Elsevier

Toxicology Letters

Volume 199, Issue 3, 15 December 2010, Pages 288-300
Toxicology Letters

Pulmonary responses to printer toner particles in mice after intratracheal instillation

https://doi.org/10.1016/j.toxlet.2010.09.011Get rights and content

Abstract

The release of ultrafine particles from office equipment is currently receiving great concerns due to its potential threat to human health when inhaled. Printer toner is one of the largest consumables in daily office work, and the particles released from printers and photocopiers may pose damage to respiratory system. In this study, we found the particles can be released into the surrounding environment during the printing process and the concentrations of PM2.5 and PM10 particles increased obviously. To evaluate the time-course pulmonary responses caused by toner particles, the toner suspension was instilled into the lungs of the male mice through intratracheally instillation every other day for four times and the pulmonary responses of the lung were monitored at days 9, 28, 56 and 84. Indeed, mice treated with toner particles displayed a slower body weight growth rate during the recovery phase. The total cell number in bronchoalveolar lavage fluids (BALF) of toner-exposed groups was much higher than the saline-treated groups. The total protein, lactate dehydrogenase and acid phosphatase in BALF exhibited significant changes (p < 0.05 or p < 0.01) at different time points. The nitric oxide synthase, interleukin 1-beta, and interleukin 6 in the lung tissue of the toner-exposed groups also exhibited significant changes (p < 0.05 or p < 0.01). The pathological examination showed that toner particles can adhere to the alveolar septal walls, then enter into the alveoli and cause pulmonary lesion. During the experimental period, particles phagocytosed by alveolar macrophages (AMs) led to an increase of both AMs number and apoptosis. The pulmonary stress still remained over time even with a clearance period for 12 weeks. These results indicate that exposure to toner particles can inhibit the normal growth of the mice and induce significant inflammatory responses and lesion in the lung tissues. The health and safety effects from working indoors in offices with fumes and particles released from photocopiers and printers need to be paid more attention.

Introduction

With the rapid development of information technology (IT), the affiliated output equipment, which is mainly composed of laser printers, inkjet printers, multifunctional photocopiers and so on, has become the third largest IT market. Various types of printers are widely used in offices and homes around the world and have become standard indoor electronic equipment. They not only bring convenience to humans, but also have been suspected as a potential source of indoor air pollutants (Wolkoff et al., 1992, Wolkoff, 1999). Some case reports and a few studies have suggested that some common office environment exposures, such as exposure to carbonless copy (CCP) (Morgan and Camp, 1986, Shehade et al., 1987, LaMarte et al., 1988, Skov et al., 1989, Kanerva et al., 1993, Jaakkola and Jaakkola, 1999) and fumes from photocopies and printers (FPP) affect health adversely (Skov et al., 1989, Jaakkola and Jaakkola, 1999, Yassi and Warrington, 1988, Fisk et al., 2004, Stenerg et al., 1993). In fact, during the printing process, the printers not only produce FPP, but also emit a variety of particles (Brown, 1999, Kagi et al., 2007, Lee et al., 2001, Eggert et al., 1990, Wensing et al., 2006, Uhde et al., 2006), which partially come from toner. As we know, toner consists of very small particles of thermoplastic polymer, usually styrene–acrylate copolymer that are fixed on the paper by fusing. Black toner contains black carbon or iron oxide as pigments. In addition to these main constituents, toner contains various additives such as wax and silica, but also small amounts of specific metal salts to control the electromagnetic properties. Typically, about 75% of the toner is transferred to the photoconductive drum. However, toner particles that do not adhere to the drum become available for emission in the indoor air. This may lead to users being exposed to different concentrations of emitted particles. Kagi et al. (2007) confirmed that an increase in the concentration of ultrafine particle number in the printing process of the printers. Especially for the case of around 50 nm particles, particulate concentration increased greatly during printing. Lee and Hsu (2007) found that the emitted particles were much smaller than the original toner powders, which was similar to the above data (Kagi et al., 2007). He et al. (2007) investigated the particle emission characteristics of office printers and found the particle emission rates are printer-type specific and are affected by toner coverage and cartridge age.

The respiratory system is sensitive to bacteria, viruses, and many airborne particles that can be inhaled. Worldwide epidemiological studies show a consistent increase in cardiac and respiratory morbidity and mortality from exposure to particulate matter (PM) (Dockery et al., 1993, Samet et al., 2000, Brook et al., 2004). PM air pollutants have been shown to exacerbate a variety of pulmonary disorders, including chronic obstructive pulmonary disease (Schwartz, 1994, Sunyer and Basagaňa, 2001), asthma (Lipsett et al., 1997, Peters et al., 1997), and lower respiratory tract infections. We have learnt that the printers can emit a lot of ultrafine particles during the printing process. The unusual physicochemical properties of nanoparticles (such as larger surface area, surface reactivity and so on), which are differ substantially from their bulk materials of the same composition, allow them to interact with biological systems and the environment, with the potential to generate toxicity (Nel et al., 2006). People spend approximately 80% of their time in indoor environment where the levels of air pollutants can be several hundred times higher than outdoor (U.S. Environmental Protection Agency, 1987, U.S. Environmental Protection Agency, 1995). Toner, as one of the largest consumables in daily office work, its demand is increasing with the popularity of printers and photocopiers. It is estimated that the global demand for toner is around 240,000–260,000 tons. So its release and influence on the respiratory system cannot be ignored.

Therefore, the aim of this study was to evaluate the pulmonary responses of toner particles via an animal model by intratracheal instillation. We firstly monitored the concentrations of particles emitted from printing process using PM2.5 and PM10 particle samplers. Then the toner particles suspension in physiological saline solution was administered into the lungs of mice by non-surgical intratracheal instillation. The mice growth, lung inflammatory and fibrotic responses, expression of pro-inflammatory cytokines and pathological changes were analyzed to evaluate the time-course pulmonary responses caused by toner particles.

Section snippets

Toner particles

The toner was purchased from Beijing Laisheng High-tech Co., Ltd. The average size and composition of the toner particles were determined by transmission electron microscopy (TEM, Tecnai G220S-TWIN) and energy dispersive X-ray (EDX) analysis at an electron beam voltage of 200 kV. The particles were also analyzed by environmental scanning electron microscope (ESEM, Quanta 200 FEG) at low vacuum condition to observe the surface morphology. The metal impurity of the particles was determined by

Characteristics and morphology of toner particle

The general composition of toner is shown in Supplementary Table 1 (Graham and Zheng, 2005). Most toner particles contain polymer binder, ferric oxide, pigment, anti-tackifier, charge control agent and mobile agent. A lot of toners use ferric oxide or ferroferric oxide as pigment. The size of these two pigments is approximate to sub-micrometer. The single component magnetic toner contains a larger proportion of ferric oxide and the value is approximate to 30–40%. Ferroferric oxide is also used

Discussion

People are often exposed to particulates of various chemical compositions at their workplace and in daily life. Some of those particles, when inhaled, may be very harmful to the respiratory system (Fubini et al., 2006). Epidemiological data show that particulate matter (PM) present in ambient air pollution may underlie increased morbidity and mortality rates related to pulmonary and cardiovascular systems (Brook et al., 2004, Ito et al., 2008, Polichetti et al., 2009). As we know, silicosis

Conclusion

In conclusion, the quantity of toner particles released during the printing process is far from negligible. We have therefore investigated the potential pulmonary toxicity of inhaled toner particles to mice via intratracheal instillation. The results of biochemical analysis of BALF and lung homogenates indicated that the lung were overloaded by toner particles, which induced inflammatory response, damaged alveolar epithelial-capillary barrier and increased cell permeability. The increased

Conflict of interest statement

None declared.

Acknowledgements

We thank the financial support from the Ministry of Science and Technology of China (2011CB933401 and 2006AA03Z321), National Natural Science Foundation of China (10975040) and the CAS Knowledge Innovation Program (KJCX2-YW-M02). We thank Drs. Dong Han and Weiguo Chu for their useful discussion and Prof. Jiayi Xie for her kind help in the use of Environmental scanning electron microscope (ESEM).

References (89)

  • J.A. Li et al.

    Comparative study on the acute pulmonary toxicity induced by 3 and 20 nm TiO2 primary particles in mice

    Environ. Toxicol. Pharm.

    (2007)
  • H. Muhle et al.

    Pulmonary response to toner upon chronic inhalation exposure in rats

    Fundam. Appl. Toxicol.

    (1991)
  • J. Muller et al.

    Respiratory toxicity of multi-wall carbon nanotubes

    Toxicol. Appl. Pharm.

    (2005)
  • A.R. Murray et al.

    Oxidative stress and inflammatory response in dermal toxicity of single-walled carbon nanotubes

    Toxicology

    (2009)
  • G. Polichetti et al.

    Effects of particulate matter (PM10, PM2. 5 and PM1) on the cardiovascular system

    Toxicology

    (2009)
  • R. Pozzi et al.

    Inflammatory mediators induced by coarse (PM2.5-10) and fine (PM2.5) urban air particles in RAW 264.7 cells

    Toxicology

    (2003)
  • B. Rehn et al.

    Investigations on the inflammatory and genotoxic lung effects of two types of titanium dioxide: untreated and surface treated

    Toxicol. Appl. Pharm.

    (2003)
  • M.P. Sherman et al.

    Pyrrolidine dithiocarbamate inhibits induction of nitric-oxide synthase activity in rat alveolar macrophages

    Biochem. Biophys. Res. Commun.

    (1993)
  • J.X. Wang et al.

    Acute toxicity and biodistribution of different sized titanium dioxide particles in mice after oral administration

    Toxicol. Lett.

    (2007)
  • J.X. Wang et al.

    Potential neurological lesion after nasal instillation of TiO2 nanoparticles in the anatase and rutile crystal phases

    Toxicol. Lett.

    (2008)
  • J.X. Wang et al.

    Time-dependent translocation and potential impairment on central nervous system by intranasally instilled TiO2 nanoparticles

    Toxicology

    (2008)
  • D.B. Warheit et al.

    Pulmonary toxicity study in rats with three forms of ultrafine-TiO2 particles: differential responses related to surface properties

    Toxicology

    (2007)
  • P. Wolkoff

    Photocopiers and indoor air pollution

    Atmos. Environ.

    (1999)
  • M.T. Zhu et al.

    Comparative study of pulmonary responses to nano- and submicron-sized ferric oxide in rats

    Toxicology

    (2008)
  • B. Ankamwar et al.

    Biocompatibility of Fe3O4 nanoparticles evaluated by in vitro cytotoxicity assays using normal, glia and breast cancer

    Nanotechnology

    (2010)
  • E. Bermudez et al.

    Pulmonary responses of mice, rats, and hamsters to subchronic inhalation of ultrafine titanium dioxide particles

    Toxicol. Sci.

    (2003)
  • J.A. Blackford et al.

    Intratracheal instillation of silica up-regulates inducible nitric-oxide synthase gene-expression and increases nitric-oxide production in alveolar macrophages and neutrophils

    Am. J. Respir. Cell Mol. Biol.

    (1994)
  • R.D. Brook et al.

    Air pollution and cardiovascular disease: a statement for healthcare professionals from the expert panel on population and prevention science of the American Heart Association

    Circulation

    (2004)
  • S.K. Brown

    Pollutant emission properties of photocopiers and laser printers

  • Bruch, J., 1999. Toxikologische in vitro Bewertung von 6 Tonerstäuben im Vektorenmodell...
  • H. Brüggemann-Prieshoff et al.

    Beurteilung der Toxizität luftgetragener Stoffe am Arbeitsplatz mittels Leuchtbakterien. Teil 1: Verfahrensentwicklung

    Gefahrstoffe Reinhalt L

    (2002)
  • B. Corrin et al.

    Ultrastructural localization of acid phosphatase in rat lung

    J. Anat.

    (1969)
  • O. Creutzenberg et al.

    Lung clearance and retention of toner, TiO2, and crystalline silica, utilizing a tracer technique during chronic inhalation exposure in Syrian golden hamsters

    Inhal. Toxicol.

    (1998)
  • H. Destaillats et al.

    Indoor pollutants emitted by office equipment: a review of reported data and information needs

    Atmos. Environ.

    (2008)
  • D.W. Dockery et al.

    An association between air pollution and mortality in six U.S. cities

    N. Engl. J. Med.

    (1993)
  • T.A. Eggert et al.

    Emission of ozone and dust from laser printers. Presentation of a New Emission Source Test Method

  • W.J. Fisk et al.

    Phase 1 of the California healthy building study: a summary

    Indoor Air

    (2004)
  • B. Fubini et al.

    An overview on the toxicity of inhaled nanoparticles

  • B. Gaston et al.

    The biology of nitrogen-oxides in the airways

    Am J. Respir. Crit. Care Med.

    (1994)
  • Graham, J.G., Zheng, X.Z. (translator), 2005. The construction of toner. Office Equip. Technol. 2,...
  • L.K. Hanna et al.

    Size-dependent toxicity of metal oxide particles – a comparison between nano- and micrometer size

    Toxicol. Lett.

    (2009)
  • G.E. Hatch et al.

    Correlation of effects of inhaled versus intratracheally injected metals on susceptibility to respiratory infection in mice

    Am. Rev. Respir. Dis.

    (1981)
  • C. He et al.

    Particle emission characteristics of office printers

    Environ. Sci. Technol.

    (2007)
  • M.S. Jaakkola et al.

    Office equipment and supplies: a modern occupational health concern?

    Am. J. Epidemiol.

    (1999)
  • Cited by (65)

    • Capture and characterisation of microplastics printed on paper via laser printer's toners

      2021, Chemosphere
      Citation Excerpt :

      Unlike conventional inkjet printing, this technology relies on the utilisation of toner powders to print documents. While ingredients of the toner powder vary across brands, the typical cyan, magenta, yellow and key (CMYK) toners powders are formulated with polymers, resins, pigments or dyes, iron oxide, amorphous silica, charge control agents, paraffin wax, black carbon, surfactants and other inorganic/organic ingredients (Bai et al., 2010; Ruan et al., 2011; Ruan et al., 2018; Gu et al., 2020). There have been reports on the issues of airborne toner particles generated in the indoor environment during printing and maintenance processes (Prata, 2018; Carll et al., 2020; Gu et al., 2020).

    • Identification and visualisation of microplastics / nanoplastics by Raman imaging (iii): algorithm to cross-check multi-images

      2021, Water Research
      Citation Excerpt :

      Further research is needed to confirm this hypothesis. In general, using Raman imaging, we can catch and visualise the toner powders, the main ingredient of which is plastic (50-80%) (Bai et al. 2010, Gu et al. 2020, Ruan et al. 2011, Ruan et al. 2018). In other words, we can map the plastics, particularly via the selected peaks at 1170 cm−1 and 1480 cm−1, even the exact ingredients or plastics are unknown and the standard Raman spectrum is unavailable.

    View all citing articles on Scopus
    1

    These authors contributed equally to this work.

    View full text