.
28. Kumar L., Rajput N., Majumdar S. Nitric oxide metabolites in induced sputum: a noninvasive marker of airway inflammation in asthma. Indian Pediatr. 2005, 42:329-337.
29. Lu Y., Feng L., Feng L., Nyunt M., Yap K., Ng T. Systemic inflammation, depression and obstructive pulmonary function: a population-based study. Respir. Res. 2013, 14:53. 10.1186/1465-9921-14-53.
30. MacNee W. Systemic inflammatory biomarkers and co-morbidities of chronic obstructive pulmonary disease. Ann. Med. 2013, 45:291-300. 10.3109/07853890.2012.732703.
31. Michael S., Montag M., Dott W. Pro-inflammatory effects and oxidative stress in lung macrophages and epithelial cells induced by ambient particulate matter. Environ. Pollut. 2013, 183:19-29. 10.1016/j.envpol.2013.01.026.
32. Mohamed N.A., Fawzy M.A., Elgamry R., Gad D.M., Ibraheem H.A. Role of adiponectin and other inflammatory biomarkers in COPD patients. Egypt. J. Chest Dis. Tuberc. 2013, 62:45-50. 10.1016/j.ejcdt.2013.03.005.
33. Ouchi N., Parker J., Lugus J., Walsh K. Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 2011, 11:85-97. 10.1038/nri2921.
34. Pradhan A.D., Manson J.E., Rifai N., Buring J.E., Ridker P.M. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 2001, 286:327-334. 10.1001/jama.286.3.327.
35. Raaschou-Nielsen O., Andersen Z.J., Hvidberg M., Jensen S.S., Ketzel M., Sørensen M., Hansen J., Loft S., Overvad K., Tjønneland A. Air pollution from traffic and cancer incidence: a Danish cohort study. Environ. Health 2011, 10:67. 10.1186/1476-069X-10-67.
36. Raaschou-Nielsen O., Andersen Z.J., Hvidberg M., Jensen S.S., Ketzel M., Sørensen M., Loft S., Overvad K., Tjønneland A. Lung cancer incidence and long-term exposure to air pollution from traffic. Environ. Health Perspect. 2011, 119:860-865. 10.1289/ehp.1002353.
37. Rajagopalan S., Brook R.D. Air pollution and type 2 diabetes: mechanistic insights. Diabetes 2012, 61:3037-3045. 10.2337/db12-0190.
38. Ranft U., Schikowski T., Sugiri D., Krutmann J., Krämer U. Long-term exposure to traffic-related particulate matter impairs cognitive function in the elderly. Environ. Res. 2009, 109:1004-1011. 10.1016/j.envres.2009.08.003.
39. Raulf-Heimsoth M., Pesch B., Kendzia B., Spickenheuer A., Bramer R., Marczynski B., Merget R., Brüning T. Irritative effects of vapours and aerosols of bitumen on the airways assessed by non-invasive methods. Arch. Toxicol. 2011, 85:41-52. 10.1007/s00204-011-0681-6.
40. Ridker P.M., Hennekens C., Roitman-Johnson B., Stampfer M., Allen J. Plasma concentration of soluble intercellular adhesion molecule 1 and risks of future myocardial infarction in apparently healthy men. Lancet 1998, 351:88-92. 10.1016/S0140-6736(97)09032-6.
41. Röpcke S., Holz O., Lauer G., Müller M., Rittinghausen S., Ernst P., Lahu G., Elmlinger M., Krug N., Hohlfeld J.M. Repeatability of and relationship between potential COPD biomarkers in bronchoalveolar lavage, bronchial biopsies, serum, and induced sputum. PLoS One 2012, 7:e46207. 10.1371/journal.pone.0046207.s011.
42. Ruckerl R., Ibald-Mulli A., Koenig W., Schneider A., Woelke G., Cyrys J., Heinrich J., Marder V., Frampton M., Wichmann H.E., Peters A. Air pollution and markers of inflammation and coagulation in patients with coronary heart disease. Am. J. Respir. Crit. Care Med. 2006, 173:432-441. 10.1164/rccm.200507-1123OC.
43. Sapey E., Ahmad A., Bayley D., Newbold P., Snell N., Rugman P., Stockley R.A. Imbalances between interleukin-1 and tumor necrosis factor agonists and antagonists in stable COPD. J. Clin. Immunol. 2009, 29:508-516. 10.1007/s10875-009-9286-8.
44. Schikowski T., Sugiri D., Ranft U., Gehring U., Heinrich J., Wichmann H.-E., Krämer U. Long-term air pollution exposure and living close to busy roads are associated with COPD in women. Respir. Res. 2005, 6. 10.1186/1465-9921-6-152.
45. Schwartz J. Air pollution and blood markers of cardiovascular risk. Environ. Health Perspect. 2001, 109:405-409.
46. Seagrave J. Mechanisms and implications of air pollution particle associations with chemokines. Toxicol. Appl. Pharmacol. 2008, 232:469-477. 10.1016/j.taap.2008.08.001.
47. Seaton A., Soutar A., Crawford V., Elton R., McNerlan S., Cherrie J., Watt M., Agius R., Stout R. Particulate air pollution and the blood. Thorax 1999, 54:1027-1032. 10.1136/thx.54.11.1027.
48. Sinden N.J., Stockley R.A. Systemic inflammation and comorbidity in copd: a result of 'overspill' of inflammatory mediators from the lungs? Review of the evidence. Thorax 2010, 65:930-936. 10.1136/thx.2009.130260.
49. Singh D., Edwards L., Tal-Singer R., Rennard S. Sputum neutrophils as a biomarker in copd: findings from the eclipse study. Respir. Res. 2010, 11. 10.1186/1465-9921-11-77.
50. Steiner M., Reinhardt K., Krammer B., Ernst B., Blann A. Increased levels of soluble adhesion molecules in type 2 (non-insulin dependent) diabetes mellitus are independent of glycaemic control. Thromb. Haemost. 1994, 72:979-984.
51. Steinvil A., Kordova-Biezuner L., Shapira I., Berliner S., Rogowski O. Short-term exposure to air pollution and inflammation-sensitive biomarkers. Environ. Res. 2008, 106:51-61. 10.1016/j.envres.2007.08.006.
52. Sun Q., Yue P., Ying Z., Cardounel A.J., Brook R.D., Devlin R., Hwang J.-S., Zweier J.L., Chen L.C., Rajagopalan S. Air pollution exposure potentiates hypertension through reactive oxygen species-mediated activation of Rho/ROCK. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1760-1766. 10.1161/ATVBAHA.108.166967.
53. Targher G., Bonadonna R., Alberiche M., Zenere M., Muggeo M., Bonora E. Relation between soluble adhesion molecules and insulin sensitivity in type 2 diabetic individuals role of adipose tissue. Diabetes Care 2001, 24:1961-1966. 10.2337/diacare.24.11.1961.
54. Teichert T., Vossoughi M., Vierkötter A., Sugiri D., Schikowski T., Schulte T., Roden M., Luckhaus C., Herder C., Krämer U. Association between traffic-related air pollution, subclinical inflammation and impaired glucose metabolism: results from the SALIA study. PLoS One 2013, 8:e83042. 10.1371/journal.pone.0083042.s002.
55. Tkacova R. Systemic inflammation in chronic obstructive pulmonary disease: may adipose tissue play a role? Review of the literature and future perspectives. Mediat. Inflamm. 2010, 2010:1-11. 10.1155/2010/585989.
56. Vernooy J.H., Küçükaycan M., Jacobs J.A., Chavannes N.H., Buurman W.A., Dentener M.A., Wouters E.F. Local and systemic inflammation in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2002, 166:1218-1224. 10.1164/rccm.2202023.
57. Vossoughi M., Schikowski T., Vierkötter A., Sugiri D., Hoffmann B., Teichert T., Herder C., Schulte T., Luckhaus C., Raulf-Heimsoth M., Casjens S., Brüning T., Krämer U. Air pollution and subclinical airway inflammation in the SALIA cohort study. Immun. Ageing 2014, 11(5). 10.1186/1742-4933-11-5.
58. Walter R., Wilk J., Larson M., Vasan R., Keaney J., Lipinska I., O'Connor G., Benjamin E. Systemic inflammation and COPD-the Framingham heart study. Chest 2008, 133:19-25. 10.1378/chest.07-0058.
59. Wang S.L., Tsai P.C., Yang C.Y., Guo Y.L. Increased risk of diabetes and polychlorinated biphenyls and dioxins. Diabetes Care 2008, 31:1574-1579. 10.2337/dc07-2449.
60. Whiteley W., Jackson C., Lewis S., Lowe G., Rumley A., Sandercock P., Wardlaw J., Dennis M., Sudlow C. Inflammatory markers and poor outcome after stroke: a prospective cohort study and systematic review of interleukin-6. PLoS Med. 2009, 6:e1000145. 10.1371/journal.pmed.1000145.
61. Xie J., Yang X.-Y., Shi J.-D., Deng X.-Q., Long W. A new inflammation marker of chronic obstructive pulmonary disease-adiponectin. World J. Emerg. Med. 2010, 1:190-195.
62. Zeng M., Wen Y., Liu L.-Y., Wang H., Guan K.-P., Huang X. Role of TNF-α, sTNF-r55 and sTNF-r75 in inflammation of acute exacerbations of chronic obstructive pulmonary disease. Respiration 2009, 78:399-403. 10.1159/000210263.