Advertisement

Environmental Science and Pollution Research

, Volume 23, Issue 11, pp 10604–10614 | Cite as

The role of the PM2.5-associated metals in pathogenesis of child Mycoplasma Pneumoniae infections: a systematic review

  • Wei Hou
  • Xijin Xu
  • Yongge Lei
  • Junjun Cao
  • Yu Zhang
  • Liang Chen
  • Xia Huo
Review Article

Abstract

The peak occurrence of Mycoplasma pneumoniae (M. pneumoniae) infections in childhood and haze episodes is concurrent. Together, the prevalence of macrolide-resistant M. pneumoniae varies among countries might also be related to the concentration of ambient fine particulate mass (aerodynamic diameter ≤2.5 μm, PM2.5). Numerous cohort studies have identified consistent associations between ambient PM2.5 and cardiorespiratory morbidity and mortality. PM2.5 is a carrier of the heavy metals. The relationship between PM2.5-associated metals and M. pneumoniae infections in childhood has been increasingly drawing public attention. First, we reviewed original articles and review papers in Pubmed and Web of Science regarding M. pneumoniae and PM2.5-associated metal and analyzed the structural basis of PM2.5-associated metal interaction with M. pneumoniae. Then, the possible mechanisms of action between them were conjectured. Mechanisms of oxidative stress induction and modulation of the host immune system and inflammatory responses via Toll-like receptors (TLRs) and/or the nuclear factor-kappa B (NF-κB) pathway are postulated to be the result of PM2.5-associated metal complex interaction with M. pneumoniae. In addition, a heavy metal effect on M. pneumoniae-expressed community-acquired respiratory distress syndrome (CARDS) toxin, and activation of the aryl hydrocarbon receptor (AhR) and TLRs to induce the differentiation of T helper (Th) cells are also regarded as important reasons for the influence of the heavy metals on the severity of M. pneumoniae pneumonia and the initial onset and exacerbation of M. pneumoniae associated asthma. PM2.5-associated metals via complex mechanisms can exert a great impact on the host through interaction with M. pneumoniae.

Keywords

M. pneumoniae Childhood PM2.5-associated-metal Oxidative stress TLR NF-κB CARDS toxin AhR 

Notes

Acknowledgments

This work was supported by the Project of International Cooperation and Innovation Platform in Guangdong Universities (2013gjhz0007) and the Education Department of Guangdong Government under the Top-tier University Development Scheme for Research and Control of Infectious Diseases (2015038). We would like to thank Dr. Stanley Lin for his constructive comments and English language editing.

Compliance with ethical standards

Ethics statement

This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Akaike H, Miyashita N, Kubo M, Kawai Y, Tanaka T, Ogita S, Kawasaki K, Nakano T, Terada K, Ouchi K, Atypical Pathogen Study Group (2012) In vitro activities of 11 antimicrobial agents against macrolide-resistant Mycoplasma pneumoniae isolates from pediatric patients: results from a multicenter surveillance study. Jpn J Infect Dis 65:535–538CrossRefGoogle Scholar
  2. Alessandria L, Schilirò T, Degan R, Traversi D, Gilli G (2014) Cytotoxic response in human lung epithelial cells and ion characteristics of urban-air particles from Torino, a northern Italian city. Environ Sci Pollut Res Int 21:5554–5564CrossRefGoogle Scholar
  3. Ani M, Moshtaghie AA, Ahmadvand H (2007) Comparative effects of copper, iron, vanadium and titanium on low density lipoprotein oxidation in vitro. Iran Biomed J 11:113–118Google Scholar
  4. Assefa S, Curtis JT, Sethi S, Davis RL, Chen Y, Kaul R (2012) Inorganic mercury exposure in prairie voles (Microtus ochrogaster) alters the expression of toll-like receptor 4 and activates inflammatory pathways in the liver in a sex-specific manner. Hum Exp Toxicol 31:376–386CrossRefGoogle Scholar
  5. Atkinson TP, Waites KB (2014) Mycoplasma pneumoniae infections in childhood. Pediatr Infect Dis J 33:92–94CrossRefGoogle Scholar
  6. Atkinson TP, Balish MF, Waites KB (2008) Epidemiology, clinical manifestations, pathogenesis and laboratory detection of Mycoplasma pneumoniae infections. FEMS Microbiol Rev 32:956–973CrossRefGoogle Scholar
  7. Averbuch D, Hidalgo-Grass C, Moses AE, Engelhard D, Nir-Paz R (2011) Macrolide resistance in Mycoplasma pneumoniae, Israel, 2010. Emerg Infect Dis 17:1079–1082CrossRefGoogle Scholar
  8. Balbi T, Smerilli A, Fabbri R, Ciacci C, Montagna M, Grasselli E, Brunelli A, Pojana G, Marcomini A, Gallo G, Canesi L (2014) Co-exposure to n-TiO2 and Cd2+ results in interactive effects on biomarker responses but not in increased toxicity in the marine bivalve M. galloprovincialis. Sci Total Environ 493:355–364CrossRefGoogle Scholar
  9. Bell ML, Ebisu K, Leaderer BP, Gent JF, Lee HJ, Koutrakis P, Wang Y, Dominici F, Peng RD (2014) Associations of PM2.5 constituents and sources with hospital admissions: analysis of four counties in Connecticut and Massachusetts (USA) for persons ≥ 65 years of age. Environ Health Perspect 122:138–144CrossRefGoogle Scholar
  10. Bray TM, Bettger WJ (1990) The physiological role of zinc as an antioxidant. Free Radic Biol Med 8:281–291CrossRefGoogle Scholar
  11. Cakmak S, Dales R, Kauri LM, Mahmud M, Van Ryswyk K, Vanos J, Liu L, Kumarathasan P, Thomson E, Vincent R, Weichenthal S (2014) Metal composition of fine particulate air pollution and acute changes in cardiorespiratory physiology. Environ Pollut 189:208–214CrossRefGoogle Scholar
  12. Cassee FR, Héroux ME, Gerlofs-Nijland ME, Kelly FJ (2013) Particulate matter beyond mass: recent health evidence on the role of fractions, chemical constituents and sources of emission. Inhal Toxicol 25:802–812CrossRefGoogle Scholar
  13. Chen F, Shi X (2002) Signaling from toxic metals to NF-kappaB and beyond: not just a matter of reactive oxygen species. Environ Health Perspect 110(Suppl 5):807–811CrossRefGoogle Scholar
  14. Chen A, Dietrich KN, Huo X, Ho SM (2011) Developmental neurotoxicants in e-waste: an emerging health concern. Environ Health Perspect 119:431–438CrossRefGoogle Scholar
  15. Chen DJ, Xu YM, Du JY, Huang DY, Lau AT (2014) Cadmium induces cytotoxicity in human bronchial epithelial cells through upregulation of eIF5A1 and NF-kappaB. Biochem Biophys Res Commun 445:95–99CrossRefGoogle Scholar
  16. Chiang WC, Teoh OH, Chong CY, Goh A, Tang JP, Chay OM (2007) Epidemiology, clinical characteristics and antimicrobial resistance patterns of community-acquired pneumonia in 1702 hospitalized children in Singapore. Respirology 12:254–261CrossRefGoogle Scholar
  17. Dagher Z, Garcon G, Billet S, Verdin A, Ledoux F, Courcot D, Aboukais A, Shirali P (2007) Role of nuclear factor-kappa B activation in the adverse effects induced by air pollution particulate matter (PM2.5) in human epithelial lung cells (L132) in culture. J Appl Toxicol 27:284–290CrossRefGoogle Scholar
  18. Duan J, Tan J (2013) Atmospheric heavy metals and arsenic in China: situation, sources and control policies. Atmos Environ 74:93–101CrossRefGoogle Scholar
  19. Dumke R, Lück C, Jacobs E (2013) Low rate of macrolide resistance in Mycoplasma pneumoniae strains in Germany between 2009 and 2012. Antimicrob Agents Chemother 57:3460CrossRefGoogle Scholar
  20. Eshaghi A, Memari N, Tang P, Olsha R, Farrell DJ, Low DE, Gubbay JB, Patel SN (2013) Macrolide-resistant Mycoplasma pneumoniae in humans, Ontario, Canada, 2010–2011. Emerg Infect Dis 19:1525–1527CrossRefGoogle Scholar
  21. Foy HM (1993) Infections caused by Mycoplasma pneumoniae and possible carrier state in different populations of patients. Clin Infect Dis 17(Suppl 1):S37–S46CrossRefGoogle Scholar
  22. Fuertes E, MacIntyre E, Agius R, Beelen R, Brunekreef B, Bucci S, Cesaroni G, Cirach M, Cyrys J, Forastiere F, Gehring U, Gruzieva O, Hoffmann B, Jedynska A, Keuken M, Klümper C, Kooter I, Korek M, Krämer U, Mölter A, Nieuwenhuijsen M, Pershagen G, Porta D, Postma DS, Simpson A, Smit HA, Sugiri D, Sunyer J, Wang M, Heinrich J (2014) Associations between particulate matter elements and early-life pneumonia in seven birth cohorts: results from the ESCAPE and TRANSPHORM projects. Int J Hyg Environ Health 217:819–829CrossRefGoogle Scholar
  23. Gao Y, Guo X, Li C, Ding H, Tang L, Ji H (2015) Characteristics of PM2.5 in Miyun, the northeastern suburb of Beijing: chemical composition and evaluation of health risk. Environ Sci Pollut Res Int 19:19Google Scholar
  24. Gen W, Tani M, Takeshita J, Ebihara Y, Tamaki K (2001) Mechanisms of Ca2+ overload induced by extracellular H2O2 in quiescent isolated rat cardiomyocytes. Basic Res Cardiol 96:623–629CrossRefGoogle Scholar
  25. Gius D, Botero A, Shah S, Curry HA (1999) Intracellular oxidation/reduction status in the regulation of transcription factors NF-kappaB and AP-1. Toxicol Lett 106:93–106CrossRefGoogle Scholar
  26. Gründel A, Friedrich K, Pfeiffer M, Jacobs E, Dumke R (2015) Subunits of the pyruvate dehydrogenase cluster of Mycoplasma pneumoniae are surface-displayed proteins that bind and activate human plasminogen. PLoS One 10:e0126600CrossRefGoogle Scholar
  27. Gururajan M, Jacob J, Pulendran B (2007) Toll-like receptor expression and responsiveness of distinct murine splenic and mucosal B-cell subsets. PLoS One 2:e863CrossRefGoogle Scholar
  28. Hansel TT, Barnes PJ (2009) New drugs for exacerbations of chronic obstructive pulmonary disease. Lancet 374:744–755CrossRefGoogle Scholar
  29. He XY, Wang XB, Zhang R, Yuan ZJ, Tan JJ, Peng B, Huang Y, Liu EM, Fu Z, Bao LM, Zou L (2013) Investigation of Mycoplasma pneumoniae infection in pediatric population from 12,025 cases with respiratory infection. Diagn Microbiol Infect Dis 75:22–27CrossRefGoogle Scholar
  30. Hemdan NY, Abu El-Saad AM, Sack U (2013) The role of T helper (TH)17 cells as a double-edged sword in the interplay of infection and autoimmunity with a focus on xenobiotic-induced immunomodulation. Clin Dev Immunol 2013:374769CrossRefGoogle Scholar
  31. Huang SK, Zhang Q, Qiu Z, Chung KF (2015) Mechanistic impact of outdoor air pollution on asthma and allergic diseases. J Thorac Dis 7:23–33Google Scholar
  32. Jin B, Sun T, Yu XH, Yang YX, Yeo AE (2012) The effects of TLR activation on T-cell development and differentiation. Clin Dev Immunol 2012:836485CrossRefGoogle Scholar
  33. Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283:65–87CrossRefGoogle Scholar
  34. Kawasaki T, Kawai T (2014) Toll-like receptor signaling pathways. Front Immunol 5:461CrossRefGoogle Scholar
  35. Kenneth NS, Hucks GE Jr, Kocab AJ, McCollom AL, Duckett CS (2014) Copper is a potent inhibitor of both the canonical and non-canonical NF-kappaB pathways. Cell Cycle 13:1006–1014CrossRefGoogle Scholar
  36. Kim HM, Shin JH, Cho YB, Roe JH (2014) Inverse regulation of Fe- and Ni-containing SOD genes by a Fur family regulator Nur through small RNA processed from 3’UTR of the sodF mRNA. Nucleic Acids Res 42:2003–2014CrossRefGoogle Scholar
  37. Kloog I, Zanobetti A, Nordio F, Coull BA, Baccarelli AA, Schwartz J (2015) Effects of airborne fine particles (PM2.5) on deep vein thrombosis admissions in the northeastern United States. J Thromb Haemost 13:768–774CrossRefGoogle Scholar
  38. Kudrin AV (2000) Trace elements in regulation of NF-kappaB activity. J Trace Elem Med Biol 14:129–142CrossRefGoogle Scholar
  39. Lanzinger S, Schneider A, Breitner S, Stafoggia M, Erzen I, Dostal M, Pastorkova A, Bastian S, Cyrys J, Zscheppang A, Kolodnitska T, Peters A, UFIREG study group (2015) Associations between ultrafine and fine particles and mortality in five central European cities—results from the UFIREG study. Environ Int 88:44–52CrossRefGoogle Scholar
  40. Layani-Milon MP, Gras I, Valette M, Luciani J, Stagnara J, Aymard M, Lina B (1999) Incidence of upper respiratory tract Mycoplasma pneumoniae infections among outpatients in Rhone-Alpes, France, during five successive winter periods. J Clin Microbiol 37:1721–1726Google Scholar
  41. Liang Y, Fang L, Pan H, Zhang K, Kan H, Brook JR, Sun Q (2014) PM2.5 in Beijing-temporal pattern and its association with influenza. Environ Health 13:102CrossRefGoogle Scholar
  42. Liu C, Fuertes E, Flexeder C, Hofbauer LC, Berdel D, Hoffmann B, Kratzsch J, von Berg A, Heinrich J, GINIplus Study Group, LISAplus Study Group (2015) Associations between ambient air pollution and bone turnover markers in 10-year old children: results from the GINIplus and LISAplus studies. Int J Hyg Environ Health 218:58–65CrossRefGoogle Scholar
  43. Miyashita N, Kawai Y, Akaike H, Ouchi K, Hayashi T, Kurihara T, Okimoto N, Atypical Pathogen Study Group (2012) Macrolide-resistant Mycoplasma pneumoniae in adolescents with community-acquired pneumonia. BMC Infect Dis 12:126CrossRefGoogle Scholar
  44. Moreno JA, Sullivan KA, Carbone DL, Hanneman WH, Tjalkens RB (2008) Manganese potentiates nuclear factor-kappaB-dependent expression of nitric oxide synthase 2 in astrocytes by activating soluble guanylate cyclase and extracellular responsive kinase signaling pathways. J Neurosci Res 86:2028–2038CrossRefGoogle Scholar
  45. Nguyen NT, Nakahama T, Le DH, Van Son L, Chu HH, Kishimoto T (2014) Aryl hydrocarbon receptor and kynurenine: recent advances in autoimmune disease research. Front Immunol 5:551CrossRefGoogle Scholar
  46. Ostro B, Roth L, Malig B, Marty M (2009) The effects of fine particle components on respiratory hospital admissions in children. Environ Health Perspect 117:475–480CrossRefGoogle Scholar
  47. Pajarinen J, Jamsen E, Konttinen YT, Goodman SB (2014) Innate immune reactions in septic and aseptic osteolysis around hip implants. J Long-Term Eff Med Implants 24:283–296CrossRefGoogle Scholar
  48. Pelaia G, Vatrella A, Busceti MT, Gallelli L, Calabrese C, Terracciano R, Maselli R (2015) Cellular mechanisms underlying eosinophilic and neutrophilic airway inflammation in asthma. Mediat Inflamm 2015:879783CrossRefGoogle Scholar
  49. Pereyre S, Touati A, Petitjean-Lecherbonnier J, Charron A, Vabret A, Bébéar C (2013) The increased incidence of Mycoplasma pneumoniae in France in 2011 was polyclonal, mainly involving M. pneumoniae type 1 strains. Clin Microbiol Infect 19:E212–E217CrossRefGoogle Scholar
  50. Price DJ, Joshi JG (1983) Ferritin. Binding of beryllium and other divalent metal ions. J Biol Chem 258:10873–10880Google Scholar
  51. Quintana FJ, Sherr DH (2013) Aryl hydrocarbon receptor control of adaptive immunity. Pharmacol Rev 65:1148–1161CrossRefGoogle Scholar
  52. Riojas-Rodríguez H, Solís-Vivanco R, Schilmann A, Montes S, Rodríguez S, Ríos C, Rodríguez-Agudelo Y (2010) Intellectual function in Mexican children living in a mining area and environmentally exposed to manganese. Environ Health Perspect 118:1465–1470CrossRefGoogle Scholar
  53. Saraya T, Kurai D, Nakagaki K, Sasaki Y, Niwa S, Tsukagoshi H, Nunokawa H, Ohkuma K, Tsujimoto N, Hirao S, Wada H, Ishii H, Nakata K, Kimura H, Kozawa K, Takizawa H, Goto H (2014) Novel aspects on the pathogenesis of Mycoplasma pneumoniae pneumonia and therapeutic implications. Front Microbiol 5:410Google Scholar
  54. Sarnat SE, Winquist A, Schauer JJ, Turner JR, Sarnat JA (2015) Fine particulate matter components and emergency department visits for cardiovascular and respiratory diseases in the St. Louis, Missouri-Illinois, Metropolitan Area. Environ Health Perspect 123:437–444Google Scholar
  55. Schmidt M, Raghavan B, Müller V, Vogl T, Fejer G, Tchaptchet S, Keck S, Kalis C, Nielsen PJ, Galanos C, Roth J, Skerra A, Martin SF, Freudenberg MA, Goebeler M (2010) Crucial role for human Toll-like receptor 4 in the development of contact allergy to nickel. Nat Immunol 11:814–819CrossRefGoogle Scholar
  56. Shafer TJ (1998) Effects of Cd2+, Pb2+ and CH3Hg+ on high voltage-activated calcium currents in pheochromocytoma (PC12) cells: potency, reversibility, interactions with extracellular Ca2+ and mechanisms of block. Toxicol Lett 99:207–221CrossRefGoogle Scholar
  57. Shimizu T, Kimura Y, Kida Y, Kuwano K, Tachibana M, Hashino M, Watarai M (2014) Cytadherence of Mycoplasma pneumoniae induces inflammatory responses through autophagy and toll-like receptor 4. Infect Immun 82:3076–3086CrossRefGoogle Scholar
  58. Shionome T, Endo S, Omagari D, Asano M, Toyoma H, Ishigami T, Komiyama K (2013) Nickel ion inhibits nuclear factor-kappa B activity in human oral squamous cell carcinoma. PLoS One 8:e68257CrossRefGoogle Scholar
  59. Somarajan SR, Al-Asadi F, Ramasamy K, Pandranki L, Baseman JB, Kannan TR (2014) Annexin A2 mediates Mycoplasma pneumoniae community-acquired respiratory distress syndrome toxin binding to eukaryotic cells. MBio 5:e01497–14CrossRefGoogle Scholar
  60. Song Y, Shryock JC, Wagner S, Maier LS, Belardinelli L (2006) Blocking late sodium current reduces hydrogen peroxideinduced arrhythmogenic activity and contractile dysfunction. J Pharmacol Exp Ther 318:214–222CrossRefGoogle Scholar
  61. Spuesens EB, Meijer A, Bierschenk D, Hoogenboezem T, Donker GA, Hartwig NG, Koopmans MP, Vink C, van Rossum AM (2012) Macrolide resistance determination and molecular typing of Mycoplasma pneumoniae in respiratory specimens collected between 1997 and 2008 in the Netherlands. J Clin Microbiol 50:1999–2004CrossRefGoogle Scholar
  62. Stafford SL, Bokil NJ, Achard ME, Kapetanovic R, Schembri MA, McEwan AG, Sweet MJ (2013) Metal ions in macrophage antimicrobial pathways: emerging roles for zinc and copper. Biosci Rep 33:e00049CrossRefGoogle Scholar
  63. Temsah RM, Netticadan T, Chapman D, Takeda S, Mochizuki S, Dhalla NS (1999) Alterations in sarcoplasmic reticulum function and gene expression in ischemicreperfused rat heart. Am J Physiol 277:H584–H594Google Scholar
  64. Traversi D, Cervella P, Gilli G (2015) Evaluating the genotoxicity of urban PM2.5 using PCR-based methods in human lung cells and the Salmonella TA98 reverse test. Environ Sci Pollut Res Int 22:1279–1289CrossRefGoogle Scholar
  65. Uldum SA, Bangsborg JM, Gahrn-Hansen B, Ljung R, Mølvadgaard M, Føns Petersen R, Wiid Svarrer C (2012) Epidemic of Mycoplasma pneumoniae infection in Denmark, 2010 and 2011. Euro Surveill 17:20073Google Scholar
  66. Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208CrossRefGoogle Scholar
  67. Viste K, Kopperud RK, Christensen AE, Døskeland SO (2005) Substrate enhances the sensitivity of type I protein kinase A to cAMP. J Biol Chem 280:13279–13284CrossRefGoogle Scholar
  68. Wages PA, Silbajoris R, Speen A, Brighton L, Henriquez A, Tong H, Bromberg PA, Simmons SO, Samet JM (2014) Role of H2O2 in the oxidative effects of zinc exposure in human airway epithelial cells. Redox Biol 3:47–55CrossRefGoogle Scholar
  69. Wagner S, Ruff HM, Weber SL, Bellmann S, Sowa T, Schulte T, Anderson ME, Grandi E, Bers DM, Backs J, Belardinelli L, Maier LS (2011) Reactive oxygen species-activated Ca/calmodulin kinase IIδ is required for late INa augmentation leading to cellular Na and Ca overload. Circ Res 108:555–565CrossRefGoogle Scholar
  70. Wagner S, Rokita AG, Anderson ME, Maier LS (2013) Redox regulation of sodium and calcium handling. Antioxid Redox Signal 18:1063–1077CrossRefGoogle Scholar
  71. Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192:95–117CrossRefGoogle Scholar
  72. WHO (2006) WHO Europe Air quality guidelines for particulate matter, ozone, nitrogen dioxide and sulfur dioxide. Global Update 2005. World Health Organization. Available at: http://www.euro.who.int/document/e90038.pdf
  73. WHO (2013) Review of evidence on health aspects of air pollution–REVIHAAP project technical report. WHO regional office for Europe, Copenhagen. http://www.euro.who.int/_data/assets/pdf_file/0004/193108/REVIHAAP-Final-technical-report-final-version.pdf?ua=1
  74. Wu Q, Martin RJ, Lafasto S, Efaw BJ, Rino JG, Harbeck RJ, Chu HW (2008) Toll-like receptor 2 down-regulation in established mouse allergic lungs contributes to decreased mycoplasma clearance. Am J Respir Crit Care Med 177:720–729CrossRefGoogle Scholar
  75. Wu PS, Chang LY, Lin HC, Chi H, Hsieh YC, Huang YC, Liu CC, Huang YC, Huang LM (2013) Epidemiology and clinical manifestations of children with macrolide-resistant Mycoplasma pneumoniae pneumonia in Taiwan. Pediatr Pulmonol 48:904–911CrossRefGoogle Scholar
  76. Yamada M, Buller R, Bledsoe S, Storch GA (2012) Rising rates of macrolide-resistant Mycoplasma pneumoniae in the central United States. Pediatr Infect Dis J 31:409–410CrossRefGoogle Scholar
  77. Yoo SJ, Kim HB, Choi SH, Lee SO, Kim SH, Hong SB, Sung H, Kim MN (2012) Differences in the frequency of 23S rRNA gene mutations in Mycoplasma pneumoniae between children and adults with community-acquired pneumonia: clinical impact of mutations conferring macrolide resistance. Antimicrob Agents Chemother 56:6393–6396CrossRefGoogle Scholar
  78. Yu W, Liu C, Zhang C, Jiang X (2013) Monitoring air quality in China is becoming big business [N]. China daily 2013-02-08. Available at:http://europe.chinadaily.com.cn/business/2013-02/08/content_16215030.htm
  79. Zelnikar M, Benčina, Jerala R, Manček-Keber M (2014) Vanadate from air pollutant inhibits hrs-dependent endosome fusion and augments responsiveness to toll-like receptors. PLoS One 9:e99287CrossRefGoogle Scholar
  80. Zeng X, Xu X, Zheng X, Reponen T, Chen A, Huo X (2016) Heavy metals in PM2.5 and in blood, and children’s respiratory symptoms and asthma from an e-waste recycling area. Environ Pollut 210:346–353CrossRefGoogle Scholar
  81. Zhang Q, Zhou T, Xu X, Guo Y, Zhao Z, Zhu M, Li W, Yi D, Huo X (2011) Downregulation of placental S100P is associated with cadmium exposure in Guiyu, an e-waste recycling town in China. Sci Total Environ 410–411:53–58CrossRefGoogle Scholar
  82. Zhao C, Liao J, Chu W, Wang S, Yang T, Tao Y, Wang G (2012) Involvement of TLR2 and TLR4 and Th1/Th2 shift in inflammatory responses induced by fine ambient particulate matter in mice. Inhal Toxicol 24:918–927CrossRefGoogle Scholar
  83. Zhao F, Liu G, Wu J, Cao B, Tao X, He L, Meng F, Zhu L, Lv M, Yin Y, Zhang J (2013) Surveillance of macrolide-resistant Mycoplasma pneumoniae in Beijing, China, from 2008 to 2012. Antimicrob Agents Chemother 57:1521–1523CrossRefGoogle Scholar
  84. Zheng G, Xu X, Li B, Wu K, Yekeen TA, Huo X (2013) Association between lung function in school children and exposure to three transition metals from an e-waste recycling area. J Expo Sci Environ Epidemiol 23:67–72CrossRefGoogle Scholar
  85. Zheng X, Xu X, Yekeen TA, Zhang Y, Chen A, Kim SS, Dietrich KN, Ho SM, Lee SA, Reponen T, Huo X (2016) Ambient air heavy metals in PM2.5 and potential human health risk assessment in an informal electronic-waste recycling site of China. Aerosol Air Qual Res 16:388–397CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Wei Hou
    • 1
    • 2
  • Xijin Xu
    • 1
    • 3
  • Yongge Lei
    • 2
  • Junjun Cao
    • 1
    • 4
  • Yu Zhang
    • 1
  • Liang Chen
    • 2
  • Xia Huo
    • 5
  1. 1.Laboratory of Environmental Medicine and Developmental Toxicology, and Guangdong Provincial Key Laboratory of Infectious Diseases and Molecular ImmunopathologyShantou University Medical CollegeShantouChina
  2. 2.People’s Hospital of New District Longhua ShenzhenShenzhenChina
  3. 3.Department of Cell Biology and GeneticsShantou University Medical CollegeShantouChina
  4. 4.Department of Pathology and Medical BiologyUniversity of Groningen, University Medical Center GroningenGroningenThe Netherlands
  5. 5.School of Environment, Guangzhou Key Laboratory of Environmental Exposure and Health, Guangdong Key Laboratory of Environmental Pollution and HealthJinan UniversityGuangzhouChina

Personalised recommendations