Potted plants do not improve indoor air quality

Journal of Exposure Science & Environmental Epidemiology (2020) 30:253 – 261 https://doi.org/10.1038/s41370-019-0175-9 ARTICLE Potted plants do not improve indoor air quality: a review and analysis of reported VOC removal ef fi ciencies Bryan E. Cummings 1 ● Michael S. Waring 1 Received: 28 February 2019 / Revised: 18 June 2019 / Accepted: 12 July 2019 / Published online: 6 November 2019 © The Author(s), under exclusive licence to Springer Nature America, Inc. 2019 Abstract Potted plants have demonstrated abilities to remove airborne volatile organic compounds (VOC) in small, sealed chambers over timescales of many hours or days. Claims have subsequently been made suggesting that potted plants may reduce indoor VOC concentrations. These potted plant chamber studies reported outcomes using various metrics, often not directly applicable to contextualizing plants ’ impacts on indoor VOC loads. To assess potential impacts, 12 published studies of chamber experiments were reviewed, and 196 experimental results were translated into clean air delivery rates (CADR, m 3 /h), which is an air cleaner metric that can be normalized by volume to parameterize fi rst-order loss indoors. The distribution of single-plant CADR spanned orders of magnitude, with a median of 0.023 m 3 /h, necessitating the placement of 10 – 1000 plants/m 2 of a building ’ s fl oor space for the combined VOC-removing ability by potted plants to achieve the same removal rate that outdoor-to-indoor air exchange already provides in typical buildings (~1 h - 1 ). Future experiments should shift the focus from potted plants ’ (in)abilities to passively clean indoor air, and instead investigate VOC uptake mechanisms, alternative bio fi ltration technologies, biophilic productivity and well-being bene fi ts, or negative impacts of other plant-sourced emissions, which must be assessed by rigorous fi eld work accounting for important indoor processes. Keywords Empirical/statistical models ● Volatile organic compounds ● Exposure modeling Introduction Inhabitants of developed countries spend up to 90% of their lives indoors [ 1 ]. As such, the quality of indoor air is critical to human exposure to pollution. Indoor pollution is com- posed of myriad constituents, which include oxidants and irritants, volatile organic compounds (VOC), and particulate matter (PM) [ 2 – 10 ]. Much, though not all, of indoor pol- lution is sourced directly from the indoor environment itself. VOC concentrations particularly are driven by indoor emissions, traceable to building materials and furnishings [ 11 ], use of consumer products and air fresheners [ 12 ], and cooking [ 13 ], among others. VOCs may be a primary cause of many sick building syndrome (SBS) symptoms and other health problems associated with indoor air [ 14 – 18 ]. Oxi- dation of VOCs can also produce secondary organic aero- sols [ 19 – 25 ], which compound the PM burden and may pose harmful health risks themselves [ 26 – 28 ]. To reduce VOCs and other indoor-sourced pollutants from the indoor environment, buildings traditionally make use of in fi ltration and natural or mechanical ventilation air exchange [ 29 ], which is the replacement of stale indoor air with fresh air from the outdoors. Higher ventilation rates have been correlated with lower absenteeism and SBS symptom incidences, reductions in perceptions of odors, and increased task performance [ 30 – 35 ]. However, increased ventilation may augment the indoor concentration of outdoor-sourced pollutants, such as ozone and PM [ 9 , 10 , 36 – 38 ]. Increased ventilation also typically uses more energy [ 39 – 41 ], as outdoor air must be conditioned to be thermally comfortable. To address these drawbacks, alternative means of purifying indoor air to replace or supplement ventilation air are being investigated. * Michael S. Waring msw59@drexel.edu 1 Department of Civil, Architectural and Environmental Engineering, Drexel University, 3141 Chestnut, St. Philadelphia, PA 19104, USA Supplementary information The online version of this article ( https:// doi.org/10.1038/s41370-019-0175-9 ) contains supplementary material, which is available to authorized users. 1234567890();,: 1234567890();,:

Experiments have demonstrated the ability of potted plants to reduce airborne VOC concentrations within sealed chambers. Many studies which carried out these experi- ments subsequently draw conclusions that potted plants may improve indoor air quality, spurring a presence of nonacademic resources (predominantly online) touting the use of houseplants as a sustainable means of cleaning indoor air. However, the experimental results of the underlying scienti fi c works are often reported in ways such that they cannot simply be extrapolated into impacts in real indoor environments. Typical for these studies, a potted plant was placed in a sealed chamber (often with volume of ~1 m 3 ), into which a single VOC was injected, and its decay was tracked over the course of many hours or days [ 42 – 52 ]. In contrast, building volumes are much larger than that of an experimental chamber, and VOC emissions are persistent. Also, indoor air is continuously exchanged with the out- doors. For instance, the median of measured residence times for air in US of fi ces is about 50 min [ 53 ], and 80 min for US homes [ 19 , 54 , 55 ], corresponding to air exchange rates (AER) of 1.2 and 0.75 h - 1 , respectively, contrasting sharply with the long timescales needed for the chamber experi- ments to produce meaningful VOC reductions. Some endeavors to minimize these differences between chambers and indoor environments have been pursued in studies, though not all issues have been resolved. For instance, Xu et al. [ 56 ] attempted to mirror more realistic conditions in what they referred to as a “ dynamic ” chamber, but no mention of air exchange was explicitly found in their work. Liu et al. [ 57 ] incorporated con- tinuous air fl ow into their experiments, with constant upstream benzene concentrations of about 150 ppb. However, they maintained a very small chamber volume, in fl ating the relative in fl uence of the plants. Sorption of VOCs onto the surfaces of the chamber is sometimes, but not always considered by these studies, which may be the cause of some of the observed VOC decay, rather than uptake by the plants. Other studies have proposed improvements to the design of plant chamber experi- ments, but they focused on conditions such as tempera- ture, humidity, and carbon dioxide concentrations (all of which may impact plant health), instead of parameters which affect pollutant-building interactions [ 58 , 59 ]. A few fi eld campaigns have tried to measure the impact of plants within indoor environments, although Girman et al. [ 60 ] documented in detail the likely inaccuracies of the measuring equipment used in these studies. More importantly, none of them controlled or measured the outdoor air exchange rate. Conclusions can therefore not be drawn about the in fl uence of plants versus the in fl uence of VOC removal by air exchange. Of these studies, however, Dingle et al. [ 61 ] found no reduction in for- maldehyde until plant density reached 2.44 plants/m 2 , at which point only a 10% reduction was seen. Wood et al. [ 62 ] claimed to observe VOC reductions of up to 75% within plant-containing of fi ces at high VOC loadings, but they only sampled 5-min measurements once each week and neglected to report air exchange. Only two publications were found that not only acknowledge these issues, but explicitly refute the notion that common houseplants improve indoor air quality. They were written by Girman et al. [ 60 ] and Levin [ 63 ]. Those works, authored by indoor air and building scien- tists, discuss in detail the history and limitations of the chamber and fi eld studies, and provide a mass balance calculation that highlights the predicted ineffectiveness of using potted plants to remove VOCs from indoor air. Building upon that foundation, the work herein presents a review and impact analysis of removal rates reported by 12 cited works, most of which were conducted after the 1992 publication by Levin [ 63 ]. Among these works, the metrics used to report VOC removal are inconsistent, so comparisons and reproducibility are dif fi cult to assess, as is predicting indoor air impacts. The present analysis thus fi rst standardizes 196 experimental results into a metric useful for measuring indoor air cleaning, and then uses those standardized results to assess the effectiveness of using potted plants to remove VOCs and improve indoor air quality. Methodology Standardization of reported VOC removal Within the building sciences, the indoor air-cleaning potential of a standalone device is parameterized with the clean air delivery rate (CADR). The CADR is the effective volumetric fl ow rate at which “ clean ” air is supplied to the environment, re fl ecting the rate at which the air cleaner removes pollutants. It is the product of the fl ow rate of air through the air cleaner ( Q ac. , m 3 /h) and its removal ef fi ciency ( η ), so CADR = Q ac η (m 3 /h). The same air cleaner will have a greater impact in a smaller environment, so to gauge the impact of an air cleaner within the context of the indoor space it occupies, CADR must be normalized by the relevant indoor volume ( V , m 3 ). This CADR/ V (h - 1 ) parameter corresponds to a fi rst-order loss rate constant (i.e., rate of pollutant removal is propor- tional to pollutant concentration). Given that suf fi cient information is provided by a chamber study (e.g. physical chamber characteristics, experimental parameters), a CADR-per-plant (CADR p , m 3 h - 1 plant - 1 ) can be computed using its results. The experimental procedures of the 12 considered studies used one of two general experi- mental setups. The fi rst setup (setup I) assumes a perfectly sealed chamber with no VOC sources with uptake by the 254 B. E. Cummings, M. S. Waring

(2) A sealed chamber (setup I) presenting a timeseries of concentration measurements. (3) A fl ow-through chamber (setup II) presenting C inlet and C outlet measurements. For the fi rst category, Eq. 3 was used to compute CADR p values for the experiments. Aydogan and Montoya [ 42 ] tabulated the time taken for two-thirds of initial for- maldehyde to be removed for four different plant species. Orwell et al. [ 47 ] tabulated average 24-h removal of ben- zene ( C 0 - C t ) from an initial dose ( C 0 ) for seven plant species, while Orwell et al. [ 48 ] tabulated the required time to reach C t / C 0 = 0.5 for various combinations of plant spe- cies, toluene, xylene. Wolverton et al. [ 49 ] tabulated percent removed after 24 h of formaldehyde, benzene, and tri- chloroethylene (TCE) for several plant species. Yoo et al. [ 51 ] reported removal per hour per leaf area (ng m - 3 h - 1 cm - 2 ) for four plants removing benzene and toluene, providing initial concentrations and leaf surface areas. This CADR p calculation was carried out assuming their reported numbers corresponded to the fi rst hour of the chamber experiment. Yang et al. [ 50 ] presented results similarly for fi ve VOCs across several plant species organized qualitatively by per- formance (i.e., “ superior, ” “ intermediate, ” and “ poor ” per- forming plants). Zhang et al. [ 52 ] used a genetically modi fi ed version of Pothos Ivy, designed to enhance VOC uptake, and provided a percent reduction of concentration achieved over the timespan of days. The CADR p results for these studies are detailed in Table S1. For the second category, a CADR p value was computed using Eq. 3 for each reported point in the timeseries. Their average was taken as the overall CADR p for that experi- ment. Irga et al. [ 43 ] plotted percent of benzene removed for two plant setups over the course of four days. Kim et al. [ 45 ] took hourly measurements over a 5-h period of cumulative concentration reduction of formaldehyde nor- malized by leaf area (μg m - 3 cm - 2 ) for dozens of plant species spanning four categories. Their 36 woody and herbaceous foliage plants were used for this dataset. Given the leaf area of all plant species and an initial concentration in the chamber, conversion to CADR p was possible. Kim et al. [ 46 ] plotted concentration over time for two distinct plant species removing three different VOCs. The CADR p results for these studies are detailed in Table S2. For the third category, computing CADR p necessitated the use of Eq. 5 . The C outlet / C inlet expression within Eq. 5 may equivalently be thought of as the fractional VOC removal, which Liu et al. [ 57 ] reported using setup II for benzene. Three of their plant species yielded 60 – 80% removal, 17 species yielded 20 – 40%, another 17 yielded 10 – 20%, 13 removed less than 10%, and 23 did not yield any benzene removal. These CADR p results are detailed in Table S3. Assessing effectiveness of potted plants as indoor air cleaners The most prominent way by which VOCs are removed from indoor spaces is by outdoor-to-indoor air exchange. Air fl ows through a building at a certain fl ow rate ( Q b , m 3 / h), which may be a combination of mechanical ventila- tion, natural ventilation, and uncontrolled in fi ltration through the building envelope. Typically, Q b scales with building size, so the volume-normalized fl ow, which is the air exchange rate (called AER or λ , h - 1 ), is used to parameterize building air fl ow, where λ = Q b / V . This metric, as with CADR/ V , is a fi rst-order loss rate constant. Consequently, λ and CADR/ V can be directly compared to assess the relative ef fi cacy of each removal type. For air cleaning to be considered effective, the loss rate due to the air cleaner (CADR/ V ) must be on the same order or higher as that of the air exchange ( λ ) loss rate. So, if λ ≫ CADR/ V , most of the pollution removal is accomplished via air exchange alone. If λ ≪ CADR/ V , the air cleaner is responsible for the most removal. If λ = CADR/ V , the two loss mechanisms have the same in fl uence. For the case of multiple indoor potted plants combining their individual CADR p to remove VOCs from an indoor environment, the net CADR/ V loss rate may be computed given the density of plants in a given fl oor area ( ρ p , plants/ m 2 ), and the volume of the considered building in terms of the product of an average ceiling height ( h , m) and the given fl oor area ( A , m 2 ) by: CADR V ¼ CADR p ρ p A ³ ´ hA ð Þ ¼ CADR p ρ p h ð 6 Þ so that CADR/ V depends on CADR p , ρ p , and h . Since the ceiling height h is likely far less varied than CADR p or ρ p throughout the US building stock, excluding atriums, it is taken as a constant h = 2.5 m ≈ 8 ft throughout the following analysis. Comparisons of plant and AER loss mechanisms may be quanti fi ed by the effectiveness parameter ( Γ ), de fi ned as the fraction of VOC removal by which plant-induced air cleaning alone is responsible: Γ ¼ ð CADR = V Þ λ þ CADR = V ð Þ ð 7 Þ Thus, Γ is bounded by 0 and 1. If Γ ⟶ 0 ( λ ≫ CADR/ V ), the air cleaner is wholly ineffective compared to air exchange loss; if Γ ⟶ 1 ( λ ≪ CADR/ V ), the air cleaner dominates removal; and if Γ = 0.5 ( λ = CADR/ V ), the air cleaner and air exchange losses contribute equally to total removal. Substituting the right-hand-side of Eq. 6 into (CADR/ V ) in Eq. 7 facilitated a simulation-based 256 B. E. Cummings, M. S. Waring

parametric analysis of the effectiveness of VOC removal by potted plants indoors. Results and discussion CADR of potted plants in reviewed studies In total, 196 CADR p values were computed from the 12 reviewed chamber studies. A histogram expressing this entire dataset is provided in Fig. 1 a, which possesses a wide spread of nearly four orders of magnitude (ranging from 0.0004 – 0.2 m 3 h - 1 plant - 1 at 10th and 90th percentiles), a median CADR p = 0.023 m 3 h - 1 plant - 1 , and a mean (standard deviation) of 0.062 (0.089) m 3 h - 1 plant - 1 . Even though these CADR p values represent best-case scenarios (as they were computed assuming negligible chamber sorption and leakage), their magnitudes are exceedingly small. For context, typical gas or particle air cleaners pos- sess average CADR values on the approximate order of ~100 m 3 /h [ 65 – 67 ]. Figure 1 b resolves all 196 datapoints contributing to the Fig. 1 a histogram by type of VOC measured, labeled by the study ‘ s fi rst author and reference number. This fi gure thus explores the possibility of constraining CADR p for each VOC. Some of the data preliminarily indicates that certain VOCs may be more ef fi ciently removed by potted plants; for instance, Kim et al. [ 44 – 46 ] observed better for- maldehyde removal than for xylene, and Wolverton et al. [ 49 ] observed a much lower TCE removal than for for- maldehyde and benzene. However, these trends are not consistent throughout all studies; for instance, Yang et al. [ 50 ] observed similar removal of TCE, benzene, and toluene. Also, not enough studies assessed the same com- binations of VOCs suf fi cient for a de fi nitive trend to be established. Furthermore, some results vary largely from study-to-study even for the same VOC. More notably, however, the variance of CADR p values belonging to a particular study is much smaller than the variance of the dataset as a whole (intra-study values range 1 – 2 orders of magnitude, as compared to the total CADR p range of ~4 orders of magnitude). For example, of the 46 CADR p values calculated from Kim et al. [ 44 – 46 ], 32 of them (70%) reside above 0.1 m 3 h - 1 plant - 1 , making up 84% of the total 38 CADR p greater than 0.1 m 3 h - 1 plant - 1 . On the other end of this spectrum, all CADR p values belonging to Irga et al. [ 43 ] and Yang et al. [ 50 ] were less than 0.001 m 3 h - 1 plant - 1 , making up all but one other CADR p below 0.001 m 3 h - 1 plant - 1 . The one remaining CADR p existing in this lowest-performing interval belongs to Zhang et al. [ 52 ], who also conducted an experiment with chloroform, despite their use of genetically modi fi ed plants shown to enhance VOC uptake. We believe these trends suggest that the varying VOC removal performance among different research studies may be an indicator of differences among removal measurement methodologies, which should be further investigated. These perhaps include measurement techniques, plant and rhizosphere health, and other char- acteristics and relative sizes of the chamber, soil, pot, or the plant itself (e.g. VOC sorption onto competing surfaces). Effectiveness in typical buildings Using the entire CADR p dataset (Fig. 1 a), Eq. 6 was used to compute four sets of total CADR/ V loss rates, binned into four distinct plant density ( ρ p ) cases separated at logarithmic intervals (0.1, 1, 10, and 100 plants/m 2 ). In Fig. 2 , these loss Fig. 1 a Histogram of the CADR p dataset assembled from the reviewed chamber studies outlined in Table 1 . CADR p computations are detailed in the SI. b The CADR p data resolved by publication (labeled by fi rst author and reference number) and measured VOC Potted plants do not improve indoor air quality: a review and analysis of reported VOC removal. . . 257

Other considerations The conditions within sealed chambers do not scale up to the conditions of real indoor environments, which have high AER, large volumes, and persistent VOC emissions. Our conclusion that plants have negligible impact on indoor VOC loads is consistent with the results of fi eld studies that did not observe real VOC reductions when plants were placed in buildings. Despite potted plants not appreciably affecting indoor VOC concentrations, con- ducting chamber experiments on plants can remain a consequential effort. There is much to still be learned pertaining to the mechanisms of botanical uptake of VOCs. And, other applications of botanical fi ltration do exist (although passively cleaning indoor air is not one of them). Potential usefulness for further research perhaps lies in plant-assisted botanical bio-trickling puri fi ers (colloquially, “ biowalls ” or plant walls), which mechani- cally pull air through a porous substrate supporting plants and their root ecosystems [ 68 – 70 ]. These may create a more effective means of VOC removal because of their size, exposed rhizosphere, and controlled and continuous air fl ow. Some recent studies suggest that biowalls may yield CADRs on orders of 10 – 100 m 3 /h for certain VOCs [ 71 , 72 ], with the potential to make worthy contributions to indoor VOC removal. However, more biowall fi eld assessments and modeling endeavors are required to better hone our understanding of their true air cleaning and cost effectiveness. Regardless of application, more rigor is required in future chamber experiments to remove methodological ambiguities. First-order loss must be used to interpret results, and chamber leakage and surface sorption (to the chamber walls as well as to the pot and soil) must be accounted for. A standardized metric to be used in mass balance calculations, such as the CADR, should also be a critical aspect of future experimental reporting. Research also suggests that the plant itself is less crucial to VOC removal than the microbial community which resides within the rhizosphere/soil system of the plant [ 73 , 74 ]. The issue of bringing plant life into the indoor environ- ment is also a complex one, not settled by a potted plant ’ s (in)ability to reduce airborne VOCs. Indoor plants, by helping to create a more biophilic indoor environment, may have a positive impact on occupant well-being [ 75 ], which may also translate into productivity improvements for businesses. However, plant introduction may also come with certain costs or trade-offs. One potential associated downside of plants indoors may be increased humidity. Also, plants have been shown to produce certain VOCs under particular conditions [ 76 , 77 ]. So even if a potted plant works to slightly reduce, for instance, the persistence of formaldehyde indoors, its net impact on total VOC concentrations and overall indoor air quality is less clear. Spores and other bioparticle emissions may also be pro- duced by plants, which have been observed from biowall systems [ 65 , 74 , 75 ]. Continued rigorous laboratory and fi eld studies are required to develop a more complete and nuanced understanding of the interplay between plants and indoor environmental outcomes. Compliance with ethical standards Con fl ict of interest The authors declare that they have no con fl ict of interest. Publisher ’ s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional af fi liations. References 1. 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