Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Changes in extrapulmonary organs and serum enzyme biomarkers after chronic exposure to Buenos Aires air pollution

  • 31 Accesses

Abstract

Urban air pollution is a serious environmental problem in developing countries worldwide, and health is a pressing issue in the megacities in Latin America. Buenos Aires is a megacity with an estimated moderate Air Quality Index ranging from 42 to 74 μg/m3. Exposure to Urban Air Particles from Buenos Aires (UAP-BA) induces morphological and physiological respiratory alterations; nevertheless, no studies on extrapulmonary organs have been performed. The aim of the present study was to explore the health effects of chronic exposure to UAP-BA (1, 6, 9, and 12 months) on the liver, heart, and serum risk biomarkers. BALB/c mice were exposed to UAP-BA or filtered air (FA) in inhalation chambers, and liver and heart histopathology, oxidative metabolism (superoxide dismutase, SOD; catalase, CAT; lipoperoxidation, TBARS), amino transaminases (AST, ALT) as serum risk biomarkers, alkaline phosphatase (ALP), paraxonase-1 (PON-1), and lipoprotein-associated phospholipase A2 (Lp-PLA2) were evaluated. Chronic exposure to real levels of UAP in Buenos Aires led to alterations in extrapulmonary organs associated with inflammation and oxidative imbalance and to changes in liver and heart risk biomarkers. Our results may reflect the impact of the persistent air pollution in Buenos Aires on individuals living in this Latin American megacity.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. Arciello M, Gori M, Maggio R, Barbaro B, Tarocchi M, Galli A, Balsano C (2013) Environmental pollution: a tangible risk for NAFLD pathogenesis. Int J Mol Sci 14:22052–22066. https://doi.org/10.3390/ijms141122052

  2. ATSDR (2016) Polycyclic aromatic hydrocarbons (PAHs). What health effects are associated with PAH exposure? https://www.atsdr.cdc. gov/csem/csem.asp?csem¼13&po¼11. Accessed 11 November 2019

  3. Avila-Costa MR, Colín-Barenque L, Zepeda-Rodríguez A, Antuna SB, Saldivar OL, Espejel-Maya G, Mussali-Galante P, del Carmen A-CM, Reyes-Olivera A, Anaya-Martinez V, Fortoul TI (2005) Ependymal epithelium disruption after vanadium pentoxide inhalation: a mice experimental model. Neurosci Lett 381:21–25. https://doi.org/10.1016/j.neulet.2005.01.072

  4. Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Organ J 5:9–19. https://doi.org/10.1097/WOX.0b013e3182439613

  5. Blank ML, Hall MN, Cress EA, Snyder F (1983) Inactivation of 1-alkyl-2-acetyl-sn-glycero-3-phosphocholine by a plasma acetylhydrolase: higher activities in hypertensive rats. Biochem Biophys Res Commun 113:666–671. https://doi.org/10.1016/0006-291x(83)91778-3

  6. Bogo H, Otero M, Castro P, Ozafrán MJ, Kreiner A, Calvo EJ, Negri RM (2003) Study of atmospheric particulate matter in Buenos Aires city. Atmos Environ 37:1135–1147. https://doi.org/10.1016/S1352-2310(02)00977-9

  7. Brook RD (2008) Cardiovascular effects of air pollution. Clin Sci (Lond) 115:175–187. https://doi.org/10.1042/cs20070444

  8. Brook RD, Rajagopalan S, Pope CA 3rd, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong Y, Luepker RV, Mittleman MA, Peters A, Siscovick D, Smith SC Jr, Whitsel L, Kaufman JD (2010) Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association. Circulation 121:2331–2378. https://doi.org/10.1161/CIR.0b013e3181dbece1

  9. Camps J, Marsillach J, Joven J (2007) Measurement of serum paraoxonase-1 activity as a potential biomarker for chronic liver impairment. Clin Chim Acta 386:114–115. https://doi.org/10.1016/j.cca.2007.07.016

  10. Camps J, Marsillach J, Joven J (2009) Measurement of serum paraoxonase-1 activity in the evaluation of liver function. World J Gastroenterol 15:1929–1933. https://doi.org/10.3748/wjg.15.1929

  11. Cohen B (2006) Urbanization in developing countries: current trends, future projections, and key challenges for sustainability. Technol Soc 28:63–80. https://doi.org/10.1016/j.techsoc.2005.10.005

  12. De Stefano A, Mannucci L, Tamburi F, Cardillo C, Schinzari F, Rovella V, Nisticò S, Bennardo L, Di Daniele N, Tesauro M (2019) Lp-PLA(2), a new biomarker of vascular disorders in metabolic diseases. Int J Immunopathol Pharmacol 33:2058738419827154–2058738419827154. https://doi.org/10.1177/2058738419827154

  13. Dey T, Gogoi K, Unni B, Bharadwaz M, Kalita M, Ozah D, Kalita M, Kalita J, Baruah PK, Bora T (2015) Role of environmental pollutants in liver physiology: special references to peoples living in the oil drilling sites of Assam. PLoS One 10:e0123370. https://doi.org/10.1371/journal.pone.0123370

  14. Dick CAJ, Singh P, Daniels M, Evansky P, Becker S, Gilmour M (2004) Murine pulmonary inflammatory responses following instillation of size-fractionated ambient particulate matter. J Toxicol Environ Health A 66:2193–2207. https://doi.org/10.1080/716100636

  15. Esen F, Tasdemir Y, Vardar N (2008) Atmospheric concentrations of PAHs, their possible sources and gas-to-particle partitioning at a residential site of Bursa, Turkey. Atmos Res 88:243–255. https://doi.org/10.1016/j.atmosres.2007.11.022

  16. Ferraro SA, Yakisich JS, Gallo FT, Tasat DR (2011) Simvastatin pretreatment prevents ambient particle-induced lung injury in mice. Inhal Toxicol 23:889–896. https://doi.org/10.3109/08958378.2011.623195

  17. Franchini M, Mannucci PM (2007) Short-term effects of air pollution on cardiovascular diseases: outcomes and mechanisms. J Thromb Haemost 5:2169–2174. https://doi.org/10.1111/j.1538-7836.2007.02750.x

  18. Furlong CE, Richter RJ, Seidel SL, Costa LG, Motulsky AG (1989) Spectrophotometric assays for the enzymatic hydrolysis of the active metabolites of chlorpyrifos and parathion by plasma paraoxonase/arylesterase. Anal Biochem 180:242–247. https://doi.org/10.1016/0003-2697(89)90424-7

  19. Hatch GE (2010) Pollution and oxidative stress in schoolchildren. Indian Pediatr 47:229–230. https://doi.org/10.1007/s13312-010-0040-3

  20. INDEC (2010). Censo Nacional de Población, Hogares y Viviendas 2010, Censo del Bicentenario. https://www.indec.gob.ar/ftp/cuadros/poblacion/censo2010_tomo1.pdf.

  21. Kim H-J, Min J-Y, Seo Y-S, Min K-B (2019) Association of ambient air pollution with increased liver enzymes in Korean adults. Int J Environ Res Public Health 16:1213. https://doi.org/10.3390/ijerph16071213

  22. Kim JW, Park S, Lim CW, Lee K, Kim B (2014) The role of air pollutants in initiating liver disease. Toxicol Res 30:65–70. https://doi.org/10.5487/TR.2014.30.2.065

  23. Kumar P, Morawska L, Birmili W, Paasonen P, Hu M, Kulmala M, Harrison RM, Norford L, Britter R (2014) Ultrafine particles in cities. Environ Int 66:1–10. https://doi.org/10.1016/j.envint.2014.01.013

  24. Kunzli N, Medina S, Kaiser R, Quenel P, Horak F Jr, Studnicka M (2001) Assessment of deaths attributable to air pollution: should we use risk estimates based on time series or on cohort studies? Am J Epidemiol 153:1050–1055. https://doi.org/10.1093/aje/153.11.1050

  25. Lemos M, Mohallen SV, Macchione M, Dolhnikoff M, Assunção JV, Godleski JJ, Saldiva PHN (2006) Chronic exposure to urban air pollution induces structural alterations in murine pulmonary and coronary arteries. Inhal Toxicol 18:247–253. https://doi.org/10.1080/08958370500444247

  26. Li R, Navab M, Pakbin P, Ning Z, Navab K, Hough G, Morgan TE, Finch CE, Araujo JA, Fogelman AM, Sioutas C, Hsiai T (2013) Ambient ultrafine particles alter lipid metabolism and HDL anti-oxidant capacity in LDLR-null mice. J Lipid Res 54:1608–1615. https://doi.org/10.1194/jlr.M035014

  27. Litvinov D, Mahini H, Garelnabi M (2012) Antioxidant and anti-inflammatory role of paraoxonase 1: implication in arteriosclerosis diseases. N Am J Med Sci 4:523–532. https://doi.org/10.4103/1947-2714.103310

  28. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275 http://www.ncbi.nlm.nih.gov/pubmed/14907713

  29. Llesuy S, Evelson P, González-Flecha B, Peralta J, Carreras MC, Poderoso JJ, Boveris A (1994) Oxidative stress in muscle and liver of rats with septic syndrome. Free Radic Biol Med 16:445–451. https://doi.org/10.1016/0891-5849(94)90121-X

  30. Maglione G, Kurtz M, Orona N, Astort F, Tavera Busso I, Mandalunis P, Berra A, Tasat D (2019) Chronic exposure to urban air pollution from Buenos Aires: the ocular mucosa as an early biomarker. Environ Sci Pollut Res Int 26:27444–27456. https://doi.org/10.1007/s11356-019-05966-6

  31. Markevych I, Wolf K, Hampel R, Breitner S, Schneider A, von Klot S, Cyrys J, Heinrich J, Döring A, Beelen R, Koenig W, Peters A (2013) Air pollution and liver enzymes. Epidemiology 24:934–935. https://doi.org/10.1097/EDE.0b013e3182a77600

  32. Martin S, Dawidowski L, Mandalunis P, Cereceda-Balic F, Tasat DR (2007) Characterization and biological effect of Buenos Aires urban air particles on mice lungs. Environ Res 105:340–349. https://doi.org/10.1016/j.envres.2007.04.009

  33. Martinez N, White V, Kurtz M, Higa R, Capobianco E, Jawerbaum A (2011) Activation of the nuclear receptor PPARalpha regulates lipid metabolism in foetal liver from diabetic rats: implications in diabetes-induced foetal overgrowth. Diabetes Metab Res Rev 27:35–46. https://doi.org/10.1002/dmrr.1151

  34. Maehly AC, Chance B (1954) The assay of catalases and peroxidases. Methods Biochem Anal 1:357–424. https://doi.org/10.1002/9780470110171.ch14

  35. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175 https://www.ncbi.nlm.nih.gov/pubmed/4623845

  36. Mohankumar S, Senthilkumar P (2017) Particulate matter formation and its control methodologies for diesel engine: a comprehensive review. Renew Sust Energ Rev 80:1227–1238. https://doi.org/10.1016/j.rser.2017.05.133

  37. Neuschwander-Tetri BA (2010) Hepatic lipotoxicity and the pathogenesis of nonalcoholic steatohepatitis: the central role of nontriglyceride fatty acid metabolites. Hepatology 52:774–788. https://doi.org/10.1002/hep.23719

  38. Orona NS, Astort F, Maglione GA, Saldiva PH, Yakisich JS, Tasat DR (2014) Direct and indirect air particle cytotoxicity in human alveolar epithelial cells. Toxicol in Vitro 28:796–802. https://doi.org/10.1016/j.tiv.2014.02.011

  39. Orona NS, Ferraro SA, Astort F, Morales C, Brites F, Boero L, Tiscornia G, Maglione GA, Saldiva PHN, Yakisich S, Tasat DR (2016) Acute exposure to Buenos Aires air particles (UAP-BA) induces local and systemic inflammatory response in middle-aged mice: a time course study. Environ Pollut 208:261–270. https://doi.org/10.1016/j.envpol.2015.07.020

  40. Pope CA 3rd, Burnett RT, Thurston GD, Thun MJ, Calle EE, Krewski D, Godleski JJ (2004) Cardiovascular mortality and long-term exposure to particulate air pollution: epidemiological evidence of general pathophysiological pathways of disease. Circulation 109:71–77. https://doi.org/10.1161/01.cir.0000108927.80044.7f

  41. Pope CA 3rd, Dockery DW (2006) Health effects of fine particulate air pollution: lines that connect. J Air Waste Manag Assoc 56:709–742. https://doi.org/10.1080/10473289.2006.10464485

  42. Ravindra K, Sokhi R, Van Grieken R (2008) Atmospheric polycyclic aromatic hydrocarbons: source attribution, emission factors and regulation. Atmos Environ 42:2895–2921. https://doi.org/10.1016/j.atmosenv.2007.12.010

  43. Schins RP, Lightbody JH, Borm PJ, Shi T, Donaldson K, Stone V (2004) Inflammatory effects of coarse and fine particulate matter in relation to chemical and biological constituents. Toxicol Appl Pharmacol 195:1–11. https://doi.org/10.1016/j.taap.2003.10.002

  44. Smichowski P, Gomez DR, Dawidowski LE, Fernanda Gine M, Claudia Sanchez Bellato A, Reich SL (2004) Monitoring trace metals in urban aerosols from Buenos Aires city. Determination by plasma-based techniques. J Environ Monit 6:286–294. https://doi.org/10.1039/B312446K

  45. Tarantino G, Capone D, Finelli C (2013) Exposure to ambient air particulate matter and non-alcoholic fatty liver disease. World J Gastroenterol 19:3951–3956. https://doi.org/10.3748/wjg.v19.i25.3951

  46. Tavera Busso I, Vera A, Mateos AC, Amarillo AC, Carreras H (2017) Histological changes in lung tissues related with sub-chronic exposure to ambient urban levels of PM 2.5 in Córdoba, Argentina. Atmos Environ 167:616–624. https://doi.org/10.1016/j.atmosenv.2017.08.061

  47. Tilg H, Moschen AR (2008) Insulin resistance, inflammation, and non-alcoholic fatty liver disease. Trends Endocrinol Metab 19:371–379. https://doi.org/10.1016/j.tem.2008.08.005

  48. United Nations (2016) The world’s cities in 2016 https://www.un.org/en/development/desa/population/publications/pdf/urbanization/the_worlds_cities_in_2016_data_booklet.pdf. Accessed 11 November 2019

  49. Upadhyay RK (2015) Emerging risk biomarkers in cardiovascular diseases and disorders. J Lipids 2015:971453–971453. https://doi.org/10.1155/2015/971453

  50. Vujovic A, Kotur-Stevuljevic J, Kornic D, Spasic S, Spasojevic-Kalimanovska V, Bogavac-Stanojevic N, Stefanovic A, Deanovic M, Babka S, Aleksic B, Jelic-Ivanovic Z (2010) Oxidative stress and anti-oxidative defense in schoolchildren residing in a petrochemical industry environment. Indian Pediatr 47:233–239. https://doi.org/10.1007/s13312-010-0045-y

  51. Wang X, Bi X, Sheng G, Fu J (2006) Chemical composition and sources of PM10 and PM2.5 aerosols in Guangzhou, China. Environ Monit Assess 119:425–439. https://doi.org/10.1007/s10661-005-9034-3

  52. Wang WY, Zhang J, Wu WY, Li J, Ma YL, Chen WH, Yan H, Wang K, Xu WW, Shen JH, Wang YP (2011) Inhibition of lipoprotein-associated phospholipase A2 ameliorates inflammation and decreases atherosclerotic plaque formation in ApoE-deficient mice. PLoS One 6:e23425. https://doi.org/10.1371/journal.pone.0023425

  53. Warnick GR, Mayfield C, Benderson J, Chen JS, Albers JJ (1982) HDL cholesterol quantitation by phosphotungstate-Mg2+ and by dextran sulfate-Mn2+-polyethylene glycol precipitation, both with enzymic cholesterol assay compared with the lipid research method. Am J Clin Pathol 78:718–723. https://doi.org/10.1093/ajcp/78.5.718

  54. Wold LE, Ying Z, Hutchinson KR, Velten M, Gorr MW, Velten C, Youtz DJ, Wang A, Lucchesi PA, Sun Q, Rajagopalan S (2012) Cardiovascular remodeling in response to long-term exposure to fine particulate matter air pollution. Circ Heart Fail 5:452–461. https://doi.org/10.1161/circheartfailure.112.966580

  55. Xu J, Jin T, Miao Y, Han B, Gao J, Bai Z, Xu X (2015) Individual and population intake fractions of diesel particulate matter (DPM) in bus stop microenvironments. Environ Pollut 207:161–167. https://doi.org/10.1016/j.envpol.2015.09.005

  56. Yin F, Lawal A, Ricks J, Fox JR, Larson T, Navab M, Fogelman AM, Rosenfeld ME, Araujo JA (2013) Diesel exhaust induces systemic lipid peroxidation and development of dysfunctional pro-oxidant and pro-inflammatory high-density lipoprotein. Arterioscler Thromb Vasc Biol 33:1153–1161. https://doi.org/10.1161/atvbaha.112.300552

  57. Zhang Y-L, Cao F (2015) Fine particulate matter (PM2.5) in China at a city level. Sci Rep 5:14884. https://doi.org/10.1038/srep14884

  58. Zheng Z, Xu X, Zhang X, Wang A, Zhang C, Hüttemann M, Grossman LI, Chen LC, Rajagopalan S, Sun Q, Zhang K (2013) Exposure to ambient particulate matter induces a NASH-like phenotype and impairs hepatic glucose metabolism in an animal model. J Hepatol 58:148–154. https://doi.org/10.1016/j.jhep.2012.08.009

  59. Zheng Z, Zhang X, Wang J, Dandekar A, Kim H, Qiu Y, Xu X, Cui Y, Wang A, Chen LC, Rajagopalan S, Sun Q, Zhang K (2015) Exposure to fine airborne particulate matters induces hepatic fibrosis in murine models. J Hepatol 63:1397–1404. https://doi.org/10.1016/j.jhep.2015.07.020

Download references

Acknowledgments

The authors specially thank Dr. Patricia Mandalunis and Ms. Mariela Lacave for their technical expertise on the histological study.

Funding

This work was partially funded by Grants: PICT 2017-1309, PICT 2017-4549, and PICT 2015-0853 from the National Agency for the Promotion of Science and Technology, Argentina.

Author information

Correspondence to Guillermo Alberto Maglione.

Ethics declarations

The experimental protocol was approved by the Ethics Committee of the University of Buenos Aires, and all procedures were conducted in keeping with the 6344/ 96 regulations of the National Drug, Food, and Medical Technology Administration (ANMAT) of Argentina.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Philippe Garrigues

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Maglione, G.A., Kurtz, M.L., Orona, N.S. et al. Changes in extrapulmonary organs and serum enzyme biomarkers after chronic exposure to Buenos Aires air pollution. Environ Sci Pollut Res (2020). https://doi.org/10.1007/s11356-020-07996-x

Download citation

Keywords

  • Buenos Aires
  • Urban air pollution
  • Chronic exposure
  • Liver
  • Heart
  • Serum risk biomarkers