Assessing risk to human health from tropical leafy vegetables grown on contaminated urban soils

Science of the Total Environment 408 (2010) 5338–5351

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Assessing risk to human health from tropical leafy vegetables grown on contaminated urban soils G. Nabulo, S.D. Young, C.R. Black ⁎ School of Biosciences, University of Nottingham, Nottingham, NG7 2RD, UK

a r t i c l e

i n f o

Article history: Received 16 February 2010 Received in revised form 17 May 2010 Accepted 17 June 2010 Available online 23 August 2010 Keywords: Human health Risk assessment Trace metals Tropical leafy vegetables

a b s t r a c t Fifteen tropical leafy vegetable types were sampled from farmers' gardens situated on nine contaminated sites used to grow vegetables for commercial or subsistence consumption in and around Kampala City, Uganda. Trace metal concentrations in soils were highly variable and originated from irrigation with wastewater, effluent discharge from industry and dumping of solid waste. Metal concentrations in the edible shoots of vegetables also differed greatly between, and within, sites. Gynandropsis gynandra consistently accumulated the highest Cd, Pb and Cu concentrations, while Amaranthus dubius accumulated the highest Zn concentration. Cadmium uptake from soils with contrasting sources and severity of contamination was consistently lowest in Cucurbita maxima and Vigna unguiculata, suggesting these species were most able to restrict Cd uptake from contaminated soil. Concentrations of Pb and Cr were consistently greater in unwashed, than in washed, vegetables, in marked contrast to Cd, Ni and Zn. The risk to human health, expressed as a ‘hazard quotient’ (HQM), was generally greatest for Cd, followed successively by Pb, Zn, Ni and Cu. Nevertheless, it was apparent that urban cultivation of leafy vegetables could be safely pursued on most sites, subject to site-specific assessment of soil metal burden, judicious choice of vegetable types and adoption of washing in clean water prior to cooking. © 2010 Elsevier B.V. All rights reserved.

1. Introduction The World's urban communities continue to increase proportionately faster than total global population as urbanisation progresses in less developed regions (UN-HABITAT, 2004). Urban expansion causes significant alterations in the physical environment and increases the accumulation of waste material resulting from human activity (Chen, 2007). There is increasing concern that the lack of suitable land for agriculture is prompting urban farmers to use contaminated land, such as waste disposal sites, to produce food crops. This situation is exacerbated by rapid population growth, urbanisation and industrialisation (Nabulo, 2009). Contamination of land with trace metals is common in urban and peri-urban areas due to past and present industrial activity and the use of fossil fuels (van Lune, 1987; Sanchez-Camazano et al., 1994; Sterrett et al., 1996; Wong, 1996; Chronopoulos et al., 1997). Moreover, in urban agriculture, wastewater and solid organic wastes are often the principal sources of irrigation and fertiliser used to enhance the yields of staple crops and vegetables (Urie, 1986; Feigin et al., 1991; Qadir et al., 2000). Municipal or industrial effluent and solid waste are often rich in trace metals and contribute significantly to metal loadings in irrigated and waste-amended urban soils

⁎ Corresponding author. Tel.: + 44 115 9516337; fax: + 44 115 9516334. E-mail address: [email protected] (C.R. Black). 0048-9697/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2010.06.034

(Nyamangara and Mzezewa, 1999; Nan et al., 2002; Singh et al., 2004; Mapanda et al., 2005). Contamination of soil with cadmium (Cd), nickel (Ni), copper (Cu), lead (Pb), arsenic (As), chromium (Cr), tin (Sn) and zinc (Zn) can be a primary route of human exposure to these potentially toxic elements (Moir and Thornton, 1989; Reilly, 1991; Lehoczky et al., 1998; DEFRA and EA, 2002). Trace metals may enter the human body via inhalation of dust, consumption of contaminated drinking water or ingestion of soil or crops grown on contaminated land (Cambra et al., 1999; Dudka and Miller, 1999). A primary concern in urban agriculture is the transfer of trace metals from vegetables through the food chain to humans; indeed, it has been estimated that this route contributes up to 70% of the dietary intake of Cd (Ryan et al., 1982; Wagner, 1993). Vegetables may accumulate trace metals from contaminated soil and are also exposed to surface deposition onto their shoots in polluted atmospheric environments. However, little information is available regarding human exposure to contaminants via urban agriculture in developing cities (Lock and de Zeeuw, 2001). In Kampala City, Uganda, and many other cities in the developing World, there is inadequate or non-existent waste collection, rapidly increasing traffic and largely unchecked industrial contamination (Cole et al., 2003). Thus, urban agriculture faces major problems in balancing demands associated with increasing populations against potential hazards arising from the use of contaminated urban sites for food production and effluents for irrigation. A previous screening experiment under glasshouse conditions involving 24 tropical and temperate leafy vegetable types grown on a

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marginally contaminated soil with a long history of sewage disposal showed that tropical vegetables exhibited greater variability in Cd uptake than temperate types (Nabulo, 2009). Cadmium concentration in the shoots of tropical vegetables differed significantly between species, being greatest in Gynandropsis gynandra, whereas Vigna unguiculata exhibited a very limited capacity to accumulate Cd from contaminated soil. The study also showed that some leafy vegetable types accumulate Cd to concentrations exceeding statutory limits

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(FAO/WHO-CAC, 2001; EC, 2001), even when grown on marginally contaminated soil, whereas others offer substantial potential for safe cultivation on more heavily contaminated urban sites. In the present study, selected tropical leafy vegetables were harvested from farmers' gardens on land contaminated by previous or current waste disposal at nine sites in and around Kampala City, Uganda. Sources of contamination included irrigation with wastewater, effluent discharge from industry and dumping of solid waste. The

Fig. 1. Map showing location of study sites in Kampala City; N.B. the Kololo site was not used in this study but is included for completeness as results for all sites are presented in a companion paper. The Kilembe and Masese sites are located c. 100 km north-east of Kampala City.

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selected sites were all used by local urban farmers to grow popular leafy vegetables for domestic use or sale. The objectives were to: (i) determine trace metal concentrations in the edible component of indigenous leafy vegetable crops grown under realistic field conditions in a tropical urban environment; (ii) assess the association between sources of trace metal contamination and uptake by plants; and (iii) quantify the potential risk to children and adults of consuming leafy vegetables grown in urban agriculture. The hypotheses tested were that, in Ugandan urban agriculture: (i) uptake of trace metals by vegetables grown on some contaminated sites may pose a risk to human health; ii) toxic hazard is highly dependent on the type of leafy Table 1 Study sites showing current and past land use and potential sources of trace metal contamination. Site

Current or past use

Railway

Located in the premises of a railway station and used for disposal of scrap metal and other solid waste. A wastewater channel from Kampala City runs through the site Dump site for solid waste including glass, metal waste, batteries, and plastics Former dumping site for municipal solid waste Location of former copper smelter; now a wastewater and pyritic waste disposal site Receives wastewater and effluent from an oil refinery; industrial effluent was discharged from a former copper smelter; farmers apply pesticides Receives wastewater and raw sewage from a nearby university and wastewater from a major hospital; surrounded by small-scale industry and metal workshops Ship-landing site on shore of Lake Victoria Situated in an industrial area and occasionally flooded by effluent from battery and steel rolling industries Receives untreated sewage from Luzira Prison and wastewater and effluent from surrounding industries

Kiwanataka Lugogo Kilembe Masese

Katanga

Port Bell Radio Murchison Bay

vegetables cultivated and; (iii) washing vegetables prior to cooking and consumption reduces risk by removing superficial contaminants resulting from atmospheric deposition or soil splash. 2. Materials and methods 2.1. Site characteristics and plant and soil sampling The study was conducted on farmers' gardens situated on seven contaminated sites used to grow vegetables for subsistence or commercial consumption in Kampala City (Fig. 1) and two sites located c. 100 km east of Kampala (Kilembe and Masese). Criteria for site selection included historical or current disposal of solid waste, effluent discharge from industry, and irrigation with wastewater. The study sites described in Table 1 were managed according to local practice by urban farmers, who allowed their crops and soil to be sampled for a fee. To assess the extent of within-site variation, each site was divided into three replicate blocks based on visible differences in soil characteristics and the form of contamination present. A composite soil sample from the 0 to 20 cm horizon (c. 1 kg) was taken from each replicate block at all sites, comprising 16 sub-samples collected at regularly spaced locations within each block. The soil samples were air-dried, ground and passed through a 6 mm sieve to remove debris and gravel before being sub-sampled (c. 0.5 kg) for transport to the UK for analysis. The 15 leafy vegetable types examined were Amaranthus hybridus L., A. lividus L. var. ascendens (Lois.) Thell., A. dubius Mart. ex Thell., Brassica oleracea L. Acephala group, B. oleracea L. Capitata group, Cucurbita maxima Duch., Colocasia esculenta L., Corchorus olitorius L., Gynandropsis gynandra L. Briq., Hibiscus cannabinus L., Phaseolus vulgaris L., Solanum aethiopicum Shum group, S. nigrum L., Spinacea oleracea L. and Vigna unguiculata L. Walp (Table 2). The vegetables were

Table 2 Description of the leafy vegetables examined, their edible components and cooking methods for leafy material. Vegetable type

Family

Common name

Duration

Edible parts

Cooking methods for leaves

Amaranthus hybridus (L.)

Amaranthaceae

Rough pigweed, Goyi or goi in Uganda

Annual/ perennial

Cooked as spinach, added to soups, salads

Amaranthus lividus (L.) subsp. ascendens (Lois.) Thell. Amaranthus dubius (Mart. ex Thell.) Brassica oleracea (L.) Acephala Brassica oleracea (L.) Capitata Corchorus olitorius (L.)

Amaranthaceae

Purple amaranth, Ebugga in Uganda

Annual

Leaves and tender shoots, seeds used as a pseudo-cereal Leaves and tender shoots

Amaranthaceae

Annual

Leaves and tender shoots Leaves

Steamed, used as pot herb

Brassicaceae

Spleen amaranth, Doodo in Uganda Collards or borekale, sukuma wiki in East Africa Cabbage

Leaves

Boiled, fried, sautéed or stuffed

Tiliaceae

Jew's mallow, Otigo in Uganda

Annual/ perennial

Leaves

Colocasia esculenta (L.)

Araceae

Perennial

Cucurbita maxima (Duch.)

Cucurbitaceae

Taro, cocoyam, arrowroot or Ttimba in Uganda Pumpkin, Ensujju in Uganda

Gynandropsis gynandra (L.) Briq.

Capparaceae

Annual

Hibiscus cannabinus (L.)

Malvaceae

Phaseolus vulgaris (L.)

Fabaceae

Solanum aethiopicum (L.) Shum group Solanum nigrum (L.)

Solanaceae Solanaceae

Spinacea oleracea (L.)

Chenopodiaceae

African spiderplant or cat's whiskers, Jobyo or Ejjobyo in Uganda Kenaf, Malakwang or Lubeera in Uganda Common bean, French bean, Ebijanjaalo in Uganda Ethiopian nightshade, scarlet eggplant, Nakati in Uganda Black Nightshade, Ensugga in Uganda Spinach

Leaves, flowers, rhizomes, stalks Leaves, flowers, fruits, seeds Leaves

Added to coarse vegetables to make them easier to swallow, used as a pot herb Boiled, steamed or fried

Vigna unguiculata (L.) Walp.

Fabaceae

Cowpea, Eggobe in Uganda

Brassicaceae

Biennial/ perennial Annual

Annual

Cooked as spinach, used as pot herb

Boiled or fried briefly

Chopped finely, boiled or steamed Boiled or steamed, used as a pot herb in soups

Annual

Leaves, flowers, seed, roots Leaves, seeds

Boiled or steamed, used as pot herb or in soups Boiled or steamed

Annual

Leaves, fruit

Boiled or steamed

Annual

Leaves, ripe orange fruits Leaves

Cooked as spinach, added to soups or stews, salads Steamed or boiled, salads

Leaves, seeds

Boiled or steamed

Annual

Annual/ biennial Annual

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sampled by harvesting plants from each of the 16 regularly spaced locations in each block used to collect soil samples for analysis. The edible portion was separated from the stems and roots and subsampled to provide a representative composite sample for each block.

where

2.2. Sample preparation and analysis

In Eq. (1), HQM represents the hazard quotient resulting from ingestion of a specified trace metal (M) through consumption of leafy vegetables, ADDM is the average daily dose (mg kg− 1 d− 1) of the metal and RfDM is the reference dose (mg kg− 1 d− 1), defined as the maximum tolerable daily intake of a specific metal that has no adverse effect. In Eq. (2), DI denotes the daily intake of leafy vegetables (kg d− 1), MFveg represents trace metal concentration in the vegetable tissue (mg kg− 1 fresh weight (fw)) and WB is the body weight (kg) of the target individual. The daily intake of fresh leafy vegetables used in the calculation was 182 g fw d− 1 for adults and 118 g fw d− 1 for children (Steyn et al., 2003). Variation in HQM values between vegetable types will therefore reflect their relative affinity for specific trace metals and differences in the RfDM for individual trace elements. A value of ADDM for a specific trace metal which exceeds the corresponding RfDM (HQM N 1) implies a potential risk to consumers. Mean body weights for adults and children were assumed to be 55.7 and 14.2 kg respectively (GEMS, 2000). Reference dose (RfD) values for selected metals are shown in Table 3.

The fresh weight of leafy vegetable samples was determined before washing approximately half of the material in tap water and then in distilled water to remove dust and other surface contamination; this material was dried at 60 °C for 48 h before being weighed. The other half of the edible shoot material was dried and weighed without washing. All plant samples were ground in an ultracentrifugal mill (Retsch, Model ZM200, Germany) fitted with a 0.5 mm titanium screen. The finely ground material (200 mg) was digested in pressurised PFA vessels in 6.0 mL of 70% Trace Analysis Grade (TAG; Thermo-Fisher Scientific, UK) HNO3 with microwave heating (Anton Paar ‘Multiwave’ fitted with a 48-place rotor). Digested samples were diluted to 20 mL using milli-Q water (18.2 MΩ cm) and stored un-refrigerated (30% HNO3) pending elemental analysis. Immediately before analysis, samples were diluted 1-in-10 with milli-Q water. Soil samples were sieved again (b2 mm) and sub-samples ground in a planetary ball mill (Retch, Model PM400, Germany) with 80 mL agate vessels and 20 mm agate balls at 200 rpm for 2 min. Approximately 200 mg of each finely ground soil sample was digested using 2.5 mL hydrofluoric acid (HF; 40% AR), 2.0 mL HNO3 (TAG; 70%), 1.0 mL HClO4 (AR; 60%) and 2.5 mL H2O in a 48-place block digestor (Model A3, Analysco Ltd, UK) with PFA digestion vials. Digested samples were diluted to 50 mL using milli-Q water (18.2 MΩ cm) and stored un-refrigerated in universal sample bottles (c. 5% HNO3) pending elemental analysis. Soil digests were diluted 1-in-10 with milli-Q water prior to analysis. Multi-element analysis was undertaken by ICPMS (Model X-SeriesII, Thermo-Fisher Scientific, Bremen, Germany) in ‘collision cell mode’ (7% hydrogen in helium) to eliminate polyatomic interference. Samples were introduced from a covered autosampler (Cetac ASX-520 with 4 × 60-place sample racks) through a concentric glass venturi nebuliser (Thermo-Fisher Scientific, Bremen, Germany; 1 mL min− 1). Internal standards introduced to the sample stream via a T-piece included Sc (50 μg L− 1), Rh (10 μg L− 1) and Ir (5 μg L− 1) in 2% TAG HNO3. External multi-element calibration standards (Claritas-PPT grade CLMS-2, Certiprep) included Al, As, Ba, Bi, Ca, Cd, Co, Cr, Cs, Cu, Fe, K, Mg, Mn, Na, Ni, Pb, Rb, Se, Sr, U, V and Zn in the range 0–100 μg L− 1. Sample processing was undertaken using Plasmalab software (Vs 2.5.4; Thermo-Fisher Scientific, Bremen, Germany) using internal crosscalibration where required. The values for each digestion batch (48 samples) were corrected using two blank digestions and quality control was assessed using two certified reference materials, CRM 1573a (tomato leaves) and CRM 2711 (Montana soil) from the National Institute of Standards and Technology (NIST). pH was determined for soil:water suspensions (1:2.5 ratio) using a pH meter and combined glass electrode (Ag/AgCl) (Model pH 209, HANNA Instruments, Bedford, UK). Five grams of b2 mm sieved air-dry soil were shaken in 50 mL centrifuge tubes (Oak Ridge, Roskilde, Denmark) with 12.5 mL deionised water end-overend at 27 rpm for 30 min.

ADDM =

Data were analysed by analysis of variance using Genstat version 11 to determine mean values, standard errors of the mean and standard errors of the difference between means. 3. Results and discussion 3.1. Trace metal concentrations in soil Soil concentrations of Cd, Zn, Ni, Cu, Pb and Ba (Fig. 2) and Cr (data not shown) varied greatly between sites (P b 0.001). The values for Cd, Zn, Cu, Ba and Cr also varied between blocks within sites (P b 0.05), suggesting localised variation in waste deposition. By contrast, the absence of significant variation in soil Pb and Ni concentrations between blocks at all sites suggests that the sources of pollution for these elements were geological or resulted from more diffuse anthropogenic sources. Concentrations of Cd, Cu and Zn varied from 0.05 to 3.62 mg Cd kg− 1 at the Masese and Railway sites, from 6.62 to 1480 mg Cu kg− 1 at Port Bell and Kilembe, and from 30.1 to 1690 mg Zn kg− 1 at Port Bell and Kinawataka. The concentrations of other elements ranged from 6.60 to 940 mg Pb kg− 1 at Port Bell and Lugogo, 2.67 to 76.8 mg Ni kg− 1 at Port Bell and Kilembe, 88.9 to 790 mg Ba kg− 1 at Masese and Lugogo, 8.14 to 200 mg Cr kg− 1 at Port Bell and Masese and 1.76 to 17.3 mg As kg− 1 at Port Bell and Lugogo. Soil Zn and Cd concentrations were closely correlated (r2 = 0.90), reflecting their common geochemical and Table 3 Metal reference doses (RfDs) for Cd, Ni, Pb, Zn and Cu. Metal

Critical effects

RfD (mg kg− 1 d− 1)

Cd1 Ni1

Affects renal and bone health Developmental effects in animals and skin hypersensitivity reactions in humans Inhibition of ferrochelatase resulting in accumulation of erythrocyte protoporphyrin Decrease in erythrocyte Cu, Zn-superoxide dismutase (ESOD) activity in healthy adult male and female volunteers Increased protein droplets in epithelial cells of proximal convoluted tubules in rats

3.6 × 10− 3 1.2 × 10− 2

Pb2

The risk to human health resulting from consumption of leafy vegetables was expressed as a ‘hazard quotient’ (HQM) calculated as:

Zn3

Cu4

HQ M

ð1Þ

ð2Þ

2.4. Statistical analysis

2.3. Risk assessment

ADDM = RfDM

ðDI × MFveg Þ WB

3.5 × 10− 3 3.0 × 10− 1

4.0 × 10− 1

Environmental Agency, 2009c; 2JECFA, 2006; 3IRIS, 2000; 4WHO, 1982.

1

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industrial origin (Singh and McLaughlin, 1999). However, the lack of covariance for other trace metal concentrations across sites suggests diverse sources of contamination rather than variation in loading of a single source of waste. Soil Cd, Zn, Pb and Ba concentrations were greatest at Lugogo (Fig. 2a, b, e, f). Lead and Cd concentrations exceeded the UK soil guideline values (Environment Agency, 2009a), while Ba and Zn concentrations exceeded the permitted UK sludge limit for agricultural soil (MAFF, 1993). This site was formerly used by Kampala City Council to dump solid waste from industrial, hospital and domestic sources and is close to a major highway. Soil at Kinawataka exceeded the UK sludge limit for Zn (MAFF, 1993; Fig. 2b) and also had elevated concentrations of Pb and Ba (Fig. 2e, f). Kinawataka is a former solid waste disposal site used by

Kampala City Council, has a wastewater channel passing through the area and served as a car-washing bay. Trace metal contamination resulted mainly from dumping of waste, although motor vehicle emissions and debris are likely to have contributed to soil contamination with Pb and Zn. The Katanga and Murchison Bay sites were both contaminated by wastewater from untreated sewage systems. Katanga is situated in a valley between two hills, the sites of Makerere University and Mulago Hospital, and is surrounded by small-scale industry. Murchison Bay is located on the shores of Lake Victoria and receives untreated sewage from Luzira Prison and industrial wastewater from the Luzira industrial site, a possible industrial source of the elevated soil Ba concentration at this site (Fig. 2f). Previous studies in the Lake Victoria Basin have shown high trace metal concentrations in sediments

Fig. 2. Mean soil concentrations of (a) Cd, (b) Zn, (c) Ni, (d) Cu, (e) Pb and (f) Ba for all study sites. Standard errors of the difference between means (SED) are shown. Vertical bars associated with each histogram show double standard errors of the mean (n = 3). Sites are arranged in descending order with respect to soil Cd concentration.

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associated with battery and metal fabricating industries (Pb), operations involving recovery of scrap metal (Zn and Cd), a former Cu smelter (Cu, Pb, Ni and Co), and tanneries and pharmaceutical industries (Cr) (Muwanga and Barifaijo, 2006). At Kilembe, soil Ni and Cu concentrations exceeded the UK sludge limits (MAFF, 1993; Fig. 2c, d) and Cu concentration was greater than at any other site (P b 0.05). The Kilembe site was situated between a smelter, located at the top of a hill, and Lake Victoria, separated by the Masese wetland at the foot of the slope. The elevated soil Cu concentration at this site resulted from effluent discharge from the smelter down-slope to the wetland, although the severity of contamination varied greatly between blocks as these were situated over a wide area; blocks situated in the path of effluent flow were more severely contaminated than more distant blocks which received effluent only during periods of heavy rain. The Cu sulphide ore used in the smelter also contained high concentrations of Co and operations to extract this from the slag produced by Cu smelting involved crushing and stock-piling material beside the smelter. As a result, additional Cu and Co would have been transported in surface run-off to the low-lying land. The Masese wetland is situated in the valley below the Kilembe smelter and close to an oil refinery, and so was exposed to Ni, Cu (Fig. 2c, d) and Co (results not shown) contamination; the concentrations of these elements were lower than at Kilembe (P b 0.05). However, soil Cr concentration was greater at Masese than at Kilembe (P b 0.05; results not shown) and exceeded the SGV value (DEFRA and EA, 2002; currently under review), suggesting that contamination with Cr did not originate exclusively from the smelter, or that the transport characteristics of contaminants from the smelter varied between sites. The Radio Uganda site is a man-made wetland in an industrial area which constantly receives wastewater from Kampala City and effluent from nearby industries. The latter includes a battery production plant, which is probably the major cause of the elevated soil Pb concentration (Fig. 2e). The elevated soil Zn concentrations (Fig. 2b) probably originated from other nearby industries, including a steel rolling plant and tyre manufacturer. The Railway site situated in Kampala's Central Division, close to the railway station, was a scrapyard for railway fuel tankers, metallic waste and scrap metal. A wastewater channel separates the site from the Mukwano soap production plant. Trace metal contamination may be attributed to several sources, including the wastewater channel, motor vehicle emissions, industry and, perhaps most importantly, the scrapyard. Surprisingly, soil trace metal concentrations were relatively low, with the exception of Cd (third highest of all sites), but varied between blocks (P b 0.05; Fig. 2a). The Port Bell site had the lowest concentrations of Zn, Ni, Cu, Pb (P b 0.05; Fig. 2b–e) and Cr (results not shown) and the second lowest Cd concentration of all sites. This site is a wetland on the shore of Lake Victoria which is irrigated with wastewater containing mixed effluent from municipal and industrial sources in and around Kampala City. The area was reclaimed by farmers to grow vegetables when the water table decreased due to drought and substantial water abstraction from Lake Victoria. The low trace element concentrations in the soil suggest that limited quantities of contaminants were supplied in the wastewater, in agreement with a recent study in Nairobi City which showed that trace metal concentrations in soil irrigated with wastewater from untreated sewage sludge were very low (Murage, 2009), and below the UK sludge limit for agricultural soil (MAFF, 1993). The contaminant profile contrasts with that for Murchison Bay, which received a greater proportion of effluent from industrial sources. 3.2. Trace metal concentrations in four leafy vegetables grown at five sites Considerable diversity in vegetable cultivation was apparent in Kampala City and its immediate peri-urban environment as not all

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fifteen vegetable types chosen for study were grown at all nine study sites. The most popular vegetables were A. dubius, C. maxima, A. hybridus and G. gynandra, which were present in at least 10 blocks spanning five sites, Lugogo, Kinawataka, Railway, Katanga and Masese; this combination of sites and vegetables was therefore chosen for more detailed analysis. Table 4 shows that soil pH and mean elemental concentrations varied greatly between these sites; elemental concentrations exceeded UK Soil Guideline Values for Cd and Pb at Lugogo and for Cr at Masese. A. dubius is a common edible weed which grows spontaneously on waste land from seeds deposited in household waste and provides a year-round supply of fresh vegetables for low-income families in Kampala. The young leaves of C. maxima are cooked as leafy vegetables and its fruit are also consumed. G. gynandra is also a weed which is cultivated for home consumption, whereas A. hybridus is often produced commercially and the young shoots are harvested and sold as leafy greens. Cadmium, Cu, Pb and Ba concentrations in washed shoot tissue differed between both vegetable types and sites (P b 0.05; Fig. 3a, d, e, f), but no significant differences between vegetable types were found for Zn, Ni (Fig. 3b, c) and Cr (results not shown), although values for specific vegetable types varied between sites (P b 0.05). Concentrations expressed on a dry weight basis ranged from 0.022 to 0.463 mg Cd kg− 1, 30.9–160 mg Zn kg− 1, 0.46–3.66 mg Ni kg− 1, 8.58–23.8 mg Cu kg− 1 and 0.23–5.69 mg Pb kg− 1. Elevated concentrations of Cd, Zn and Ba were apparent at Lugogo (Fig. 3a, b, f), for Ni at Kilembe (Fig. 3c) and Pb at Kinawataka and Lugogo for at least some vegetables. G. gynandra accumulated the highest mean Cd concentration across all sites (Fig. 3a), demonstrating its greater ability to absorb this element from contaminated soil. In marked contrast, C. maxima accumulated the lowest Cd concentration across all sites, suggesting an exceptional ability to restrict uptake of this element from contaminated soil. Averaged over all study sites, tissue Cd concentration was 6-fold greater in G. gynandra than in C. maxima, reflecting results from earlier glasshouse experiments and reinforcing the view that G. gynandra may pose a significant health risk resulting from ingestion of Cd (Nabulo, 2009). However, only Cd was effectively excluded by C. maxima and the concentrations of other metals were similar to, or exceeded, those for the other vegetable types; indeed, C. maxima was among the worst in terms of accumulating Ni across all sites and Pb at Kinawataka (Fig. 3c, e). Nickel concentration was lower in A. hybridus than in the other vegetable types, most of which clearly showed the influence of variation in soil Ni concentration between sites, with uptake being particularly high at Kilembe and Masese (Fig. 3c). A. dubius and A. hybridus accumulated the highest Zn concentrations at all

Table 4 pH and mean trace metal concentrations in soil for five selected sites on which the same vegetable types were grown; sites are arranged in descending order of Cd concentration. Bold values indicate where soil trace metal concentrations exceed UK Soil Guideline Values (SGV). Site

Lugogo Kinawataka Railway Katanga Masese SGV UK Sludge Limit

pH

7.28 6.66 7.12 4.67 5.63 ≤ 5.5 5.6–6.0 6.1–7.5

Trace metal concentration (mg kg− 1 dw) Cd

Ni

Cu

Zn

Pb

Ba

Cr

2.13 1.18 0.904 0.460 0.098 1.8a 3.00 3.00 3.00

32.4 39.0 19.1 20.1 41.1 230b 50.0 60.0 75.0

238 141 35.9 42.8 249 na 50.0 100 135

1060 742 179 313 58.6 na 300 250 300

770 247 82.0 97.3 9.44 450c 300 300 300

641 321 202 236 91.4 na na

114 123 62.3 53.8 196 130cd 400 400 400

a SGV, Soil Guideline Value, Environment Agency (2009a); bEnvironment Agency (2009b); cDEFRA and the Environment Agency (2002); dcurrently under review. na = not available.

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contaminated sites (Fig. 3b), which might potentially be beneficial for health, although the corresponding relatively high Cd concentrations (Fig. 3a) could pose a risk to human health. A. dubius and A.

hybridus also had the highest concentrations of Ba, especially at Lugogo (Fig. 3f), while, G. gynandra had by far the highest Cu concentration at Kilembe (Fig. 3d).

Fig. 3. Mean concentrations of (a) Cd, (b) Zn, (c) Ni, (d) Cu, (e) Pb and (f) Ba for A. dubius, A. hybridus, C. maxima and G. gynandra plants grown at five study sites. SED represents the standard error of the difference between means for the vegetable type x soil interaction. Vertical bars associated with each histogram show double standard errors of the mean (n = 3).

Table 5 Trace metal concentrations in the edible shoots of leafy vegetables sampled from contaminated sites before and after washing with deionised water. The concentration range and mean values for individual elements are shown; standard errors of the mean are shown in parenthesis. *Denotes P b 0.05; NS = no significant difference. n

A. dubius

16

C. maxima

14

A. hybridus

12

G. gynandra

12

V. unguiculata

12

B. oleracea Acephala

9

C. esculenta

8

B. oleracea capitata

5

C. olitorius

5

S. nigrum

5

S. aethiopicum

4

H. cannabinus

3

P SED

Ni (mg kg− 1 dw)

Cu (mg kg− 1 dw)

Zn (mg kg− 1 dw)

Pb (mg kg− 1 dw)

Cr (mg kg− 1 dw)

Unwashed

Washed

Unwashed

Washed

Unwashed

Washed

Unwashed

Washed

Unwashed

Washed

Unwashed

Washed

0.0320–1.03 0.236 (0.0895) 0.00986–0.170 0.042 (0.0123) 0.0258–0.389 0.142 (0.0321) 0.0441–0.555 0.229 (0.0515) 0.0142–1.0439 0.129 (0.0848) 0.0879–0.578 0.227 (0.0572) 0.0222–0.509 0.233 (0.060) 0.065–0.215 0.119 (0.0266) 0.0732–1.69 0.477 (0.308 0.0910–0.565 0.286 (0.0773) 0.0522–0.154 0.093 (0.0269) 0.0851–0.297 0.184 (0.0617) * 9.41

0.050–1.10 0.237 (0.0937) 0.01–0.15 0.0387 (0.00943) 0.04–0.51 0.172 (0.0339) 0.04–0.51 0.212 (0.0435) 0.01–1.29 0.144 (0.104) 0.08–0.32 0.240 (0.0587) 0.03–0.47 0.264 (0.0673) 0.05–0.16 0.136 (0.0381) 0.09–1.48 0.469 (0.264) 0.10–0.60 0.298 (0.0854) 0.07–0.31 0.142 (0.0562) 0.15–0.25 0.211 (0.0317) NS 0.159

0.432–5.63 1.86 (0.557) 0.0810–1.98 2.25 (0.511) 0.0823–5.34 0.900 (0.185) 0.237–4.40 1.57 (0.432) 0.262–9.98 2.15 (0.772) 0.0.0823–5.34 1.59 (0.634) 1.06–7.10 3.30 (0.703) 0.224–3.09 1.28 (0.536) 0.216–1.38 0.780 (0.219) 0.648–2.09 0.974 (0.334) 0.086–4.97 1.87 (1.11) 0.359–2.14 1.13 (0.527) NS 1.15

0.460–4.66 1.62 (0.447) 0.70–5.65 2.00 (0.378) 0.38–4.42 0.855 (0.117) 0.38–4.42 1.53 (0.343) 0.31–3.09 1.28 (0.253) 0.19–2.96 1.04 (0.314) 0.75–6.47 3.59 (0.839) 0.31–1.65 1.49 (0.669) 0.65–1.08 0.78 (0.141) 0.29–2.90 1.08 (0.467) 0.24–3.43 2.34 (0.720) 0.25–1.74 0.817 (0.465) * 0.74

6.93–17.1 11.3 (0.951) 1.88–18.7 13.9 (1.11) 3.00–15.7 10.4 (0.963) 1.62–24.1 13.0 (1.89) 1.43–40.3 11.9 (2.82) 1.66–25.9 7.06 (2.47) 9.05–30.1 18.2 (2.27) 4.39–8.55 6.66 (0.738) 7.11–19.4 15.2 (2.20) 3.18–21.0 14.9 (3.16) 2.31–32.3 17.2 (8.26) 1.24–12.5 8.45 (3.62) * 3.66

6.47–14.9 10.5 (0.726) 2.10–19.0 14.0 (1.16) 4.92–23.8 9.77 (0.768) 4.92–23.8 13.1 (1.520) 1.26–14.9 9.72 (1.29) 1.31–15.4 6.12 (1.48) 8.61–31.1 18.1 (2.35) 3.89–7.91 5.86 (0.647) 7.03–18.7 15.2 (2.17) 3.01–22.7 15.6 (3.64) 5.60–33.0 19.0 (6.71) 2.13–12.0 8.59 (3.23) * 2.50

56.2–829 180 (78.7) 26.8–143 60.2 (8.76) 33.2–155 79.4 (11.2) 41.4–332 91.4 (22.7) 27.7–333 77.0 (24.0) 55.4–635 182 (61.9) 53.6–159 98.1 (13.5) 28.2–62.4 37.2 (6.45) 28.4–163 71.0 (24.4) 31.8–88.0 52.3 (10.1) 27.4–68.9 46.3 (9.51) 33.2–55.3 41.6 (6.92) NS 74.3

52.4–743 168 (70.6) 28.5–154 59.5 (8.81) 38.4–310 80.2 (12.5) 38.4–310 87.9 (21.8) 27.1–270 72.4 (19.7) 39.4–610 172 (60.2) 62.9–146 104 (12.1) 23.9–57.1 36.3 (5.75) 14.1–161 70.7 (28.2) 32.3–55.3 42.7 (3.800 38.2–56.1 46.5 (4.42) 10.5–34.6 25.9 (7.75) NS 70.7

0.154–12.6 2.83 (1.23) 0.09–7.91 2.32 (0.622) 0.179–5.82 1.97 (0.425) 0.218–22.2 4.46 (2.01) 0.0961–13.9 2.76 (1.16) 0.0585–2.64 1.03 (0.332) 0.138–0.918 0.396 (0.089) 0.137–1.10 0.451 (0.179) 0.135–6.69 2.38 (1.16) 0.205–2.61 1.07 (0.438) 0.271–1.58 0.889 (0.301) 0.143–1.52 0.933 (0.438) NS 2.32

0.11–4.70 1.23 (0.393) 0.18–5.34 1.53 (0.418) 0.11–5.69 1.18 (0.167) 0.11–5.69 1.35 (0.433) 0.10–2.60 0.901 (0.246) 10–1.47 0.503 (0.146) 0.04–0.55 0.226 (0.053) 0.10–0.42 0.247 (0.064 0.51–1.37 0.838 (0.236) 0.16–1.25 0.600 (0.205) 0.16–3.34 1.34 (0.712) 0.33–0.64 0.480 (0.095) * 0.676

0.381–7.75 2.82 (0.708) 0.280–22.0 4.12 (1.59) 0.324–7.70 2.47 (0.549) 0.395–9.65 3.07 (0.930) 0.179–13.1 2.80 (1.19) 0.182–4.58 1.47 (0.438) 0.226–1.41 0.68 (0.140) 0.155–4.05 1.44 (0.740) 0.237–2.09 1.14 (0.312) 0.302–4.43 2.07 (0.781) 0.187–3.54 1.51 (0.740) 0.273–1.30 0.733 (0.300) NS 2.24

0.35–3.16 1.51 (0.313) 0.19–5.75 1.82 (0.365) 0.33–2.55 1.60 (0.270) 0.33–2.55 1.22 (0.239) 0.22–2.84 1.11 (0.280) 0.25–3.79 1.00 (0.384) 0.28–0.59 0.395 (0.0360) 0.30–0.87 0.535 (0.118) 0.34–0.76 0.545 (0.086) 19.2–70.5 0.873 (0.288) 0.32–6.66 2.24 (1.480) 0.33–0.64 0.508(0.0902) NS 20.6

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Cd (mg kg− 1 dw)

Vegetable type

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3.3. Effect of washing on trace metal concentrations in leafy vegetables Previous studies have examined the effect of washing leafy vegetables on trace metal concentrations, as this is often assumed to be normal practice during preparation for consumption (Qadir et al., 2000; Itanna, 2002; Mapanda et al., 2005; Huang et al., 2006). However, preparation of leafy vegetables grown in tropical cities such as Kampala often involves steaming freshly picked leaves without washing, maximising the risk of transferring superficial contaminants to the human diet (Nabulo, 2009). Trace metal concentrations in both washed and unwashed material varied between vegetable types (P b 0.05; Table 5). The highest recorded concentrations of individual elements expressed on an unwashed tissue dry weight basis were 1.69 mg Cd kg− 1 (C. olitorius), 9.98 mg Ni kg− 1 (V. unguiculata), 40.3 mg Cu kg− 1 (V. unguiculata), 829 mg Zn kg− 1 (A. dubius), 22.2 mg Pb kg− 1 (G. gynandra) and 22.0 mg Cr kg− 1 (C. maxima). Cadmium concentration was consistently lowest in C. maxima at nine study sites with contrasting sources and severity of contamination, strongly suggesting that this species has an unusual capacity to restrict Cd uptake from contaminated soil. This trait may indicate a useful role in improving the safety of food produced in urban and peri-urban agriculture. Fig. 4 shows trace metal concentration ratios (unwashed:washed values) for the edible shoots, averaged over all vegetable types and study sites. The results demonstrate that aerial deposition of Cr and Pb was substantially greater than for Cd, Ni, Zn and Cu, for which uptake must have occurred predominantly via systemic uptake by the roots and subsequent transport to the edible shoot component. The relatively high mean unwashed:washed ratio for Cu was perhaps caused by the elevated concentration of this element in unwashed material from Masese, for which the unwashed:washed ratio was 1.18 compared to 1.04 for all other sites and 1.03 for the Kilembe smelter site. The latter had the largest number of vegetable types present and the highest mean Cu concentration in washed vegetables (18.2 mg kg− 1) relative to the mean for all other sites (10.8 mg kg− 1). The high unwashed: washed ratio at Masese was attributed to contamination of the edible shoot by soil splash and immersion during flooding of the wetland. Fig. 5 shows the contrasting importance of superficial leaf contamination for the two main contaminants of concern (Pb and Cd) for all 10 vegetable types (Fig. 5a, b) or eight study sites (Fig. 5c, d). For Cd, there was no significant difference in concentration between washed and unwashed shoots (Figs. 4, 5b and d), confirming that uptake from the soil by roots was the main source of Cd in the shoots. Almost all

samples were below the FAO/WHO recommended limit of 0.2 mg Cd kg− 1 fw (Fig. 5b). By contrast, there was substantial deviation from the 1:1 line for Pb (P b 0.05) and clear evidence of a major contribution from aerial sources at concentrations N0.5 mg kg− 1 fw (Fig. 5a, c). The differences between washed and unwashed tissue were greatest at the Lugogo, Kinawataka and Radio sites (Fig. 5c). Lead concentration in unwashed vegetables spanned a wider range in A. dubius, C. maxima and C. esculenta than in the other vegetables examined (Fig. 5a). The worst combinations of vegetable type and site were A. dubius and C. maxima grown at Lugogo and Kinawataka, both former solid waste disposal sites; Lugogo is situated beside a major highway, while Kinawataka has a wastewater channel and car-washing facility. The unwashed:washed ratio for tissue Pb concentration reached a maximum of 9.1 for C. maxima at Lugogo, suggesting that deposition on leaves contributed c. 90% of the Pb present in the edible shoots of unwashed leafy vegetables. Of the 85 vegetable samples analysed, 34% of the unwashed samples had Pb concentrations exceeding the recommended maximum of 0.3 mg kg− 1 fw for leafy vegetables (FAO/WHO-CAC, 2001; EC, 2001; Fig. 5a). Of the unwashed samples which exceeded WHO limits, washing reduced Pb concentration to below the maximum permitted value for 69% of samples and, on average, reduced Pb concentration by 35% relative to unwashed material. This finding clearly demonstrates the benefit of washing leafy vegetables with clean water prior to preparation and consumption. A previous study by Marshall et al. (2003) showed that 72% of Palak leaf samples grown in Delhi, India had a Pb concentration exceeding the permissible limit for Pb of 2.50 mg kg− 1 fw (Indian Prevention of Food Adulteration Act (PFA, 1954) and all samples exceeded the more stringent CODEX limit of 0.30 mg kg− 1 fw. Moreover, at least 50% of the Pb was present on the surface of the vegetables, and washing these twice in clean water reduced contamination to within PFA safe limits (Marshall et al., 2003; Sharma et al., 2007). The relationship between Cr concentrations in unwashed and washed leafy material was similar to that for Pb, as washing removed a substantial proportion at high concentrations (Figs. 4, 6e) and reduced Cr concentration by 21% overall. Differences in Cr concentration between unwashed and washed shoot tissue were greatest for S. aethiopicum grown at Kilembe, C. maxima at Masese and V. unguiculata at Kinawataka. Variation between vegetable types in the extent of surface contamination due to aerial deposition may reflect differences in leaf characteristics; for example, the rough leaves of C. maxima and the presence of hairs may cause increased retention of particulate pollutants from aerial sources. Accumulation of Pb and Cr by leafy vegetables resulting from aerial deposition has been reported previously (Voutsa et al., 1996; De Nicola et al., 2008). By contrast, all vegetable types demonstrated mainly systemic control of Ni, Cu, Zn and Ba concentrations in their shoots, with no evidence of extraneous sources even when metal concentrations in unwashed shoots were high (Fig. 6a–d).

3.4. Assessing risk from consumption of vegetables

Fig. 4. Mean ratios of shoot metal concentrations (unwashed:washed) for all vegetable types and sites. Vertical bars associated with each histogram show double standard errors of the mean (n = 3).

The risk to human health arising from consumption of leafy vegetables grown on contaminated land was initially expressed as metal-specific hazard quotients (HQM) for each vegetable type (Eq. (1)) averaged over all study sites. The summation of HQM values based on tissue metal concentrations was invariably greater for unwashed than for washed leafy vegetables (Fig. 7), demonstrating the substantial benefit of this process in reducing risk to human health. Combined HQM values are sometimes described as ‘Hazard Indices’, although their application is controversial as their value and significance depend on the number of contaminants involved and the extent to which toxic responses are truly additive (Hough et al., 2004). Washing reduced mean summed HQM values for 12 leafy vegetables by 0.25 for the five metals included in the assessment.

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Values of HQM for individual elements were generally greatest for Cd, followed sequentially by Zn, Pb, Ni and Cu (Fig. 7), although the values for Pb occasionally exceeded those for Cd when the latter were unusually low, for example, in V. unguiculata and C. maxima. The large combined HQM values for unwashed S. aethiopicum and A. dubius were respectively primarily attributable to their high concentrations of Cd and Pb, whereas V. unguiculata and C. maxima had the lowest HQM values for Cd in both unwashed and washed tissue. Zinc is an essential element in the human diet but is hazardous at elevated concentrations. Its Reference Dose (RfD) is 0.3 mg Zn kg− 1 d− 1 (IRIS, 2000), giving a maximum safe intake of 16.7 mg d− 1 based on an average adult body weight of 55.7 kg. The recommended dietary allowance (RDA) for Zn is 11 mg d− 1 for adult males and 8 mg d− 1 for adult females who are not pregnant or lactating (IOM, 2001). The gap

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between the RDA and RfD for Zn is therefore relatively small. Thus, although enrichment of urban vegetables with Zn might be regarded as beneficial, the surprisingly high HQZn values shown in Fig. 7 suggest this may not always be the case, although the highest recorded HQZn value of 0.54 in A. dubius was well below the value of 1 regarded as potentially posing a risk. Values for HQM were much greater for children than for adults (Fig. 7), suggesting that the former may be more vulnerable to trace metal exposure. However, this conclusion is based on the assumption that children have a greater daily intake of vegetables relative to their body weight than adults (GEMS, 2000); young children may therefore be highly exposed to environmental hazards. Ryan and Chaney (1995) postulated that assessments of potential risk to the health of children as a vulnerable group may be useful in predicting risks for highly

Fig. 5. Relationship between Pb and Cd concentrations in washed and unwashed leafy vegetables grouped by vegetable type (a, b) or site (c, d). Solid lines with arrow-head tips show maximum recommended Pb (Fig. 5a) and Cd (Fig. 5b) concentrations (FAO/WHO-CAC, 2001; EC, 2001).

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exposed sub-populations on the basis that, if the worst-case scenario is acceptable, the majority of the population will be protected. Mean HQM values for all vegetable types grown at individual sites showed that Kilembe produced the highest combined hazard for children (Fig. 8a), whereas the corresponding value for Lugogo did not fully reflect its elevated soil concentrations for most trace elements. Similarly, the greatest HQCd values were at Murchison Bay, which was unexpected in view of its relatively low soil Cd concentration (Fig. 2). In addition to differences in soil metal availability between sites, these

apparent disparities may result from variation in the vegetable types grown at each site. Thus, the total HQM value for Lugogo was based on only three vegetable types, A. dubius, A. hybridus and B. oleraceae Acephala, whereas the corresponding value for Kilembe was based on nine vegetable types. This emphasises the need for site-specific risk assessments using HQM values based on individual vegetables to protect consumers who rely on local sources and may have restricted preferences for specific vegetable types. The HQM values for individual vegetables grown at Kilembe (Fig. 8b) clearly show that the dietary

Fig. 6. Relationship between (a) Ni, (b) Cu, (c) Zn, (d) Ba and (e) Cr concentrations in washed and unwashed leafy vegetables grouped by vegetable type.

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choices of consumers choosing from vegetable types grown on specific contaminated sites may pose remarkably different risks to human health. For Cd, the contrast in HQCd between S. aethiopicum (HQCd = 2.32) and V. unguiculata (HQCd = 0.145) or C. maxima (HQCd = 0.099) is particularly striking and demonstrates the potential value of the latter vegetable types in providing safe strategies for cultivation of contaminated urban soils. 4. Conclusions The present study suggests that HQM values depend on site-specific factors including source of contamination, trace metal loading, vegetable type, and whether the harvested material is washed prior to consumption. Broad-based risk assessments based on metal concentrations for generic classes of vegetables and applied to large urban areas may conceal substantial variation between specific vegetable types and locations. Site-specific assessments are therefore necessary for each vegetable type to determine the potential risk associated with consuming locally grown leafy vegetables. This is clearly shown by the risk assessment for Kilembe (Fig. 8b), where the marked dependence of HQM values on vegetable type not only highlights potential dangers, but also suggests possible management solutions. Thus, a policy of

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promoting cultivation of selected vegetables, such as C. maxima and V. unguiculata, could enable agriculture in contaminated locations. Washing leafy vegetables prior to consumption is also recommended to reduce HQM values for Pb and Cr. If there is a risk of contamination from dust or soil splash, washing could be augmented by mulching vegetable gardens located on contaminated soil to reduce loading of exogenous trace contaminants on leaves. Leafy vegetables grown on urban soils may provide a suitable dietary source of Zn if they can restrict the uptake of other potentially hazardous elements. Although it may be tempting for urban authorities to regard urban cultivation as an unsafe practice which should be discouraged, local demand for food and income in developing cities may make this policy untenable. Thus, realistic solutions, based on local risk assessment, are required, rather than attempting to enforce a complete ban on urban agriculture.

Acknowledgements Grace Nabulo thanks Makerere University, Uganda, for study leave to carry out the work reported here, the Commonwealth Scholarship Commission for funding, and Sonoko Mitsui-Angwin for expert assistance in preparing the figures.

Fig. 7. Mean hazard quotients (HQM) for 12 leafy vegetables averaged over all study sites showing the contribution for each element for (a) children and (b) adults. U and W denote unwashed and washed edible leafy material.

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Fig. 8. (a) Mean hazard quotients (HQM) for children of all vegetable types present at specific sites showing the contribution for individual elements; (b) HQM values for individual vegetable types at Kilembe, representing the worst-case scenario in terms of risk to human health. U and W denote unwashed and washed leafy vegetable material.

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