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Home , Epipremnum aureum, Ozone depletion

as a result of increased input of the Effectiveness of in Reducing precursors of into the atmos- the Indoor Air Ozone phere (Mustafa, 1990). Automobiles are the principal contributors to sec- ondary tropospheric ozone genera- Heather L. Papinchak1, E. Jay Holcomb2,4, tion (Maroni et al., 1995). Teodora Orendovici Best3, and Dennis R. Decoteau2 Ozone as an indoor air pollutant can be prevalent in homes and offices due to infiltration of outdoor ambient ADDITIONAL INDEX WORDS. mitigation, depletion rates, foliage air indoors (Weschler, 2000). Ozone- emitting equipment such as copy UMMARY trifasciata S . Three common indoor houseplants, snake ( ), machines, laser printers, spider plant (Chlorophytum comosum), and golden ( aureum), were evaluated for their effectiveness in reducing ozone concentrations in a lighting, and some electrostatic air simulated indoor environment. Continuously stirred tank reactor (CSTR) chambers purification systems may also contrib- housed within a greenhouse equipped with a charcoal filtration air supply system ute to indoor ozone levels (Maroni were used to simulate an indoor environment in which ozone concentrations could et al., 1995; Weschler, 2000). Ozone be measured and regulated. Ozone was injected into the chambers and when generation from appliances such as concentrations reached 200 ± 5 ppb, the ozone-generating system was turned off photocopiers on average yield 5.2 and ozone concentrations over time (ozone was monitored every 5–6 min in each mgh–1 and laser printers on average chamber) were recorded until about <5 ppb were measured in the treatment produce 1.2 mgh–1; however, con- chamber. On average, ozone depletion time (time from when the ozone generating centrations could vary based on < system was turned off at 200 ppb to 5 ppb in the chamber) ranged from 38 to equipment maintenance (Black and 120 min per evaluation. Ozone depletion rates were higher within chambers that contained than within control chambers without plants, but there were no Worthan, 1999; Weschler, 2000). plant species differences. Depending on the air exchange rates between outdoor and indoor envi- ronments, indoor air has been ndoor air is ranked as appear to be equal for developing reported to contain from 10% to one of the world’s greatest public and developed countries. ’s 50% of outdoor values (Weschler, Ihealth risks (Wolverton, 1997). Commonwealth Council has 2006) to five to seven times the The United Nations Development suggested that 9 of 10 deaths due to contaminant concentrations of ambi- Program estimated in 1998 that over indoor air are experienced by the ent urban air (Brown et al., 1994; 2 million humans die each year due to developing world (Brennan and With- Orwell et al., 2004). the persistence of deleterious indoor gott, 2005). The principal groups at risk to air (Brennan and Withgott, 2005). It Ozone (O3), a photochemical ozone toxicity are organisms in which has also been estimated that globally oxidant with a potential of the primary route of exposure is via 14 times as many deaths occur from +2.07 V, is one of the most powerful inhalation (Wright and Welbourn, poor compared naturally occurring oxidants (Maroni 2002). Daily inhalation of indoor with ambient (Brennan et al., 1995; Mustafa, 1990). It is ozone for these organisms (such as and Withgott, 2005). considered a secondary ambient pol- humans) are estimated to be between Because humans in industrialized lutant and one of the components 25% and 60% of total ozone intake countries spend about of 80% to 90% of tropospheric , which can (Weschler, 2006). Major toxic effects of their time indoors (Orwell et al., adversely affect human health and of ozone in humans include altera- 2004; Wolverton, 1997), negative property (Mustafa, 1990). Ozone is tions in pulmonary function in addi- societal consequences due to polluted produced within the by tion to cellular and biochemical indoor air can be great (Fisk and Rose- chemical reactions involving free rad- endpoints (Wright and Welbourn, nfeld, 1997). For example, the cost of icals. It is formed during the reaction 2002). Exposure to ozone also may unhealthy indoor air in Australia has of carbon monoxide (CO) and vola- result in pulmonary edema, hemor- been estimated at $12 billion annually tile organic compounds (VOCs) in rhage, inflammation, and extensive due to losses in productivity, higher the presence of oxides lesions on the lung tissue, trachea, medical costs, more absenteeism, and (NOX), and . There and upper bronchi (Mehlman and lower earnings (, 2003). In is strong evidence to suggest that Borek, 1987). addition, the health burden associated average ozone concentrations have Indoor exposures to ozone are with indoor air pollution does not been rising during the past century often accompanied by exposure to the

We thank James Savage and Jonathan Ferdinand for providing technical assistance. 1Department of Economics, Environmental Units Management, The Pennsylvania State University, To convert U.S. to SI, To convert SI to U.S., University Park, PA 16802 multiply by U.S. unit SI unit multiply by 2 Department of Horticulture, The Pennsylvania State 0.0283 ft3 m3 35.3147 University, University Park, PA 16802 6.4516 inch2 cm2 0.1550 3School of Resources, The Pennsylvania State 28,350 Oz mg 3.5274 · 10–5 University, University Park, PA 16802 1 ppb nLL–1 1 4Corresponding author. E-mail: [email protected]. (F – 32) O 1.8 F C (1.8 ·C) + 32

286 • April–June 2009 19(2) products of ozone-initiated oxidative of ozone within a simulated indoor recorded at approximate 5- to 6-min reactions (such as isoprenes, styrenes, environment. intervals. This depletion rate was used terpenes, sesquiterpenes, and unsatu- as an indicator that the aerial portion rated fatty acids) (Weschler, 2004). Materials and methods of the plant was assisting in ozone The average daily intakes of ozone PLANT MATERIAL AND GROWING mitigation. Air circulation within the oxidative products are roughly one- CONDITIONS. Three plants species, chambers continued during all trials. third to twice the average daily intake snake plant, spider plant, and golden Five spider plants, five golden of ozone alone (Brown et al., 1994). pothos, were evaluated for their effec- pothos plants, and two snake plants Some of the oxidative products of tiveness in reducing ozone concen- (because of their larger size) per rep- ozone that are known or suspected trations in a simulated indoor lication were used in this evaluation. to adversely affect human health environment. These plant species During the evaluations, the top part include , acrolein, were chosen because of their popular- of each pot was enclosed with hydrogen peroxides, and fine and ity as indoor houseplants (primarily sheeting in such a manner that only ultrafine particles (Weschler, 2004). due to their low cost, low mainte- the aerial portion of the plants was Common indoor sources of reactive nance, and rich foliage) and their exposed to ozone. One chamber that chemicals to ozone include occupants previously reported ability to reduce did not contain any plants served as themselves, soft , linoleums, air other than ozone (Wol- control. certain paints, polishes, cleaning verton, 1986, 1997). At the completion of the evalua- products, soiled fabrics, and soiled Plants were grown in greenhouse tions, surface area and stomatal ventilation filters. Indirect evidence pots (one plant per pot) containing conductance (gS) of the plants were supports connections between human peatlite commercial growing mix measured. Leaf surface area (cm2) was morbidity/mortality and exposures (Sunshine #4; Sun Gro Horticulture, measured via an area meter (LI-3100; to indoor ozone and its oxidative Bellevue, WA) in a greenhouse at The LI-COR, Lincoln, NE) on all the products (Weschler, 2006). Pennsylvania State University campus plants within the individual chambers As indoor air pollution poses in University Park. Watering, fertil- and is reported as leaf area per cham- –2 –1 concerns for human health, cost- ization, and pest control were con- ber. GS [ (molm s )] was effective and easy-to-implement meth- ducted according to recommendations measured midleaf on representative ods are needed to eliminate or reduce and ensured good healthy plant growth midaged (while avoiding large concentrations. Activated charcoal fil- before and during the experiments. veins or any patterns of variegation) ters reduce air pollutants but installa- OZONE EXPOSURE AND MONIT- on individual plants via a portable tion and maintenance costs can be ORING. Four continuously stirred photosynthesis system (LI-6400; LI- high (Wolverton, 1997). As an alter- tank reactor (CSTR) chambers (2 COR) equipped with a leaf chamber 3 native, foliage plants could be used to m volume) covered with clear Tef- fluorometer and is reported as gS sequester some types of air pollution, lonÒ film and situated within a green- average per chamber. although their effectiveness appears house equipped with a charcoal STATISTICAL DESIGN AND ANALYSIS. to be plant species specific and air filtration air supply system (resulting The experiment was conducted as a pollutant dependent (Wolverton, in ambient levels of ozone within the completely randomized design with 1986). greenhouse of <5 ppb) were used to plant species as the main effect repli- Wolverton (1984) evaluated com- simulate an indoor environment in cated six times (trials) over the course mon foliage plants in controlled which ozone concentrations were of 3 d (27 June 2006, 28 June 2006, chambers (that simulated indoor measured and regulated. The CSTR and 3 July 2006) under similar envi- environments) for their ability to chambers previously described by ronmental conditions (Table 1). Three reduce concentrations of several air Heck et al. (1978) had an air flow of the trials were conducted during pollutants. Depletion rates of known circulation within the chambers of the late morning (AM) and three trials concentrations of air pollutants within 4.5 m3min–1. All of the CSTR were conducted during the early the enclosed chambers containing chambers were air tight when sealed afternoon (PM); day and time of day plants were measured. Wolverton and were maintained under green- (AM or PM) were noted for each trial. concluded that of the taxa selected, house conditions [e.g., photosynthetic The plant species evaluated were common spider plant and golden pot- photon flux (PPF), humidity, and alternated among specific chambers hos most effectively reduced various temperature]. Ozone was injected during the replications over time to air pollution concentrations (e.g., into the chambers via a controllable exclude any possible chamber effect. formaldehyde, nitrogen dioxide, and micrometering system and concentra- The same individual plants within carbon monoxide) from closed cham- tions were monitored with an ozone species were used for all trials. bers (Wolverton, 1984, 1986). Be- analyzer (TECO model 49; Thermo Data were analyzed using Mini- cause ozone was not one of the Electron Corp., Hopkinton, MA) and tab (release 14; Minitab, State College, indoor air pollutants evaluated in the data logger/computer recording sys- PA), Excel (Microsoft, Redmond, previous study (Wolverton, 1984) tem. Impeller fans ensured mixing of WA), and SAS (SAS Institute, Cary, and it is an important indoor air the gases within the chambers. Once NC). Significant results are reported pollutant for which mitigation meth- the ozone concentrations within the at the level of a = 0.05 (unless other- ods are limited, the objective of the chambers reached 200 ± 5 ppb, the wise noted). The slope was calculated current study was to determine the ozone-generating system was turned as the derivative of the depletion curve effectiveness of using common foliage off and the ozone depletion rate (time over time s=½otðÞ0 otðÞ1 =ðÞt 0 t 1 , houseplants in reducing concentrations to <5 ppb) for each chamber was where o(t) represents the value of

• April–June 2009 19(2) 287 RESEARCH REPORTS ozone at time t. Ozone depletion de- Table 1. Environmental conditions of temperature and relative humidity in the pends on the uptake of ozone by the continuously stirred tank reactor chambers during the six trials conducted in plant species, therefore it was not 2006 to test the effectiveness of houseplants in reducing ozone. PPF levels –2 –1 appropriate to use a simple decay ranged from 150 to 200 mmolm s . formula. The absolute value of slope Temp (F)y Relative humidity of the depletion curves (i.e., ozone Day Time of dayz (avg ± SD) (%) (avg ± SD) concentration per time interval), time 27 June AM 103.2 ± 6.6 59.2 ± 3.4 to 50% reduction of ozone, and time PM 101.1 ± 2.0 55.0 ± 2.6 to less than 5 ppb ozone within the 28 June AM 98.2 ± 3.6 53.6 ± 0.2 chamber (the point at which the trial PM 98.3 ± 3.3 49.8 ± 5.4 were ended) were used to account for 2 July AM 87.9 ± 2.4 75.6 ± 2.4 the ozone depletion rate for each PM 92.4 ± 4.3 67.3 ± 5.8 treatment. General Linear Model zAM = late morning, PM = early afternoon. (GLM) was used to determine the yC=(F – 32) O 1.8 significant factors affecting the deple- tion curves. Day, time of day (AM or PM), chamber, and treatments (e.g., Table 2. Analysis of variance comparing day, time of day (late morning versus early afternoon), and plant species (snake plant, spider plant, and golden pothos) species/control) as well as gS and total z plant leaf area were all considered in on absolute slope of the ozone depletion curves. the statistical model. Source df Mean square F P > F Day 2 16.231 1.73 0.180 Results Time of day 1 1.918 0.20 0.652 Analysis of variance of the six Plant species 3 46.223 4.92 0.003 trials determined that there was no Error 224 9.400 day or time of day (AM vs. PM) effect on zOzone concentrations among the plant species were sampled over time during the trials, and the absolute slope of the ozone depletion rates (as meas- the resulting ozone depletion curves was calculated as the derivative of the depletion curve over time s = ½otðÞotðÞ= t ðt Þð , where o(t) represent the value of ozone at time t. ured as absolute slopes of the curves) 0 1 0 1 among the treatments (Table 2). The negative slopes of the ozone curves from the experimental treatments indicated that ozone was mitigated from the chambers among the four treatments (Fig. 1). There was an effect of treatment on time to <5 ppb (the conclusion of the trial) and absolute slope of the ozone depletion curve (Table 3). Time to <5 ppb among treatments ranged from 38 to 120 min. Any of the plant species treatments evaluated required a shorter time to reach <5 ppb than the control treatment that contained no plants. The absolute slope of the control treatment was the smallest and was significantly dif- ferent from the golden pothos and snake plant treatments, but similar to the spider plant. There was no stat- istical difference among treatments in the amount of time for the ozone to reduce to 50% (data not presented). There were statistical differences Fig. 1. Sampled ozone concentrations over time among the plant (chamber) in gS (Table 4) among the plant treatments used to evaluate the effectiveness of houseplants in reducing ozone species evaluated. The spider plant concentrations. When ozone concentrations reached about 200 ppb, the ozone had the greatest conductance, while generator was turned off (time = 0) and ozone concentrations among the treatments the golden pothos had the least, and over the ensuing time were measured (snake = snake plant, pothos = golden pothos, 21 snake plant was intermediate. spider = spider plant, control = no plants, 1 ppb = 1nLL ).

Discussion mitigating ozone (compared with a interior environment. These results Plant species evaluated in this control that did not contain any are consistent to those reported by study (snake plant, spider plant, and plants) from the CSTR chambers that Wolverton (1984, 1986) using similar golden pothos) were effective in were used to simulate a controlled plant species for mitigation of VOCs.

288 • April–June 2009 19(2) Table 3. Influence of selected houseplants on ozone concentrations within implications for developing and chambers over time. Once the ozone concentration within the chambers reached developed countries. Because indoor 200 ± 5 ppb, the ozone-generating system was turned off and the ozone air pollution extensively affects devel- concentration for each chamber was recorded at approximate 6-min intervals. oping countries (Brennan and With- The control chamber did not contain any plants. gott, 2005; Smith, 2002), using Time to < 5 ppbz Absolute slope plants as a mitigation method could Plant ozone (min) of ozone curvey serve as a cost-effective tool in the Control 74.8 ax 2.64 b developing world where expensive Spider plant 50.3 b 3.95 ab pollution mitigation technology may Golden pothos 46.5 b 4.33 a not be economically feasible. Snake plant 46.3 b 4.49 a Significance ***w ** Literature cited z1 ppb = 1 nLL–1. ySlope was determined as the average of the instantaneous rate of change (derivative) for each sampling period. Black, M.S. and A.W. Worthan. 1999. xValues followed by the same letter within a column did not differ according to Tukey’s standardized range test at Emissions from office equipment, p. P < 0.05. 454–459. In: G. Raw, C. Aizlewood, w ,**, ***Statistical significance at P < 0.01 and P < 0.001, respectively, by analysis of variance (n = 5). and P. Warren (eds.). Indoor air 99. Vol. 2. Construction Research Communica- tions, London. Table 4. GS rates and leaf surface area of houseplants evaluated for their effectiveness in reducing ozone concentrations within chambers. Brennan, S. and J. Withgott. 2005. Envi- ronment: The science behind the stories. G Leaf surface area S Pearson, San Francisco. Plant [water (molm–2s–1)] (cm2 per chamber)z Spider plant 0.1184 ay 7,718.8 Brown, S.K., M.R. Sim, M.J. Abramson, and C.N. Gray. 1994. Concentrations of Snake plant 0.0998 ab 14,711.0 volatile organic compounds in indoor air: Golden pothos 0.0581 b 13,227.7 A review. Indoor Air 4:123–134. Significance **x na z1cm2 = 0.1550 inch2. Fisk, W.J. and A.H. Rosenfeld. 1997. yValues followed by the same letter within a column did not differ according to Tukey’s standardized range test Estimates of improved productivity and (P < 0.05). health from better indoor environments. x ,**Statistical significance at P < 0.01 by analysis of variance (n = 5), na = statistics not available as values are per Indoor Air 7:158–172. chamber and only one observation was recorded. Heck, W.W., R.B. Philbeck, and J.A. Although other studies have sug- indoor plant/substrate microcosm Dunning. 1978. A continuous stirred tank reactor (CSTR) system for exposing gested differential VOC depletion and to deplete contaminants plants to gaseous contaminants: Princi- rates for plant species (Wolverton, more effectively (Orwell et al., 2004; ples, specifications, construction, and 1984), in the current study, we were Wolverton and Wolverton, 1993). operation. U.S. Dept. Agr., Agr. Res. unable to identify any interspecies Our study did not consider soil or Serv. Publ. No. ARS-S-181. differences in depletion rates for ozone. microorganisms as factors in deter- A plant’s ability to reduce con- ozone mitigation; prospec- Maroni, M., B. Seifert, and T. Lindvall centrations of ozone in its surrounding tively, we plan on exposing soil and (eds.). 1995. Indoor air quality: A com- prehensive reference book. Elsevier Sci- environment appears to be dependent microorganisms to ozone to determine ence, New York. upon uptake of ozone through the their effect of indoor ozone depletion. stomata and subsequent detoxifica- In conclusion, common house- Mehlman, M.A. and C. Borek. 1987. tion reactions within the intracellular plants reduce ozone concentrations Toxicity and biochemical mechanisms of spaces. Therefore, the instantaneous in a simulated indoor setting. As a ozone. Environ. Res. 42:36–53. rate at which plant surfaces absorb method to reduce airborne contami- Mustafa, M.G. 1990. Biochemical basis of ozone would depend on the gS and nants, plant implementation may be ozone toxicity. Free Radic. Biol. Med. the total leaf surface area of the plant cost effective and readily applied 9:245–265. species. Because gS per plant and total throughout the world. In particular, Orwell, R.L., R.L. Wood, J. Tarran, F. leaf area of the plants within the the plant species evaluated in this Torpy, and M.D. Burchett. 2004. chambers varied among the treat- study were common, inexpensive, Removal of by the indoor ments, it was not possible to deter- and easy to grow and maintain. More plant/substrate microcosm and implica- mine if gS or total leaf area was the information is needed on species tions for air quality. Water Air Soil Pollut. more important plant variable in mit- effectiveness, the number of plants 157:193–207. igating ozone. Additional research required per unit area, and other Smith, K.R. 2002. Indoor air pollution in with plants of varying gS and leaf area environment interactions (including developing countries: Recommendations as well as alternative nonplant materi- light, temperature, and humidity) to for research. Indoor Air 12:198–207. als that increased the surface area are develop more effective recommenda- needed to further understand these tions. Regardless, our results provide Weschler, C.J. 2000. Ozone in indoor variables before more precise plant relevant evidence of a viable indoor environments: Concentration and chem- recommendations can be made. ozone mitigation technique using com- istry. Indoor Air 10:269–288. In previous research, emphasis mon indoor plants that could have Weschler, C.J. 2004. New directions: had been placed on the ability of the medical, environmental, and economic Ozone-initiated reaction products

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indoors may be more harmful than ozone Wolverton, B.C. 1986. Houseplants, Wood, R.A. 2003. Improving the indoor itself. Atmos. Environ. 38:5715–5718. indoor air pollutants, and allergic reac- environment for health, well-being and tions. Natl. Aeronautics Space Admin., productivity. In: Greening cities: A new Weschler, C.J. 2006. Ozone’s impact on Natl. Space Technol. Lab., Stennis Space . 30 Apr. 2003. Australian public health: Contributions from indoor Center, MS. Technology Park, Sydney, Australia. exposures to ozone and products of ozone-initiated chemistry. Environ. Wolverton, B.C. 1997. How to grow Wright, D.A. and P. Welbourn. 2002. Health Perspect. 114:1489–1496. fresh air. Penguin, New York. Environmental toxicology. Cambridge University Press, Cambridge, UK. Wolverton, B.C. 1984. The role of plants Wolverton, B.C. and J.D. Wolverton. and microorganisms in assuring a future 1993. Plants and soil micro-organisms: supply of clean air and water. Natl. Aero- Removal of formaldehyde, xylene nautics Space Admin., Natl. Space Tech- and ammonia from the indoor environ- nol. Lab., Stennis Space Center, MS. ment. J. Mississippi Acad. Sci. 38(2):11–15.

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