Elsevier

Environment International

Volume 60, October 2013, Pages 145-162
Environment International

Review
The health significance of gas- and particle-phase terpene oxidation products: A review

https://doi.org/10.1016/j.envint.2013.08.002Get rights and content

Abstract

The reactions between terpenes and ozone (or other oxidants) produce a wide variety of both gas- and particle-phase products. Terpenes are biogenic volatile organic compounds (VOCs) that are also contained in many consumer products. Ozone is present indoors since it infiltrates into the indoor environment and is emitted by some office and consumer equipment. Some of the gaseous products formed are irritating to biological tissues, while the condensed-phase products have received attention due to their contribution to ambient fine particulate matter (PM2.5) and its respective health significance. Despite common scientific questions, the indoor and ambient air research communities have tended to operate in isolation regarding this topic. This review critically evaluates the literature related to terpene oxidation products and attempts to synthesize results of indoor and ambient air studies to better understand the health significance of these materials and identify knowledge gaps. The review documents the results of a literature search covering terpene oxidation chemistry, epidemiological, toxicological, and controlled human exposure studies, as well as health studies focused more generically on secondary organic aerosol (SOA). The literature shows a clear role for gas-phase terpene oxidation products in adverse airway effects at high concentrations; however, whether these effects occur at more environmentally relevant levels is unclear. The evidence for toxicity of particle-phase products is less conclusive. Knowledge gaps and future research needs are outlined, and include the need for more consistency in study designs, incorporation of reaction product measurements into epidemiological studies conducted in both indoor and ambient settings, and more focused research on the toxicity of SOA, especially SOA of biogenic origin.

Introduction

In recent years, there has been increasing interest in the potential health impacts of secondary organic compounds formed via terpene oxidation reactions. Such compounds include both gas-phase materials such as formaldehyde as well as particle-phase components such as pinic acid (Grosjean et al., 1992, Jang and Kamens, 1999). Interestingly, research related to this issue is divided based on the medium of interest, with both indoor air and ambient air researchers involved, often without knowledge of or interaction with the other. For example, at a recent indoor air meeting (Indoor Air 2011), there were a total of six papers on terpenes and/or secondary organic aerosol; however, these were all presented by researchers primarily involved in the indoor air field and were focused on indoor air sources, formation, and health effects. Conversely, at the American Association of Aerosol Research's 2012 annual meeting, there were 14 presentations on secondary organic aerosol (SOA) specifically related to terpenes, but none took an indoor air perspective. It would be helpful if the two research communities could share information in a more systematic way, as each discipline has much to learn from the other.

Indoor air research on terpene oxidation products was prompted in large part by the investigation of health complaints in indoor environments, including eye, nose, and throat irritation, dry skin, headaches, and other nonspecific symptoms (Wolkoff et al., 1997). Despite extensive epidemiological research on potential causes of these complaints, the cause of these symptoms remains elusive. Some hypotheses that have been considered include low levels of multiple volatile organic compounds (VOCs), low relative humidity, thermal comfort effects, and elevated CO2 concentration indoors (Norback, 2009). More recently, the idea that reactions among indoor air pollutants can generate irritating compounds has been forwarded, and a number of studies have noted toxicological effects in animal models exposed to reaction products (e.g., Rohr et al., 2002, Sunil et al., 2007, Wolkoff et al., 1999, Wolkoff et al., 2012).

There is also much interest in terpene oxidation from an ambient atmospheric chemistry perspective, particularly with respect to secondary organic aerosol. Secondary aerosol forms from gas-to-particle conversion processes, including nucleation, condensation, and heterogeneous and multiphase chemical reactions (Hallquist et al., 2009). Much attention has been focused on understanding the mechanisms of formation of SOA, identifying the products formed, modeling SOA formation at local and regional scales, and evaluating the impact of these aerosols on climate. Less attention has been given to investigating potential health effects from SOA exposure, although interest appears to be increasing in this area as understanding the role played by various particulate matter (PM) components in adverse health effects becomes a higher priority research topic. Currently, PM is regulated in the United States with a mass-based National Ambient Air Quality Standard (NAAQS), despite accumulating evidence that different components of PM have different inherent toxicity (e.g., Kelly and Fussel, 2012, Rohr and Wyzga, 2012). Knowledge of the health effects of other major PM components such as sulfate, nitrate, and elemental carbon is reasonably well-developed; however, the effects attributable to the organic carbon component, comprised of both primary aerosol and SOA, is less well understood (Mauderly and Chow, 2008).

This review attempts to bring together the two distinct sets of literature related to indoor and ambient air and critically evaluate, based on existing evidence, the potential for human health impacts from exposure to terpene oxidation products. It should be noted that the focus is on monoterpenes (and isoprene, a hemiterpene); little is known about the health impacts of sesquiterpenes or their oxidation products and thus they are not included in the scope.

Section snippets

Methods

An extensive search was conducted for published information related to terpene oxidation product epidemiological, toxicological, and controlled human exposure studies on the PubMed database, using combinations of keywords “terpene”, “ozone”, “oxidation”, “pinene”, “limonene”, “isoprene”, “toxicology”, and “epidemiology”. In addition, to allow inclusion of up-to-date information on terpene oxidation product chemistry, formation, and related issues, the Science Direct database was searched using

Sources

Terpenes are unsaturated organic compounds of biogenic origin that contain one or more Cdouble bondC bonds. The monoterpenes (C10H16) and sesquiterpenes (C15H24) are volatile and are emitted from vegetation in large quantities. Monoterpenes such as α-pinene and d-limonene are commonly found in room fresheners and pine cleaners, wood products, and wood-based furniture coatings; these two terpenes are often detectable in the form of a pinene or lemon scent, respectively. They have also been measured in

Discussion

A broad spectrum of literature exists on the health impacts of terpene oxidation products; this literature spans the indoor air and ambient air areas, and includes epidemiological, toxicological, and controlled human exposure studies. In considering the literature as a whole, terpene/ozone reaction products can cause adverse effects in rodents at high concentrations. Most notably, sensory irritation and airflow limitation have been observed consistently in response to pinene, limonene, and

Knowledge gaps and future research

Despite substantial effort on the part of indoor and ambient air scientists, there are many unanswered questions with regard to the health effects of terpene oxidation products. The indoor community has appeared to be more united in an attempt to address the major scientific questions, and in fact a 2004 workshop entitled “Indoor Chemistry and Health” was aimed at promoting communications between experts in indoor chemistry and those examining health effects (Weschler et al., 2006). Workshop

Conclusion

Although terpene oxidation products have been studied for decades, the vast majority of research on this topic has focused on the chemistry and formation of these materials and not on their potential health effects. More recently, with the advancement of the “reactive chemistry” hypothesis to potentially explain complaints in indoor settings, efforts have been expended to test this hypothesis using a variety of animal and human exposure experimental designs. While results have varied and not

Acknowledgments

This work was funded by the Electric Power Research Institute. Dr. Rohr is employed by the Electric Power Research Institute, which is primarily supported by the electric industry in the U.S. and abroad. EPRI is an independent non-profit 501(c)(3) organization that funds external research at a number of universities and institutes worldwide.

References (137)

  • J. Nojgaard et al.

    The effect of human eye blink frequency of exposure to limonene oxidation products and methacrolein

    Toxicol Lett

    (2005)
  • J.K. Nøjgaard et al.

    The effect of nitrogen dioxide on particle formation during ozonolysis of two abundant monoterpenes indoors

    Atmos Environ

    (2006)
  • A.W. Norgaard et al.

    Secondary limonene endo-ozonide: a major product from gas-phase ozonolysis of R-(+)-limonene at ambient temperature

    Atmos Environ

    (2006)
  • E.D. Pellizzari et al.

    Comparison of indoor and outdoor residential levels of volatile organic chemicals in five U.S. geographical areas

    Environ Int

    (1986)
  • C.J. Proctor et al.

    A comparison of methods of assessing exposure to ETS in non-smoking British women

    Environ Int

    (1991)
  • A.C. Rohr et al.

    Attributing health effects to individual particulate matter constituents

    Atmos Environ

    (2012)
  • U. Schlink et al.

    Seasonal cycle of indoor-VOCs: comparison of apartments and cities

    Atmos Environ

    (2004)
  • American Society for Testing and Materials (ASTM)

    Standard test method for estimating sensory irritancy of airborne chemicals. Designation: E981–84

    (1984)
  • S.E. Anderson et al.

    Evaluation of dicarbonyls generated in a simulated indoor air environment using an in vitro exposure system

    Toxicol Sci

    (2010)
  • R. Atkinson et al.

    Gas-phase tropospheric chemistry of biogenic volatile organic compounds: a review

    Atmos Environ

    (2003)
  • R. Atkinson et al.

    Atmospheric degradation of volatile organic compounds

    Chem Rev

    (2003)
  • R. Atkinson et al.

    Rate constants for the gas-phase reactions of O3 with a series of monoterpenes and related compounds at 296 ± 2 K

    Int J Chem Kinet

    (1990)
  • R. Atkinson et al.

    Formation of OH radicals in the gas phase reactions of O3 with a series of monoterpenes and related compounds at 296 ± 2 K

    Int J Chem Kinet

    (1992)
  • T.C. Bond et al.

    A technology-based global inventory of black and organic carbon emissions from combustion

    J Geophys Res

    (2004)
  • B. Bonn et al.

    Influence of water vapor on the process of new particle formation during monoterpenes ozonolysis

    J Phys Chem A

    (2002)
  • H.S. Brightman et al.

    Evaluating building-related symptoms using the US EPA BASE study results

    Indoor Air

    (2008)
  • N. Britigan et al.

    Quantification of ozone levels in indoor environments generated by ionization and ozonolysis air-purifiers

    J Air Waste Manage Assoc

    (2006)
  • F. Broeckaert et al.

    Lung hyperpermeability, Clara-cell secretory potein (CC16), and susceptibility to ozone of five inbred strains of mice

    Inhal Toxicol

    (2003)
  • R. Buchdahl et al.

    Associations between ambient ozone, hydrocarbons, and childhood wheezy episodes: a prospective observational study in southeast London

    Occup Environ Med

    (2000)
  • J.C. Cabada et al.

    Estimating the secondary organic aerosol contribution to PM2.5 using the EC tracer method

    Aerosol Sci Technol

    (2004)
  • M.J. Campen et al.

    A comparison of vascular effects from complex and individual air pollutants indicates a role for monoxide gases and volatile hydrocarbons

    Environ Health Perspect

    (2010)
  • N. Carslaw et al.

    A significant role for nitrate and peroxide groups on indoor secondary organic aerosol

    Environ Sci Technol

    (2012)
  • X. Chen et al.

    Secondary organic aerosol from alpha-pinene ozonolysis in dynamic chamber system

    Indoor Air

    (2009)
  • X. Chen et al.

    A chamber study of secondary organic aerosol formation by limonene ozonolysis

    Indoor Air

    (2010)
  • X. Chen et al.

    Secondary organic aerosol from ozonolysis of biogenic volatile organic compounds: chamber studies of particle and reactive oxygen species formation

    Environ Sci Technol

    (2011)
  • P.A. Clausen et al.

    Chemical and biological evaluation of a reaction mixture of R-(+)-limonene/ozone: formation of strong airway irritants

    Environ Int

    (2001)
  • R.J. Delfino et al.

    Circulating biomarkers of inflammation, antioxidant activity, and platelet activation are associated with primary combustion aerosols in subjects with coronary artery disease

    Environ Health Perspect

    (2008)
  • R.J. Delfino et al.

    Air pollution exposures and circulating biomarkers of effect in a susceptible population: clues to potential causal component mixtures and mechanisms

    Environ Health Perspect

    (2009)
  • R.J. Delfino et al.

    Associations of primary and secondary organic aerosols with airway and systemic inflammation in an elderly panel cohort

    Epidemiology

    (2010)
  • R.J. Delfino et al.

    Electrocardiographic ST-segment depression and exposure to traffic-related aerosols in elderly subjects with coronary artery disease

    Environ Health Perspect

    (2011)
  • P. Depuydt et al.

    Ambient ozone concentrations induce airway hyperresponsiveness in some rat strains

    Eur Respir J

    (1999)
  • H. Destaillats et al.

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

  • E.A. Diaz et al.

    Toxicological Evaluation of Realistic Emission Source Aerosols (TERESA)—power plant studies: assessment of breathing pattern

    Inhal Toxicol

    (2011)
  • K.S. Docherty et al.

    Contributions of organic peroxides to secondary aerosol formed from reactions of monoterpenes with O3

    Environ Sci Technol

    (2005)
  • N. Donahue et al.

    Critical factors determining the variation in SOA yields from terpene ozonolysis: a combined experimental and computational study

    Faraday Discuss

    (2005)
  • M. Doyle et al.

    Effects of 1,3-butadiene, isoprene, and their photochemical degradation products on human lung cells

    Environ Health Perspect

    (2004)
  • U.S. Environmental Protection Agency

    FY2014 EPA budget in brief

  • Z. Fan et al.

    Ozone-initiated reactions with mixtures of volatile organic compounds under simulated indoor conditions

    Environ Sci Technol

    (2003)
  • J.D. Fenske et al.

    Human breath emissions of VOCs

    J Air Waste Manage Assoc

    (1999)
  • N. Fiedler et al.

    Health effects of a mixture of indoor air volatile organics, their ozone oxidation products, and stress

    Environ Health Perspect

    (2005)
  • Cited by (93)

    View all citing articles on Scopus
    View full text