The Safe Urban Harvests Study: A Community-Driven Cross-Sectional Assessment of Metals in Soil, Irrigation Water, and Produce from Urban Farms and Gardens in Baltimore, Maryland

Urban agriculture (UA), which includes growing food for human consumption, fiber, plant-based dyes, and other crops, and in some cases, raising livestock and bees, is increasing in popularity worldwide for its numerous public health, community, environmental, and economic benefits (Allen et al. 2008; Santo et al. 2016). Urban agriculture may also help achieve various targets established as part the United Nations’ Sustainable Development Goals (Nicholls et al. 2020). In addition, a growing body of literature uses an environmental justice lens to investigate soil contamination concerns in UA (Horst et al. 2017; Malone 2021; McClintock 2012).

Urban soils may be contaminated with heavy metals [e.g., lead (Pb), arsenic (As), cadmium (Cd)] due to current and historical industrial activities (e.g., fossil fuel combustion, waste incineration, chromate processing) (Harvey et al. 2017), legacy uses of Pb-based paint and leaded gasoline (Mielke et al. 1983, 2011; Mielke and Reagan 1998; Schwarz et al. 2012; Yesilonis et al. 2008), and applications of pesticides (e.g., lead arsenate) (Hood 2006; McBride et al. 2015) as well as their natural occurrence. Urban growers may be exposed to metals via incidental ingestion and inhalation of soil particles and via dermal contact with soil. Consumers may also be exposed via ingestion of contaminated urban-grown produce. A patchwork body of literature exists investigating the relationship between metals in soils and various types of urban-grown produce via uptake (Codling et al. 2016; Codling and Onyeador 2017; McBride et al. 2013, 2015) and other environmental processes (McBride et al. 2014). To date, much of this literature has been focused on a narrow set of metals (e.g., Pb, As) in areas known to be contaminated (Ramirez-Andreotta et al. 2013a, 2013b), resulting in limited generalizability for areas where previous evidence of contamination is absent and in a lack of clear, practicable recommendations for urban growers. As a result, urban growers may encounter unclear or inconsistent recommendations regarding best practices, and consumers may perceive that urban-grown produce is less safe than produce grown in other production systems (Kim et al. 2014). Globally, prior investigations of soil contamination (such as in backyard gardens in Australia (Harvey et al. 2018; Rouillon et al. 2017; Taylor et al. 2021); urban gardens in Spain (De Miguel et al. 2017; Izquierdo et al. 2015); and community gardens in New York, New York (USA) (McBride et al. 2014; Mitchell et al. 2014) have indicated wide variation in metals concentrations across geographic contexts. These findings emphasize the importance of site-specific screening and context-specific guidelines for urban agriculture.

Safety determinations are often made by comparing measured concentrations to established public health guidelines. Although the U.S. Environmental Protection Agency (U.S. EPA) has urban gardening guidance specifically for Pb in soils (U.S. EPA Technical Review Workgroup for Lead 2014), comparable guidance for other metals in soil (e.g., As, Cd) is not available. Existing guidelines, which vary by promulgating agency, are generally intended for the clean-up and remediation of brownfields (Jennings 2013); their appropriateness for the UA context and the safety of food grown in soils is unknown. Furthermore, guidelines for metals in produce exist for only a few metals (e.g., Pb, Cd) in some groups of foods (e.g., leafy greens, root vegetables) (Food and Agriculture Organization 1995). These guidelines are not enforceable and are not available for all metals that may be present in fruits and vegetables, making determination of safety difficult without additional exposure and risk assessments.

Baltimore City, Maryland (henceforth, Baltimore), is a postindustrial city in the mid-Atlantic region of the United States with an emerging and vibrant UA scene. The city’s government has enacted and passed numerous policies and programs to promote and encourage UA (Baltimore Office of Sustainability 2013, 2014; Halvey et al. 2021). Baltimore also has a robust network of nonprofit organizations that supports urban growers. Given Baltimore’s industrial history and legacies of Pb-based paint in homes, several studies have investigated concentrations of metals (primarily Pb) in city soils (Yesilonis et al. 2008), including some backyard garden soils (Mielke et al. 1983; Schwarz et al. 2016). No citywide attempt has been made to concurrently assess the safety of urban agricultural soils and the produce grown in them in Baltimore.

The Safe Urban Harvests study was a community-driven investigation that aimed to answer community questions about the safety of conducting UA in Baltimore. This study was designed, conducted, interpreted, and communicated in cooperation with several community partners who facilitated the gathering of opinions, questions, and concerns from Baltimore growers and consumers. Community partners included Baltimore City Office of Sustainability, Farm Alliance of Baltimore, Parks and People Foundation (and their formerly active Community Greening Resource Network), and University of Maryland Extension—Baltimore City. We measured the concentrations of nine metals [As, barium (Ba), Cd, chromium (Cr), copper (Cu), Pb, manganese (Mn), nickel (Ni), zinc (Zn)] in soil, irrigation water, and urban-grown produce and compared them to existing public health guidelines. To address urban growers’ questions, we characterized relationships between metals in soils and urban-grown produce. Finally, to address consumer questions about the safety of urban-grown produce, we compared the concentrations of metals in urban-grown produce with concentrations of the same metals in nonurban-grown produce (e.g., conventionally grown and U.S. Department of Agriculture (USDA)–certified organic produce purchased from grocery stores and farmers markets).

With rare exception, our findings suggest engaging in UA is safe with respect to metals exposures for urban growers and consumers of urban-grown produce in Baltimore. Concentrations of metals were highest in soils, followed by produce and irrigation water. Mean concentrations of all measured metals in irrigation water were below drinking water guidelines (Figure S3; Excel Table S6). This finding is consistent with the reality that most sites relied on municipal water at least in part as a source of irrigation water. Mean concentrations of nonessential metals in growing area soils were below public health guidelines for Ba, Cd, Pb, and Ni and at or below background for As and Cr (Excel Table S4).

Based on our comparisons of the concentrations of metals in urban- and nonurban-grown produce (Figure 2), our main finding for produce consumers is that we found no reason to recommend changes in produce consumption, either by type of produce or by production system (e.g., urban, peri-urban, conventional, or organic.) Although we observed a few statistically significant differences in metals concentrations between urban- and nonurban-grown produce for some produce items, we found no discernable pattern in these differences. Any observed differences are likely an artifact of the multiple comparisons made.

We observed variation in metals concentrations across vegetable types (Figures 3–4 and Figures S4–10). We observed the highest levels of Pb in root vegetables, regardless of production category (Excel Table S8). We observed higher levels of As, Ba, and Pb in urban-grown leafy greens in comparison with nonurban-grown (Figure 2), though almost all Pb concentrations were far below the World Health Organization’s recommendations for Pb levels in leafy greens (Excel Table S9). Although these absolute differences may be informative, additional modeling and assessment are needed to determine whether these differences translate into appreciable increased risks or benefits for consumers. Moreover, although we present concentrations of metals in different produce groups (Figures 3–4 and Figures S4–10) (e.g., nightshade fruits, root vegetables, leafy greens), our investigation was not designed to compare the safety of different kinds of fruits and vegetables to each other; further analyses must also consider differences in typical amounts consumed of each item.

We did not observe significant correlations between levels of metals in urban soils and urban-grown produce (Figure S11 and Excel Table S10), suggesting that a higher concentration of metals in soil is not a strong indicator of higher concentrations in produce grown in that soil and that determinations of safety for produce and soil should be made independently. This finding was consistent for all 13 produce items investigated. Across urban soils, we generally observed higher concentrations of metals in nongrowing areas, e.g., pathways and undisturbed areas (Excel Table S4 and S5). This finding may suggest that growers’ practices (e.g., importing soil and applying soil amendments) may dilute and/or reduce the concentrations of contaminants in soils (Moskal and Berthrong 2018), though we did not collect enough information about site-specific growing practices (e.g., types and amounts of amendments applied and at what frequency) to evaluate this hypothesis. Although our research contributes to the overall body of literature characterizing the relationship between metals in soil and produce, additional field-based experiments are needed to further characterize and quantify the human (e.g., growing and irrigation practices), ecological (e.g., weather conditions, soil health parameters), and plant-specific (e.g., cultivar) factors that may affect direct uptake of metals.

Although existing public health guidelines (Excel Table S2) are an important decision-making tool for public health practitioners and urban growers, our findings suggest the need for a broader discussion and more nuanced application of such guidelines. For example, applying the U.S. EPA’s Soil Screening Level for As ($0.68\text{\hspace{0.17em}ppm}$) as the sole decision-making tool in this study would have led to a determination that all 104 participating agriculture sites were not “safe” for production due to As levels in soil; however, this guideline as derived is lower than the naturally occurring background level of As in soils and is not intended to suggest the site is not suitable for the safe conduct of UA when exceeded. Rather, this guideline, when exceeded, suggests additional investigation of the metal exposure may be warranted via a site-specific risk assessment. Furthermore, this soil guideline has no connection to or consideration of levels of As in produce, so application of this guideline in isolation would not address questions about the safety of consuming produce grown in soils.

Using the U.S. EPA’s guideline for Pb in soils as the sole decision-making tool for determination of site safety would have made four UA sites “unsafe” for UA; however, in practice, 35 of these sites yielded at least one produce sample that exceeded Codex guidelines. Furthermore, we must acknowledge that these guidelines are generally not intended for the UA context, so the assumptions about exposure used to derive such guidelines may not be truly representative of exposures in UA. For example, the $400\text{\hspace{0.17em}ppm}$ guideline for Pb in soil, although widely used and cited as an acceptable level for Pb in soils, was derived in 1994 by the U.S. EPA for the specific purpose of protecting children from unacceptable exposures to Pb in residential soils and preventing 95% of the population of U.S. children from having blood Pb levels exceeding $10\mathrm{\mu }\mathrm{g}/\text{dL}$, which was the Centers for Disease Control and Prevention (CDC) action level for blood Pb at the time. Given increasing evidence that there is no level of Pb known to be without adverse effect in children, the CDC has reduced the blood Pb reference value to $5\mathrm{\mu }\mathrm{g}/\text{dL}$ (Centers for Disease Control and Prevention 2021). Questions remain, however, regarding whether the current guideline is adequately protective for children (Gilbert and Weiss 2006; Gottesfeld 2021; Paulson and Brown 2019). Although childhood and pregnancy are vulnerable life stages for Pb exposure, children’s exposures to soil are likely less and also less relevant for this context than those of agricultural workers and community gardeners who routinely engage in intentional contact with soils while growing food. Guidelines for Pb in soils intended to protect adults engaging in UA should be linked to more appropriate and relevant end points (e.g., cardiovascular, neurodegeneration, and others) for adult life stages. Interventions on Pb exposures are most successful if they address all the potential exposure pathways (e.g., dietary, inhalation, ingestion); in the context of UA, where metals exposures may be greater, critical pieces of information needed to derive and/or revise guidelines for soils are estimates of soil intake for children and adults engaged in agriculture. To date, the U.S. EPA has low confidence in existing estimates of soil intake among children and adults in the general population (U.S. EPA. 2017), and no estimates of soil intake exist for agricultural workers and other populations who have occupational or recreational soil contact.

In addition, these soil guidelines do not consider specific exposure patterns (e.g., time spent on site or specific activities conducted) or exposure-reduction behaviors (e.g., use of tools and/or personal protective equipment such as gloves). For example, more focused investigations of how growers divide their time among specific tasks (e.g., planting, irrigating, weeding) at both a daily and seasonal level would greatly improve our understanding and estimation of soil exposure in the UA context (Lupolt et al. 2021). Although existing exposure models have modeled the transport pathway of outdoor soil and indoor dust (Layton and Beamer 2009), additional investigation is needed to evaluate the relevance of these models to the UA context. Specifically, these models should incorporate the contribution of human interaction with the environment (e.g., urban growers’ deliberate and intentional disruption and transportation of soil). Furthermore, guidelines for metals in soil do not account for aggregate exposures that may occur via other pathways, such as inhalation and dietary intake. For urban growers, a single guideline for soil, irrigation water, or produce should not be applied as a single binary determination of the safety of UA at a given site, but as part of a nuanced site-specific assessment, with the limitations and caveats for each guideline noted.

Existing public health guidance for metals in produce adopts one of two approaches: a single food regulatory approach or a total diet guideline approach. The former describes the approach employed by the Food and Agriculture Organization in Codex Alimentarius (Food and Agriculture Organization 1995), which establishes regulatory limits for a single food (or food group) and a single metal using estimates of intake for that food and toxicity information about that metal. The latter approach, adopted by the U.S. Food and Drug Administration (U.S. FDA), establishes a daily tolerable intake for Pb in the entire diet for adults and children (Carrington and Bolger 1992). Such a guideline, which to date has only been provisionally established for Pb, is helpful for determining overall risks from dietary exposures, but better surveillance of the metals in the food supply is needed to develop actionable recommendations (by identifying specific foods or groups of foods) for consumers or regulatory agencies interested in reducing exposures.

A key methodological strength of our study was the use of laboratory-based analytical methods for soil and produce that allowed us to achieve low analytical detection limits (Excel Table S1). As other environmental sources of Pb continue to decline (Dignam et al. 2019; Resongles et al. 2021), it is increasingly necessary to quantify the remaining exposures with adequate precision. Thus, a sensitive laboratory method is critical for risk analyses and future decision-making. In addition, we recorded sample weights pre- and post lyophilization, which enabled us to calculate fresh weight concentrations using sample-specific water content, increasing the precision of our produce concentration data. Similar studies have reported metals concentration in dry weight only (Finster et al. 2004) or used standard estimates of water content (Kohrman and Chamberlain 2014; McBride et al. 2014). In addition, we are among the first to present metals concentrations of 13 commonly grown produce items, across 4 production methods, facilitating multiple comparisons by both produce type and production method.

Previous investigations (Mitchell et al. 2014; Spliethoff et al. 2016) of metals in soils used for UA have used similar public health guidelines for decision-making. In the absence of public health guidelines for metals in foods, other researchers have compared metals concentrations to concentrations measured in the U.S. FDA’s Total Diet Study (McBride et al. 2014; Ramirez-Andreotta et al. 2013a, 2013b). Other researchers have conducted risk assessments using default assumptions about incidental soil ingestion and/or produce consumption intended for the general population or study-specific assumptions (Entwistle et al. 2019; Hough et al. 2004; Manjón and Ramirez-Andreotta 2020; Ramirez-Andreotta et al. 2013a; Spliethoff et al. 2016). Although these assessments are helpful for assessing site safety in retrospect, their study-specific assumptions make comparison of studies and generalizability about the safety of UA difficult. Furthermore, because these studies were conducted on active UA operations, this approach may limit the transferability of findings to new operations and do not provide consistent characterization of site conditions and practices nor specific exposure pattern information to advance the development of public health guidelines intended for UA growers and consumers.

In recognition of the deficiencies of specific guidelines, additional research is needed to better understand agricultural practices among urban growers, and consumption patterns of urban-grown produce relative to nonurban produce among different populations to derive more applicable and nuanced public health guidelines. Given the limitations of existing public health guidelines and the limitations in their interpretation demonstrated in our study, our findings suggest a paradigm shift is needed in the establishment of public health guidelines that sufficiently account for the nuanced reality of metal exposure—including exposures via other pathways.

Based on our findings, we believe that guidelines for agricultural soils should be derived using estimates of soil ingestion and time in contact with soil specific to growers, rather than the general U.S. population. Guidelines for metals in produce should incorporate a more nuanced and tiered approach that considers exposures that occur through the diet overall as well as targets those individual foods that may contribute the most to dietary exposures. Furthermore, because fruits and vegetables (both urban- and nonurban-grown) are a critical part of a healthy diet and provide important nutritional benefits, a more nuanced risk–benefit model of guidance may provide more actionable recommendations for consumers. Guidance developed jointly by the U.S. FDA and the U.S. EPA for methylmercury in fish (U.S. Food and Drug Administration 2020) may be a helpful model for providing guidance for balancing nonessential metals and beneficial nutrients in a wider array of produce.

The authors thank the Baltimore farmers and gardeners who participated in the Safe Urban Harvests study and allowed us to test their soil, irrigation water, and produce. The authors are grateful to M. Gesese, who invested a great amount of time processing and analyzing both plant and soil samples at the USDA Adaptive Cropping Systems Laboratory. This study would not have been possible without the support of the Johns Hopkins Center for a Livable Future’s research assistants; the authors thank R. Burrows, S. Cebron, B. Evenson, E. Evans, M. Halvey, J. Huang, and M. Kessler for their tireless assistance with sample collection and processing and reporting back results to farmers and gardeners. The authors also thank G. Hamra and J. McGready for their data analysis advice.

This work was supported by the Santa Barbara Foundation (https://www.sbfoundation.org/). At the time of writing, S. Lupolt was also supported by a Johns Hopkins Center for a Livable Future-Lerner Fellowship, the Johns Hopkins 21st Century Cities Initiative the Johns Hopkins Education and Research Center for Occupational Safety and Health, supported by the National Institute for Occupational Safety and Health and the US Department of Agriculture Northeast Sustainable Agriculture Research and Education Program. The funders had no role in preparing, reviewing, or editing the manuscript.

The Materials Research Collaborative Access Team (MRCAT) operations are supported by the Department of Energy and the MRCAT member institutions. This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the U.S. DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. Although the U.S. EPA contributed to this article, the research presented was not performed by or funded by the U.S. EPA and was not subject to the U.S. EPA’s quality system requirements. Consequently, the views, interpretations, and conclusions expressed in this article are solely those of the authors and do not necessarily reflect or represent the U.S. EPA’s views or policies.

The authors declare they have no actual or potential competing financial interests.