Uptake of Heavy Metals by Vegetables Irrigated Using Wastewater and The Subsequent Risks in Harare, Zimbabwe
Uptake of Heavy Metals by Vegetables Irrigated Using Wastewater and The Subsequent Risks in Harare, Zimbabwe
Uptake of Heavy Metals by Vegetables Irrigated Using Wastewater and The Subsequent Risks in Harare, Zimbabwe
Abstract
Contamination of leafy vegetables (Brassica species) with copper (Cu), zinc (Zn), cadmium
(Cd), nickel (Ni), lead (Pb) and chromium (Cr), and the subsequent human exposure risks, were
determined at two sites in the City of Harare, where wastewater is used for irrigating vegetables.
The concentrations of heavy metals (mg kg-1 dry weight) in vegetable leaves ranged from 1.0-3.4
for Cu, 18-201 for Zn, 0.7-2.4 for Cd, 2.5-6.3 for Ni, 0.7-5.4 for Pb and 1.5-6.6 for Cr. Bio-
concentration factors in the range of 0.04-3 were obtained, with Zn and Cd having the highest
concentration factors of 1.6 and 3, respectively. ERstimated intakes rates of heavy metals from
consumption of the vegetables in mg day-1 ranged from 0.04-0.05 for Cu, 0.6-3.3 for Zn, 0.02-
0.04 for Cd, 0.05-0.1 for Ni, 0.05-0.09 for Pb and 0.05-0.1 for Cr. Cadmium intake rates were
above their recommended Minimum Risk Levels (MRLs) at both sites, while Cu, Ni, Cr and Pb
had daily intakes above 40 % of their MRLs. Potential health risks, particularly from Cd intake,
existed for the daily consumers of the leafy vegetables at both Mukuvisi and Pension sites. Thus,
although the practice of growing leafy vegetables using wastewater for irrigation is aimed at
producing socio-economic benefits, it is not safe and may not be sustainable in the long-term.
There is need for an improved food quality assurance system to ensure that the vegetables
1
Key words: contamination, heavy metals, soil, vegetables wastewater
1. Introduction
Consumers’ demand for better quality vegetables is increasing. The perceptions of what is
regarded as ‘better quality’ are however subjective. Some consumers consider undamaged, dark
green and big leaves as characteristics of good quality leafy vegetables. However, the external
morphology of vegetables cannot guarantee safety from contamination. Heavy metals ranks high
amongst the chief contaminants of leafy vegetables. In Zimbabwe, land disposal of sewage and
industrial effluents has been implicated as the chief source of heavy metal enrichment of
pasturelands and agricultural fields, particularly near Sewage Treatment Works in urban areas
(Mangwayana, 1995; Nyamangara and Mzezewa, 1999; Mapanda et al., 2005). The production
of leafy vegetables (Brassicas) using wastewater for irrigation is practiced in the City of Harare,
but little is known on the contamination of these vegetables with heavy metals. Studies
conducted by Kisku et al. (2000) in Kalipur, Bangladesh, on the uptake of Cu, Pb, Ni and Cd by
Brassica oleracea from fields irrigated with industrial effluent indicated widespread
contamination from heavy metals despite showing a healthy and gigantic external morphology.
The use of wastewater for agricultural purposes in Zimbabwe is recommended for surface
irrigation of grain crops, crops grown for industrial processing and pastures for slaughter stock
provided that certain standard are met. However, it is prohibited for the irrigation of leafy
vegetable crops (NRB, 1974). Informal surveys have indicated that in Harare alone, there are
more than 100 hectares of land under horticultural production that utilize wastewater for
irrigating crops, such as maize (Zea mays) and leafy vegetables (Brassica spp.). Wastewater use
occurs either indirectly, when partially treated and untreated effluents are discharged into rivers
such as Mukuvisi that supply water for horticulture along riverbanks, or directly, at municipal
farms such as Pension where partially treated sewage effluent is diverted into vegetable gardens
2
Leafy vegetables have greater potential of accumulating heavy metals in their edible parts than
grain or fruit crops. Studies on the uptake of heavy metals by plants have shown that heavy
metals can be transported passively from roots to shoots through the xylem vessels (Kirkham,
1977; Krijger et al., 1999). In addition, plant organs such as fruit and seed that have low
transpiration rates (e.g. fruits and seeds) did not accumulate heavy metals because the storage
organs are largely phloem-loaded and heavy metals are generally poorly mobile in the phloem.
Zheljazkov and Neilsen (1996) found that the concentrations of heavy metals in vegetables per
unit dry matter generally follow the order: leaves >fresh fruits >seeds.
Contamination of the human food chains by heavy metals is not directly affected by the plants’
total uptake, but rather by the concentration in those parts that are directly consumed (Bieleski
and Launchli, 1983). Thus, in assessing exposure risks, heavy metal contents in roots and stems
of Brassicas are of less importance than those in the edible leaves. According to Alloway and
Ayres (1993) and Lee et al. (1996), sensitivity of organisms to heavy metal toxicity depends on
heavy metal accumulation rate in plants, intake rate (in animals) and age of the consuming
organism amongst other factors. The Consumer Council of Zimbabwe’s total dietary study
estimated a leafy vegetable consumption rate for low-income urban dwellers to be 66.7-79.8 kg
The main objectives of this study were to determine the concentrations of Cu, Zn, Cd, Ni, Cr and
Pb in Brassica juncea and B. napus leaves from gardens irrigated with wastewater from the
Mukuvisi River and partially treated sewage effluent at Pension farm in Harare, and to estimate
their intake rates by people consuming the vegetables. Results showing the long-term effects on
soils irrigated with wastewater at these sites were reported elsewhere (Mapanda et al., 2005).
3
Mapanda et al. (2005) reported elevated concentrations of Cu, Zn, Cd, Ni, Cr and Pb in the
topsoil of sites irrigated with wastewater compared with the control soils and subsoil.
Two vegetable production sites, Mukuvisi and Pension, were selected from Harare (Figure 1)
where various pollution problems as well as some significant commercial horticultural activities
have been reported (Mapanda et al., 2005). Harare experiences cold-dry winters and hot-wet
summers (sub-tropical) with an average annual rainfall of about 850 mm. Average annual
temperature ranges between 18-20 °C. The Mukuvisi site extends from 30° 58' E to 31° 03' E and
lies between 17° 54' S and 17° 57' S, while the Pension site is located on Pension Farm extending
from 30°52' E and 30°55' E and lying between 17°52' S to 17°55' S. The Mukuvisi site is located
along the riverbanks and irrigated with wastewater from the Mukuvisi River. Sources of
contamination of the Mukuvisi River wastewater include industrial discharges from Masasa and
Graniteside industrial areas, waste dumpsites along the riverbanks and sewage effluent partially
discharged from Firle Sewage Treatment Works (FSTWs) (Zaranyika et al., 1993). The Pension
site is located near FSTWs and has been under irrigation using a mixture of partially treated
Vegetable gardens at the Mukuvisi site are scattered along the riverbanks on undulating terrains
of up to about 8 % slope while those at the Pension site are found in clusters on gently
undulating terrains of about 2-5 % slope. The volumes of wastewater used for irrigating
vegetables at the Mukuvisi site ranged from 6-29 ML ha-1 year-1 (average, 16 ML ha-1 year-1),
while the volumes of irrigation wastewater at the Pension site ranged from 24-36 ML ha-1 year-1
practiced along riverbanks by households from the surrounding high-density areas of Glen Norah
4
and Highfields, on areas ranging from about 200 m2 to >10 000 m2. Vegetable gardens at Pension
are irrigated using flood-beds and cultivated by over 50 households, each with a holding area
The underlying geology at the area surrounding the Mukuvisi River and Pension Farm is coarse-
grained granite (Baldock, 1991). Textures of the studied soils ranged from sands to sandy loams
(Arenosols). Soils at the Mukuvisi site had low cation exchange capacities (7.0-10.4 cmol (+) kg-
1
) and low to medium organic carbon (0.98-1.2 %) in the 0-10 cm depths, while soils at the
(+)
Pension site also had low cation exchange capacities (5.0-6.4 cmol kg-1) and medium organic
Soil and vegetable leaf samples were collected from the gardens irrigated with wastewater at the
Mukuvisi and Pension sites. A composite soil sample (about 1 kg) made up of five sub-samples
was collected with a bucket-auger from each garden under vegetables. The sub-samples were
collected along independent zigzag paths to achieve randomness. The samples were collected in
the 0-20 cm depths at Pension and in the 0-10 cm depths at Mukuvisi because of the shallower
effective depths. The soil samples (three from the Mukuvisi site and seven from the Pension
site) were collected in duplicates from the gardens where the leafy vegetables were currently
growing.
Vegetable leaf samples were collected by randomly picking up two or three mature bottom
leaves from the plants until a bundle of about 15-20 cm diameter was gathered from each garden.
The vegetable bundles (three from the Mukuvisi site and seven from the Pension site) were
collected for both Brassica juncea (6) and B. napus (4) and washed once with distilled water by
running the water through the leaves to mimic the general practice of unsuspecting consumers.
5
Each bundle was sub-divided in the laboratory to give triplicate samples weighing approximately
200 g (fresh weight). The fresh vegetable samples were dried in an oven at 70 °C for three days,
reweighed and ground to pass though a 1 mm mesh sieve (Campbell and Plank, 1992) prior to
Soil pH was measured with a digital pH meter (Model: Philips W409) using the water method
(McNeal, 1982). The soil samples were digested for heavy metal analysis using the aqua regia
(mixture of concentrated hydrochloric (HCl) and nitric acids (HNO3) in the HCl: HNO3 ratio of
3:1) digestion method (Baker and Amacher, 1982) and refluxed. The digested mixture was
centrifuged at 1 500 rpm and the supernatant analysed for Cu, Zn Cr, Cd, Ni and Pb by atomic
absorption spectrophotometry.
About 2 g of oven-dried and ground leaf samples were accurately weighed into small crucibles
and ashed in a muffle furnace (Model: Wildbarfield M1354) housed in a fume hood. The
samples were ashed at 450 °C for 24 hours to a whitish-to-grey ash (Hanlon, 1992). The
crucibles were cooled in a desiccator and 5 ml of aqua regia were added to the residual ash. The
mixture was covered with watch glasses and digested on a homogenising hot plate (Model:
Philips 492-11) at 105 °C and 50 cycles per minute for 30 minutes. Evaporation was
compensated during digestion by drop-wise replenishment with distilled water. Three drops of 2
M HNO3 were added to the digestants before they were transferred to 50 ml volumetric flasks.
The crucibles were washed once with distilled water and the mixture topped up with 2 M HNO3.
Genstat statistical package, version 4.1 (Lawes Agriculture Trust, Rothamsted Experiment
The Daily Intake (DI) rates of heavy metals were estimated from the average concentrations
(fresh wt., derived at 91 % moisture) of heavy metals in vegetable leaves and the vegetable
6
consumption rate of 0.18-0.22 kg fresh wt. day-1 estimated from a Total Diet Study (Vhurumuku,
2000).
3. Results
The total concentrations of heavy metals in the soils from which vegetables were sampled at the
Mukuvisi and Pension sites were below the maximum permissible limits (MAFF, 1993). Soil pH
(in water) was higher in Mukuvisi gardens (6.1-7.8) than in Pension gardens (5.1-6.3), while the
concentrations of all heavy metals tested were lower at the Mukuvisi site than at the Pension site
(Table 1).
The total concentration of selected heavy metals in leaves of B. juncea and B. napus from
selected gardens at both studied sites are shown in Table 2. Concentrations of Cu in plant tissues
(dry wt.) averaged 2.4 mg kg-1 at Mukuvisi and 2.3 mg kg-1 at Pension. No significant
differences (P >0.05) in plant Cu were found between the sites, while all samples’ Cu
concentrations were below the permissible limit of 200 mg kg-1 dry wt. (Food Standards
Committee, 1950). Zinc concentrations in the vegetable leaves averaged 36 mg kg-1 at the
Mukuvisi site and 164 mg kg-1 at the Pension site. The concentrations of Zn in leaf tissues were
significantly (P <0.05) higher at the Pension site than at Mukuvisi. However, the concentrations
of Zn in all samples were below the permissible limit of 500 mg kg-1 dry wt. (Food Standards
Committee, 1950).
Cadmium concentrations in leaf tissues of the vegetables averaged 2.0 mg kg-1 at the Mukuvisi
site and 1.1 mg kg-1 at the Pension site. Significant differences (P <0.05) in plant Cd
concentrations were found between the sites and higher concentrations were found at Mukuvisi
7
than at Pension. The concentrations of Cd in plant tissues exceeded the permissible limit of 2 mg
kg-1 (Codex Alimentarius, 2001a) in 67 % of the vegetables from the Mukuvisi site. The
concentration of Ni in the vegetables averaged 3.1 mg kg-1 at the Mukuvisi site and, 4.9 mg kg-1
at the Pension site. Significant differences (P <0.05) in Ni concentrations were found between
the sites and higher concentrations were found at the Pension site than at Mukuvisi. However, all
Ni concentrations were below the tolerable limit of 680 mg kg-1 dry wt. (Weigert, 1991).
Lead concentrations in leaf tissues averaged 2.5 mg kg-1 at the Mukuvisi site and 4.0 mg kg-1 at
the Pension site, and were significantly (P <0.05) higher at the Pension site than at the Mukuvisi
site. The Pb concentrations in Pension and Mukuvisi vegetables exceeded their permissible limit
the leaf tissues averaged 5.1 mg kg-1 at the Mukuvisi site and 2.9 mg kg-1 at the Pension site.
Significant differences (P <0.05) in Cr concentrations were found between the sites and higher
concentrations were found at the Mukuvisi site than at the Pension site. However, Cr
concentrations at both sites did not exceed the tolerable limit of 23 mg kg-1 (Weigert, 1991).
The mean bio-concentration factors (CFs) of the selected heavy metals at the Pension and
Mukuvisi sites, calculated as the concentration of the heavy metals in leaves relative to
concentration in soil, ranged from 0.04-3 depending on the element (Table 3). The order was:
CFCd >CFZn >CFNi >CFPb >CFCu>CFCr at Mukuvisi and CFZn >CFCd = CFNi >CFPb >CFCu >CFCr at
Pension. The proportions of studied heavy metal in vegetable leaves, expressed as a percentage
fraction of their added total concentration in the leaves were in the order: Zn >Cr >Ni >Cu >Cd
>Pb for vegetables at the Mukuvisi site and Zn >Ni = Pb >Cu = Cr >Cd for vegetables at the
Pension site. Zinc made the highest fractions of 48-75 % (Mukuvisi) and 88-92 % (Pension).
8
The heavy metals daily intakes of by consumers of the vegetables, estimated from the average
concentrations of heavy metals in leaves and the vegetable consumption rate (183-219 g person-1
day-1), were below the Minimum Risk Levels (MRLs) for all studied heavy metals, except Cd.
All Cd intake rates were above the MRL of 0.012 mg Cd day-1, and the highest Cd intake rate
4. Discussion
concentrations of Cu and Zn in the vegetable leaves at both Pension and Mukuvisi sites. The
concentrations of Cu in the leaves were all below the toxic range of 20-100 mg Cu kg-1 dry wt.
(Ross and Kaye, 1994). Studies by Berry and Wallace (1989) indicated that Zn phytotoxicity in
most leafy vegetables (expressed by reduced growth) occurs when Zn accumulates to an average
tissue concentration of 500 mg kg-1 dry wt, more than twice the concentration of Zn found in the
Although the total concentrations of Cu in soils at the Pension site were more than twice the
concentrations found in soils at the Mukuvisi site, the uptake of Cu by vegetables at the two sites
were comparable. This was also confirmed by the mean Cu bio-concentration factor of 0.13 at
the Mukuvisi site and 0.05 at the Pension site, indicating higher Cu uptake efficiency at the
Mukuvisi sites. This could be attributed to higher soil organic matter content in the gardens at the
Pension site than in soils at the Mukuvisi site, despite the generally lower pH of the soils at
Pension. Gardens at the Pension site are irrigated with treated effluent mixed with digested
sludge, which contains a lot of organic matter (Nyamangara and Mzezewa, 1999), while gardens
at Mukuvisi site are irrigated with river water that is mainly contaminated by inorganic effluent
from industries like fertilizer companies (Zaranyika, 1996). Studies by Sauve et al. (2000) on the
uptake of heavy metals by plants from contaminated soil indicated that of all the studied heavy
9
metals Cu2+ had the strongest affinity for organic matter and was easily complexed, reducing its
The estimated intake rates of Cu and Zn suggested that the contribution of leafy vegetables to the
intake of these heavy metals is low and does not pose potential health risk to consumers of
vegetables. No adverse, non-cancerous health effects are thus expected from Cu and Zn intake
from the leafy vegetables unless other additional and richer sources of these heavy metals in the
The concentrations of Cd in vegetable leaves at the Mukuvisi site were above the FAO/WHO
recommended limit (<2 mg Cd kg-1, dry wt.), indicating that exposure to Cd may be high. Higher
Cd concentrations in vegetable leaves were found at the Mukuvisi site than at the Pension site,
despite the generally higher Cd concentrations in the soil at the Pension site. This could also be
attributed to higher organic matter at the Pension site than at the Mukuvisi site as was recorded
for Cu. Brown et al. (1998) studied Cd uptake in sludge-amended and Cd-salt treated soils
maintained at high and low soil pH. They found that Cd uptake by plants grown in sludge
amended soils was significantly lower than Cd uptake by plants grown in the Cd-salt treated soils
at low and high pH. Similarly, the availability of Cd at the Pension site would be lower since the
treated effluent applied is sometimes mixed with digested sludge (with higher organic matter).
This increases soil organic matter in the gardens, unlike at the Mukuvisi site where most Cd in
river water may be in the inorganic form originating from acid-battery factories and surrounding
industries that discharge their partially treated effluent into the Mukuvisi River (Zaranyika et al.,
1993).
The result of the study showed a 25 % prevalence of Pb in vegetables from both sites exceeding
the FAO/WHO recommended limits (<3 mg Pb kg-1, dry wt.). This is an indication of a high
10
potential risk of Pb exposure at both Pension and Mukuvisi sites. Lead is a non-essential element
for plants and animals, and should be available to plants in low quantities (Alloway and Ayres,
1993). The mean Pb bio-concentration factors were comparable at the Mukuvisi and Pension
sites despite the lower pH values found in the gardens at the Pension site. The relatively high
plant Pb found at the Mukuvisi site could be attributed to dry deposition from industrial and
vehicle fumes. According to Wild (1993), most Pb taken up by Brassica plants is retained in the
roots, but the greatest threat is Pb deposited on leaves because only half of the Pb is removed by
washing.
Typical daily intakes of Pb by adults range from 0.015-0.1 mg day-1, depending on the
composition of the diet and where the consumer lives (Codex, 1995). Lead intakes from leafy
vegetables at the Pension and Mukuvisi sites were 34-79 % of the upper limit of this typical Pb
intake rate. Thus, the vegetables at the sites under this study could be contributing significantly
to Pb intake. Children are more susceptible to adverse effects of Pb because they eat more food
relative to their body mass than adults. They absorb Pb more readily than adults and their major
organs, including the brain, are still under developed (Carrington and Bolger, 1992), making
Nickel is found in small quantities in many foodstuffs (0.001-0.01 mg kg-1, fresh wt.), but in
higher concentrations in foodstuffs such as grain, nuts, and seeds (up to 0.8 mg kg-1, fresh wt.)
(National Food Agency of Denmark, 1995). Weigert (1991) indicated that Ni concentrations of
up to 68 mg kg-1, fresh wt. may still be safe for consumption since more than 90 % of Ni taken in
is held in the organic form that can be safely excreted. Thus the risk of exposure to Ni at the
11
Chromium concentrations in vegetables from the Pension and Mukuvisi sites were generally low
and the daily intakes of Cr from leafy vegetable were about 50 % of the estimated typical daily
intake rates of 0.025-0.2 mg day-1 (Codex, 1995). Thus, approximately 50 % of daily Cr intake
from foodstuffs could come from the leafy vegetables grown at the study sites.
5. Conclusion
Based on the results of this study, leafy vegetables grown at the Pension and Mukuvisi sites
where wastewater is used for irrigating the vegetables were contaminated Cu, Zn, Cd, Ni, and
Pb. Potential public health hazards, especially from Cd, are high at the sites. It is possible that
other sites receiving wastewater for irrigation in Harare have similarly been affected. Although
the practice is aimed at producing socio-economic benefits it is not safe and may not be
sustainable in the long-term. There is need for an improved food quality assurance system and
promotion of the production of vegetables that comply with existing standards on heavy metal
concentrations.
Acknowledgements
This study was sponsored through a grant from the Department For International Development
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N
NW Highlands N
Avondale
Avonlea Borrowdale
Mabelreign Hatcliff
Vainona
W Tynwald
Dzivarasekwa Mt. Pleasant
W. Park
Marlborough
E
Rugare, Kuwadzana,
Crowborough CENTRAL
DISTRICT Eastlea CLEVELAND DAM
(CITY CENTER) Cranboughn
Eastern Highlands
WSW Mufakose
SE Mandara
Budiriro Masasa
Glen view SW Mabvuku
Mukuvisi River
Highfields
Glen Norah
34
S
Mbare
Chadcombe, Hillside
Sunningdale, Hatfield
Masasa Park
4
(to lake Chivero) Uplands
Pension Site
Mukuvisi Sites (Plots 4 and 34)
4
Waterfalls
Figure 1. The City of Harare’s nine administrative Districts showing residential and industrial
areas found in Harare and the Mukuvisi River. The Pension Farm is located near Firle Sewage
Treatment Works, while the Mukuvisi sites are along the riverbanks of the Mukuvisi River.
15
Table 1. Mean concentrations of heavy metals in mg kg-1 dry weight in the topsoil of the gardens from which vegetable leaves were sampled at the
Mukuvisi and Pension sites in Harare. The number in brackets are standard errors.
16
Table 2. Mean concentrations of selected heavy metals in vegetable leaves (mg kg-1 dry wt.) from selected gardens at the Mukuvisi and Pension sites,
and their maximum permissible limits (mg kg-1 dry weight, derived from fresh weight at 91 % moisture).
#
Food Standard Committee (1950) Guidelines (UK); ‡FAO/WHO (Codex Alimentarius Commission, 2001a,b); ‡‡Weigert, 1991
17
Table 3. The concentrations of tested heavy metals in leaves of Brassica juncea and B. napus
relative to their concentrations in soil (bio-concentration factors, CFs) at the Mukuvisi and
Pension sites in Harare.
Site Garden No. Species CFCu CFZn CFCd CFNi CFPb CFCr
4a B. napus 0.16 0.7 4.6 0.5 0.4 0.07
Mukuvisi 34 B. napus 0.06 0.7 1.7 0.6 0.03 0.07
4b B. juncea 0.18 1.2 2.7 0.4 0.4 0.10
Mean CF value 0.13 0.9 3.0 0.5 0.3 0.08
1 B. napus 0.03 0.8 0.3 0.3 0.1 0.01
2 B. napus 0.02 1.2 0.4 0.4 0.2 0.04
3 B. juncea 0.03 0.8 0.5 0.2 0.1 0.02
Pension 4 B. juncea 0.06 1.3 0.2 0.5 0.1 0.02
5 B. juncea 0.08 2.3 0.6 0.4 0.2 0.04
6 B. juncea 0.08 1.8 0.5 0.4 0.2 0.05
7 B. juncea 0.08 2.6 0.6 0.5 0.2 0.09
Mean CF value 0.05 1.6 0.4 0.4 0.2 0.04
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Table 4. Mean concentrations of heavy metals in vegetables (fresh wt.) and the heavy metals
intake rates by an adult (of 60 kg body wt.) from the Mukuvisi and Pension sites relative to
the Minimum Risk Levels (MRLs).
†
Average content in leaves Intake rate MRL
Metal
(mg kg-1, fresh wt.) (mg day-1) (mg day-1)
Mukuvisi Pension Mukuvisi Pension
†
Minimal Risk Levels (developed by the Agency for Toxic Substances and Disease Registry (ATSDR) and the
United States Environmental Protection Agency (USEPA) are intake rates below which adverse, non-cancerous
health effects are not likely to occur (for Cu, Zn and Cd) (ATSDR, 1999), or daily human exposure for a
lifetime below which non-cancer and other adverse health effects are unlikely to occur (for Ni, Cr and Pb)
(ATSDR, 2003).
19