Advertisement

Current Environmental Health Reports

, Volume 5, Issue 2, pp 244–254 | Cite as

A Meta-analysis of Arsenic Exposure and Lung Function: Is There Evidence of Restrictive or Obstructive Lung Disease?

  • Tiffany R. Sanchez
  • Martha Powers
  • Matthew Perzanowski
  • Christine M. George
  • Joseph H. Graziano
  • Ana Navas-Acien
Water and Health (T Wade, Section Editor)
  • 61 Downloads
Part of the following topical collections:
  1. Topical Collection on Water and Health

Abstract

Purpose of Review

Hundreds of millions of people worldwide are exposed to arsenic via contaminated water. The goal of this study was to identify whether arsenic-associated lung function deficits resemble obstructive- or restrictive-like lung disease, in order to help illuminate a mechanistic pathway and identify at-risk populations.

Recent Findings

We recently published a qualitative systematic review outlining the body of research on arsenic and non-malignant respiratory outcomes. Evidence from several populations, at different life stages, and at different levels of exposure showed consistent associations of arsenic exposure with chronic lung disease mortality, respiratory symptoms, and lower lung function levels. The published review, however, only conducted a broad qualitative description of the published studies without considering specific spirometry patterns, without conducting a meta-analysis, and without evaluating the dose-response relationship.

Summary

We searched PubMed and Embase for studies on environmental arsenic exposure and lung function. We performed a meta-analysis using inverse-variance-weighted random effects models to summarize adjusted effect estimates for arsenic and forced expiratory volume in one second (FEV1), forced vital capacity (FVC), and FEV1/FVC ratio. Across nine studies, median water arsenic levels ranged from 23 to 860 μg/L. The pooled estimated mean difference (MD) comparing the highest category of arsenic exposure (ranging from > 11 to > 800 μg/L) versus the lowest (ranging from < 10 to < 100 μg/L) for each study for FEV1 was – 42 mL (95% confidence interval (CI) − 70, − 16) and for FVC was – 50 mL (95% CI − 63, − 37). Three studies reported effect estimates for FEV1/FVC, for which there was no evidence of an association; the pooled estimated MD was 0.01 (95% CI − 0.005, 0.024). This review supports that arsenic is associated with restrictive impairments based on inverse associations between arsenic and FEV1 and FVC, but not with FEV1/FVC. Future studies should confirm whether low-level arsenic exposure is a restrictive lung disease risk factor in order to identify at-risk populations in the USA.

Keywords

Arsenic Epidemiology Meta-analysis Restrictive lung disease Spirometry Systematic review 

Abbreviations

ATS

American Thoracic Society

CFTR

Cystic fibrosis transmembrane conductance

ERS

European Respiratory Society

FEV1/FVC

Ratio of FEV1 to FVC

FEV1

Forced expiratory volume in one second

FVC

Forced vital capacity

PFT

Pulmonary function test

Notes

Funding Information

This work was supported by the National Institute of Environmental Health Sciences at the National Institutes of Health (grant numbers R01ES021367, 1R01ES025216, 5P30ES009089, and P42ES010349).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Supplementary material

40572_2018_192_MOESM1_ESM.docx (251 kb)
ESM 1 (DOCX 250 kb)

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    World Health Organization. Exposure to arsenic: a major public health concern. http://www.who.int/ipcs/features/arsenic.pdf. Published 2010. Accessed November 15, 2016.
  2. 2.
    National Research Council. Critical aspects of EPA’s IRIS assessment of inorganic arsenic: interim report. Washington, DC: The National Academies Press; 2014.Google Scholar
  3. 3.
    Straif K, Benbrahim-Tallaa L, Baan R, Grosse Y, Secretan B, el Ghissassi F, et al. A review of human carcinogens—part C: metals, arsenic, dusts, and fibres. Lancet Oncol. 2009;10(5):453–4.  https://doi.org/10.1016/S1470-2045(09)70134-2.CrossRefPubMedGoogle Scholar
  4. 4.
    Sanchez TR, Perzanowski M, Graziano JH. Inorganic arsenic and respiratory health, from early life exposure to sex-specific effects: a systematic review. Environ Res. 2016;147:537–55.  https://doi.org/10.1016/j.envres.2016.02.009.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Smith AH, Marshall G, Yuan Y, Liaw J, Ferreccio C, Steinmaus C. Evidence from Chile that arsenic in drinking water may increase mortality from pulmonary tuberculosis. Am J Epidemiol. 2011;173(4):414–20.  https://doi.org/10.1093/aje/kwq383.CrossRefPubMedGoogle Scholar
  6. 6.
    Smith AH, Marshall G, Yuan Y, Ferreccio C, Liaw J, von Ehrenstein O, et al. Increased mortality from lung cancer and bronchiectasis in young adults after exposure to arsenic in utero and in early childhood. Environ Health Perspect. 2006;114(8):1293–6.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Tsai SM, Wang TN, Ko YC. Mortality for certain diseases in areas with high levels of arsenic in drinking water. Arch Environ Health. 1999;54(3):186–93.  https://doi.org/10.1080/00039899909602258.CrossRefPubMedGoogle Scholar
  8. 8.
    Argos M, Parvez F, Rahman M, Rakibuz-Zaman M, Ahmed A, Hore SK, et al. Arsenic and lung disease mortality in Bangladeshi adults. Epidemiology. 2014;25(4):536–43.  https://doi.org/10.1097/EDE.0000000000000106.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Pesola GR, Parvez F, Chen Y, Ahmed A, Hasan R, Ahsan H. Arsenic exposure from drinking water and dyspnoea risk in Araihazar, Bangladesh: a population-based study. Eur Respir J. 2012;39(5):1076–83.  https://doi.org/10.1183/09031936.00042611.CrossRefPubMedGoogle Scholar
  10. 10.
    Rahman A, Vahter M, Ekstrom EC, Persson LA. Arsenic exposure in pregnancy increases the risk of lower respiratory tract infection and diarrhea during infancy in Bangladesh. Environ Health Perspect. 2011;119(5):719–24.  https://doi.org/10.1289/ehp.1002265.CrossRefPubMedGoogle Scholar
  11. 11.
    Parvez F, Chen Y, Yunus M, Olopade C, Segers S, Slavkovich V, et al. Arsenic exposure and impaired lung function. Findings from a large population-based prospective cohort study. Am J Respir Crit Care Med. 2013;188(7):813–9.  https://doi.org/10.1164/rccm.201212-2282OC.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Dauphine DC, Ferreccio C, Guntur S, et al. Lung function in adults following in utero and childhood exposure to arsenic in drinking water: preliminary findings. Int Arch Occup Environ Health. 2011;84(6):591–600.  https://doi.org/10.1007/s00420-010-0591-6.CrossRefPubMedGoogle Scholar
  13. 13.
    Recio-Vega R, Gonzalez-Cortes T, Olivas-Calderon E, Lantz RC, Gandolfi AJ, De Alba CG. In utero and early childhood exposure to arsenic decreases lung function in children. J Appl Toxicol. 2015;35(4):358–66.  https://doi.org/10.1002/jat.3023.CrossRefPubMedGoogle Scholar
  14. 14.
    Pellegrino R, Viegi G, Brusasco V, Crapo RO, Burgos F, Casaburi R, et al. Interpretative strategies for lung function tests. Eur Respir J. 2005;26(5):948–68.  https://doi.org/10.1183/09031936.05.00035205.CrossRefPubMedGoogle Scholar
  15. 15.
    Steele MP, Schwartz DA. Molecular mechanisms in progressive idiopathic pulmonary fibrosis. Annu Rev Med. 2012;64(1):120928131129008–276.  https://doi.org/10.1146/annurev-med-042711-142004.Google Scholar
  16. 16.
    Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology a proposal for reporting. JAMA. 2000;283(15):2008–12.  https://doi.org/10.1001/jama.283.15.2008.
  17. 17.
    Navas-Acien A, Francesconi KA, Silbergeld EK, Guallar E. Seafood intake and urine concentrations of total arsenic, dimethylarsinate and arsenobetaine in the US population. Environ Res. 2011;111(1):110–8.  https://doi.org/10.1016/j.envres.2010.10.009.CrossRefPubMedGoogle Scholar
  18. 18.
    Ho JC, Au WY, Han L, Kwong YL, Ip MS. Effect of therapeutic arsenic exposure on pulmonary function. Respir Med. 2013;107(9):1423–30.  https://doi.org/10.1016/j.rmed.2013.06.012.CrossRefPubMedGoogle Scholar
  19. 19.
    Navas-Acien A, Sharrett AR, Silbergeld EK, Schwartz BS, Nachman KE, Burke TA, et al. Arsenic exposure and cardiovascular disease: a systematic review of the epidemiologic evidence. Am J Epidemiol. 2005;162(11):1037–49.  https://doi.org/10.1093/aje/kwi330.CrossRefPubMedGoogle Scholar
  20. 20.
    Greenland S. Quantitative methods in the review of epidemiologic literature. Epidemiol Rev. 1987;9:1–30.CrossRefPubMedGoogle Scholar
  21. 21.
    Das D, Bindhani B, Mukherjee B, Saha H, Biswas P, Dutta K, et al. Chronic low-level arsenic exposure reduces lung function in male population without skin lesions. Int J Public Health. 2014;59(4):655–63.  https://doi.org/10.1007/s00038-014-0567-5.CrossRefPubMedGoogle Scholar
  22. 22.
    von Ehrenstein OS, Mazumder DNG, Yuan Y, Samanta S, Balmes J, Sil A, et al. Decrements in lung function related to arsenic in drinking water in West Bengal, India. Am J Epidemiol. 2005;162(6):533–41.  https://doi.org/10.1093/aje/kwi236.CrossRefGoogle Scholar
  23. 23.
    Steinmaus C, Ferreccio C, Acevedo J, Balmes JR, Liaw J, Troncoso P, et al. High risks of lung disease associated with early-life and moderate lifetime arsenic exposure in northern Chile. Toxicol Appl Pharmacol. 2016;313:10–5.  https://doi.org/10.1016/j.taap.2016.10.006.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Egger M, Davey-Smith G, Altman D (eds). Systematic reviews in health care: meta-analysis in context, 2nd edition. London: BMJ Publishing Group; 2001.  https://doi.org/10.1002/9780470693926.
  25. 25.
    Smith AH, Yunus M, Khan AF, Ercumen A, Yuan Y, Smith MH, et al. Chronic respiratory symptoms in children following in utero and early life exposure to arsenic in drinking water in Bangladesh. Int J Epidemiol. 2013;42(4):1077–86.  https://doi.org/10.1093/ije/dyt120.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Ahmed S, Akhtar E, Roy A, von Ehrenstein OS, Vahter M, Wagatsuma Y, et al. Arsenic exposure alters lung function and airway inflammation in children: a cohort study in rural Bangladesh. Environ Int. 2017;101:108–16.  https://doi.org/10.1016/j.envint.2017.01.014.CrossRefPubMedGoogle Scholar
  27. 27.
    Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ, 1997;315(7109):629–34.  https://doi.org/10.1136/bmj.315.7109.629.
  28. 28.
    Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.CrossRefPubMedGoogle Scholar
  29. 29.
    Crippa A, Orsini N. Dose-response meta-analysis of differences in means. BMC Med Res Methodol. 2016;16:91.  https://doi.org/10.1186/s12874-016-0189-0.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Harbord RM, Higgins JPT. Meta-regression in Stata. Stata J. 2008;8(4):493–519.Google Scholar
  31. 31.
    Nafees AA, Kazi A, Fatmi Z, Irfan M, Ali A, Kayama F. Lung function decrement with arsenic exposure to drinking groundwater along River Indus: a comparative cross-sectional study. Environ Geochem Health. 2011;33(2):203–16.  https://doi.org/10.1007/s10653-010-9333-7.CrossRefPubMedGoogle Scholar
  32. 32.
    Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J. 2005;26(2):319–38.  https://doi.org/10.1183/09031936.05.00034805.CrossRefPubMedGoogle Scholar
  33. 33.
    Feng W, Huang X, Zhang C, et al. The dose–response association of urinary metals with altered pulmonary function and risks of restrictive and obstructive lung diseases: a population-based study in China. BMJ Open. 2015;1(5):1–24.  https://doi.org/10.1017/CBO9781107415324.004.Google Scholar
  34. 34.
    De BK, Majumdar D, Sen S, Guru S, Kundu S. Pulmonary involvement in chronic arsenic poisoning from drinking contaminated ground-water. J Assoc Physicians India. 2004;52:395–400.PubMedGoogle Scholar
  35. 35.
    Selman M, Pardo A. Alveolar epithelial cell disintegrity and subsequent activation. Am J Respir Crit Care Med. 2012;186(2):119–21.  https://doi.org/10.1164/rccm.201206-0997ED.CrossRefPubMedGoogle Scholar
  36. 36.
    Olsen CE, Liguori AE, Zong Y, Lantz RC, Burgess JL, Boitano S. Arsenic upregulates MMP-9 and inhibits wound repair in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2008;295(2):L293–302.  https://doi.org/10.1152/ajplung.00134.2007.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Lantz RC, Chau B, Sarihan P, Witten ML, Pivniouk VI, Chen GJ. In utero and postnatal exposure to arsenic alters pulmonary structure and function. Toxicol Appl Pharmacol. 2009;235(1):105–13.  https://doi.org/10.1016/j.taap.2008.11.012.CrossRefPubMedGoogle Scholar
  38. 38.
    Choudhury S, Gupta P, Ghosh S, Mukherjee S, Chakraborty P, Chatterji U, et al. Arsenic-induced dose-dependent modulation of the NF-κB/IL-6 axis in thymocytes triggers differential immune responses. Toxicology. 2016;357-358:85–96.  https://doi.org/10.1016/j.tox.2016.06.005.CrossRefPubMedGoogle Scholar
  39. 39.
    Mazumder DN, Steinmaus C, Bhattacharya P, et al. Bronchiectasis in persons with skin lesions resulting from arsenic in drinking water. Epidemiology. 2005;16(6):760–5.CrossRefPubMedGoogle Scholar
  40. 40.
    •• Mazumdar M, Christiani DC, Biswas SK, Ibne-Hasan OS, Kapur K, Hug C. Elevated sweat chloride levels due to arsenic toxicity. N Engl J Med. 2015;372(6):582–3.  https://doi.org/10.1056/NEJMc1413312. This study shows evidence that arsenic is associated with elevated sweat chloride levels among persons exposed to arsenic in the absence of a genetic diagnosis of cystic fibrosis. CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Bomberger JM, Coutermarsh BA, Barnaby RL, Stanton BA. Arsenic promotes ubiquitinylation and lysosomal degradation of cystic fibrosis transmembrane conductance regulator (CFTR) chloride channels in human airway epithelial cells. J Biol Chem. 2012;287(21):17130–9.  https://doi.org/10.1074/jbc.M111.338855.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Han SG, Castranova V, Vallyathan V. Heat shock protein 70 as an indicator of early lung injury caused by exposure to arsenic. Mol Cell Biochem. 2005;277(1–2):153–64.  https://doi.org/10.1007/s11010-005-5874-y.CrossRefPubMedGoogle Scholar
  43. 43.
    Cohen DS, Palmer E, Welch WJ, Sheppard D. The response of guinea pig airway epithelial cells and alveolar macrophages to environmental stress. Am J Respir Cell Mol Biol. 1991;5(2):133–43.CrossRefPubMedGoogle Scholar
  44. 44.
    Broeckaert F, Clippe A, Knoops B, Hermans C, Bernard A. Clara cell secretory protein (CC16): features as a peripheral lung biomarker. Ann N Y Acad Sci. 2000;923:68–77.  https://doi.org/10.1111/j.1749-6632.2000.tb05520.x.CrossRefPubMedGoogle Scholar
  45. 45.
    Parvez F, Chen Y, Brandt-Rauf PW, Bernard A, Dumont X, Slavkovich V, et al. Nonmalignant respiratory effects of chronic arsenic exposure from drinking water among never-smokers in Bangladesh. Environ Health Perspect. 2008;116(2):190–5.  https://doi.org/10.1289/ehp.9507.PubMedGoogle Scholar
  46. 46.
    Olivas-Calderon E, Recio-Vega R, Gandolfi AJ, et al. Lung inflammation biomarkers and lung function in children chronically exposed to arsenic. Toxicol Appl Pharmacol. 2015;287:161–7.  https://doi.org/10.1016/j.taap.2015.06.001.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Atkinson JJ, Senior RM. Matrix metalloproteinase-9 in lung remodeling. Am J Respir Cell Mol Biol. 2003;28(1):12–24.  https://doi.org/10.1165/rcmb.2002-0166TR.CrossRefPubMedGoogle Scholar
  48. 48.
    Lederer DJ, Enright PL, Kawut SM, Hoffman EA, Hunninghake G, van Beek EJR, et al. Cigarette smoking is associated with subclinical parenchymal lung disease: the Multi-Ethnic Study of Atherosclerosis (MESA)-lung study. Am J Respir Crit Care Med. 2009;180(5):407–14.  https://doi.org/10.1164/rccm.200812-1966OC.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Ferreccio C, Gonzalez C, Milosavjlevic V, Marshall G, Sancha AM, Smith AH. Lung cancer and arsenic concentrations in drinking water in Chile. Epidemiology. 2000;11(6):673–9.  https://doi.org/10.1097/00001648-200011000-00010.CrossRefPubMedGoogle Scholar
  50. 50.
    Hertz-Picciotto I, Smith AH, Holtzman D, Lipsett M, Alexeeff G. Synergism between occupational arsenic exposure and smoking in the induction of lung cancer. Epidemiology. 1992;3(1):23–31.CrossRefPubMedGoogle Scholar
  51. 51.
    IHME. Epi visualization. http://ghdx.healthdata.org/gbd-results-tool?params=querytool-permalink/fc7c45515025010a96c2a7dd49ed751f. Published 2016. Accessed October 27, 2016.
  52. 52.
    Carlin DJ, Naujokas MF, Bradham KD, Cowden J, Heacock M, Henry HF, et al. Arsenic and environmental health: state of the science and future research opportunities. Environ Health Perspect. 2015;124:890–9.  https://doi.org/10.1289/ehp.1510209.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Farzan SF, Korrick S, Li Z, Enelow R, Gandolfi AJ, Madan J, et al. In utero arsenic exposure and infant infection in a United States cohort: a prospective study. Environ Res. 2013;126:24–30.  https://doi.org/10.1016/j.envres.2013.05.001.CrossRefPubMedGoogle Scholar
  54. 54.
    Araujo BB, Dolhnikoff M, Silva LFF, Elliot J, Lindeman JHN, Ferreira DS, et al. Extracellular matrix components and regulators in the airway smooth muscle in asthma. Eur Respir J. 2008;32(1):61–9.  https://doi.org/10.1183/09031936.00147807.CrossRefPubMedGoogle Scholar
  55. 55.
    • Sherwood CL, Lantz RC. Lung cancer and other pulmonary disease. In: States JC, ed. Arsenic: exposure sources, health risks, and mechanisms of toxicity. John Wiley & Sons, Inc.; 2015:137–162.  https://doi.org/10.1002/9781118876992.ch7. This chapter reviews possible mechanisms for arsenic-associated lung disease, both malignant and non-malignant.
  56. 56.
    Ramsey KA, Larcombe AN, Sly PD, Zosky GR. In utero exposure to low dose arsenic via drinking water impairs early life lung mechanics in mice. BMC Pharmacol Toxicol. 2013;14:13.  https://doi.org/10.1186/2050-6511-14-13.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Tiffany R. Sanchez
    • 1
  • Martha Powers
    • 2
  • Matthew Perzanowski
    • 1
  • Christine M. George
    • 3
  • Joseph H. Graziano
    • 1
  • Ana Navas-Acien
    • 1
  1. 1.Department of Environmental Health SciencesColumbia UniversityNew YorkUSA
  2. 2.Department of Environmental Health and EngineeringJohns Hopkins University Bloomberg School of Public HealthBaltimoreUSA
  3. 3.Department of International HealthJohns Hopkins University Bloomberg School of Public HealthBaltimoreUSA

Personalised recommendations