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Human and Ecological Risk Assessment: An International Journal

ISSN: 1080-7039 (Print) 1549-7860 (Online) Journal homepage: http://www.tandfonline.com/loi/bher20

Bioaccumulation of heavy metals in local edible plants near a municipal landfill and the related human health risk assessment Patcharin Ruchuwararak, Somsak Intamat, Bundit Tengjaroenkul & Lamyai Neeratanaphan To cite this article: Patcharin Ruchuwararak, Somsak Intamat, Bundit Tengjaroenkul & Lamyai Neeratanaphan (2018): Bioaccumulation of heavy metals in local edible plants near a municipal landfill and the related human health risk assessment, Human and Ecological Risk Assessment: An International Journal, DOI: 10.1080/10807039.2018.1473755 To link to this article: https://doi.org/10.1080/10807039.2018.1473755

Published online: 23 May 2018.

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HUMAN AND ECOLOGICAL RISK ASSESSMENT https://doi.org/10.1080/10807039.2018.1473755

Bioaccumulation of heavy metals in local edible plants near a municipal landfill and the related human health risk assessment Patcharin Ruchuwararaka,b,c, Somsak Intamata,d, Bundit Tengjaroenkula,e, and Lamyai Neeratanaphana,b a Research Center for Environmental and Hazardous Substance Management, Khon Kaen University, Khon Kaen, Thailand; bDepartment of Environmental Science, Faculty of Science, Khon Kaen University, Khon Kaen, Thailand; c Research for Social Development Institute, Khon Kaen University, Khon Kaen, Thailand; dThatphanom Crown Prince Hospital, Nakornphanom, Thailand; eDepartment of Veterinary Medicine, Faculty of Veterinary Medicine, Khon Kaen University, Khon Kaen, Thailand

ABSTRACT

ARTICLE HISTORY

The increase in municipal solid waste generation, along with high concentrations of heavy metals in environments near municipal landfill, has led to human health hazards. This study investigated heavy metal contamination in water, sediment, and edible plants near a municipal landfill, including the bioaccumulation factor (BAF) and potential health risks. The heavy metal concentrations in the samples were analyzed using inductively coupled plasma optical emission spectrometry (ICP-OES). The concentrations of arsenic (As), lead (Pb), cadmium (Cd), and chromium (Cr) in water samples were not detected (ND), ND, 0.006 § 0.01 mg/L, and ND, respectively, and in sediment samples, the concentrations were 1.19 § 0.44, 3.20 § 0.62, 0.46 § 0.21, and 6.97 § 0.34 mg/kg, respectively. The highest concentrations of As (5.03 § 0.38), Pb (1.81 § 0.37), and Cd (1.93 § 0.13) were found in Marsilea crenata, whereas that of Cr (5.68 § 0.79) was detected in Ipomoea aquatica. The Cr concentration in all plant species exceeded the standard for vegetables. The BAF values followed the heavy metal concentrations. All plant species have a low potential for accumulating Pb and Cr. The edible plants in this study area might cause health hazards to consumers from As, Pb, and Cd contamination.

Received 13 February 2018 Revised manuscript accepted 3 May 2018 KEYWORDS

bioaccumulation; municipal landfill; leachate; heavy metal

Introduction Municipal solid waste (MSW) is a crucial problem worldwide, especially waste generation in urban areas in lower middle-income countries, which are expected to generate the highest volume of urban waste, 956 million tons/year, in 2025 (Hoornweg and Bhada-Tata 2012). Thailand, one of the lower middle-income countries in Southeast Asia with a current population of 65 million, has a management and disposal problem for MSW (Chiemchaisri et al. 2007). The total MSW generated nationwide in 2016 amounted to 27.06 million tons or 74,130 tons/day. The amount of waste generated per person increased on average from 1.13 to 1.14 kg/day (PCD 2016). The five provinces CONTACT Lamyai Neeratanaphan Khon Kaen University 40002, Thailand. © 2018 Taylor & Francis Group, LLC

[email protected]

Department of Environmental Science, Faculty of Science,

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that generated the most MSW were Bangkok, Chon Buri, Nakhon Ratchasima, Samut Prakan, and Khon Kaen (PCD 2014). Additionally, there is an accumulation of old waste in municipal waste management facilities nationwide that had not been managed, totaling 9.96 million tons. Khon Kaen province generated one of the highest tonnages of solid waste per year (710,298.01 tonnes per year), and the accumulation of old MSW was 754,904 tons (PCD 2016). The high accumulation of old MSW dissipated the leachate through the layers of landfill to contaminate ground water, surface water, and sediment (Kanmani and Gandhimathi 2013). In addition, animals and plants with habitats adjacent to the municipal landfill were more likely to be exposed to leachate through both direct and indirect exposure. Landfill leachate is a complicated cocktail of heavy metals and a broad range of xenobiotic organic compounds (Kjeldsen et al. 2002). The heavy metals present in municipal landfills include chromium (Cr), cadmium (Cd), mercury (Hg), lead (Pb), and a metalloid, arsenic (As) (Earle et al. 1999; Jain et al. 2005; Promsid 2014; Phoonaploy et al. 2016). Previous studies observed high heavy metal concentrations in water, sediment, and aquatic animals and plants in this study site (Promsid 2014; Phoonaploy et al. 2016; Intamat et al. 2017; Sriuttha et al. 2017). Heavy metal accumulation in aquatic animals and plants, which have habitat near municipal landfills, is important since these organisms are regular food sources for local people. The main route to human beings is via oral exposure. High heavy metal exposure can cause adverse health effects in humans since it is associated with multisystem disease (Sin et al. 2001; Scheplyagina 2005; Nordberg et al. 2007; Khan et al. 2011; Varol and Sen 2012). Over 500 plant species are well known for their high potential to accumulate heavy metals. These plants have been used as hyperaccumulators for phytoremediation (Sarma 2011). However, plants high in heavy metals could cause serious health hazards in humans (Singh et al. 2011; Agil et al. 2017); the hyperaccumulation plants, especially edible plants near municipal landfill, might not be suitable for consumption. Different species of edible plants are grown throughout the year, but there is limited information on their heavy metal content (Alam et al. 2003). Thus, it is necessary to study the potential for accumulation in the different plants near a municipal landfill. Previous studies have reported heavy metal accumulation in four species of aquatic plants (Intamat et al. 2017; Sriuttha et al. 2017). While studies on more edible plant species, which local people regularly consume, are lacking. This study investigated heavy metal accumulation in the water, sediment, and local edible plants near a municipal landfill. Additionally, the bioaccumulation factor (BAF) and potential health risks, including the estimated daily intake (EDI), health risk index (HRI), and carcinogenic risk (CR), were investigated.

Methods and materials Study area The study site was the paddy field that was located near a municipal landfill in the Kambon village, Maung District, Khon Kaen province in Thailand (Figure 1). The distance from the paddy field to the landfill was 100 meters in the leachate direction. A municipal landfill was located approximately 2 km from the Chum Jarn community. In the landfill area, most of

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Figure 1. The municipal landfill located in Khon Kaen province, Thailand. The locations of the sampling collection sites are shown in the dashed area.

the untreated effluent flowed into a small drainage stream. The majority of the land around this area is used for agricultural crops, such as rice and sugarcane. Sample collection Nine water samples in the paddy field near the municipal landfill were collected with glass bottle samplers and directly acidified with nitric acid. The nine sediment samples were collected along the wetland in the paddy field. They were air-dried and crushed by hand with a porcelain mortar and pestle. Ten species of edible plant samples were randomly collected from the paddy field. The edible parts (stems and leaves) were cut into small pieces and oven dried at 80 C. The dried samples were crushed with a porcelain mortar and pestle. Sample preparation and analysis Each 25-mL water sample was digested with 1.25 mL of nitric acid and boiled in a water bath at 90 C for 30 min. The digested samples were then adjusted to 25 mL with deionized distilled water. The final solution was filtered through a cellulose filter paper. The 1-g dried sediment samples were digested with 5 mL of nitric acid, 15 mL of hydrogen chloride, and 10 mL of hydrogen peroxide and then boiled in a digestion block at 180– 220 C for 2 h. The digested samples were then adjusted to 50 mL with deionized distilled water. The final solution was filtered through a cellulose filter paper. The 0.5-g plant samples were digested with 5 mL of nitric acid and 3 mL of hydrogen peroxide and heated up on a hot plate at 120 C until the solution evaporated to near dryness. Then, the digested samples were adjusted with deionized water to 25 mL. The final solution was filtered through a cellulose filter paper (Chand and Prasad 2013). All of the solution samples were analyzed for 3 heavy metals and a metalloid, including Cd, Cr, Pb, and As, with inductively coupled plasma optical emission spectrometry (ICP-

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OES) (ICP: Perkin Elmer Optima 7000 DV). The limit of detection of ICP-OES was 0.001 mg/kg for Cd and Cr, 0.005 mg/kg for Pb, and 0.006 mg/kg for As. The ICP-OES wavelength analyses for Cd, Cr, Pb, and As were set to 226.502, 267.716, 220.353, and 188.979 nm, respectively. Quality control and quality assurance The blank reagents were measured at every tenth sample to detect contamination. The elemental concentrations of procedural blanks were generally As (1.19 § 0.44 mg/kg) >Cd (0.46 § 0.21 mg/kg). The heavy metal concentrations were lower than the soil quality standards for Thailand. The results of this study were lower than previous studies (Sriuttha et al. 2017; Intamat et al. 2017), which detected Cd (0.47 § 0.23 mg/kg), Cr (18.65 § 11.39 mg/kg), Pb (5.36 § 2.08 mg/kg), and As (1.08 § 0.64), respectively. These data may be explained by the study site. Fishery ponds, which were located near the municipal landfill, were selected as the study site in previous studies. However, the samples in this study were collected from a rice field. The rice plant has a high potential for phytoremediation of heavy metals in soil (Abedin et al. 2002; Du et al. 2005; Neeratanaphan et al. 2017). The heavy metal concentrations in the sediment samples were higher than in the water samples. Sediment is regarded as the major sink material for uptaking the heavy metals (Weber et al. 2013). The major

Figure 2. Health risk index (HRI) of As and Cd (A), and Pb and Cr (B) in plant samples.

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Figure 3. Carcinogenic risk (CR) of As and Pb in plant samples.

sources of heavy metals in landfills are co-disposed industrial waste, incineration ashes, and household hazardous materials such as batteries, paints, and dyes (Erses and Onay 2003). Solid wastes were the main sources that were found in the study site. This is in accordance with a previous study, which identified the type of solid waste in the study area as household hazardous waste from the Khon Kaen sanitary landfill that included light bulbs, chemical containers, and lubricators (Sarun 2004). The heavy metal contamination in sediment leads to the accumulation of heavy metals in aquatic plants, particularly marginal plants. Heavy metal concentrations in plant samples The Cr concentration in all species exceeded the FAO standard for vegetables. This result concurs with a previous study in the same area (Sriuttha et al. 2017), in that Cr concentrations exceeded the standard in four plant species. The highest concentrations of As, Pb, and Cd were detected in M. crenata. All heavy metal concentrations in M. crenata exceeded the standard. M. crenata grows in water and sediment; thus, it likely absorbs pollutants from both water and sediment. In addition, M. crenata has a high surface ratio to be exposed pollutants from the environment. The leaves and stems of M. crenata are part of the local cuisine. In the previous study, Marsilea sp. showed the highest As concentration (45 mg/kg) among 8 aquatic plants. Marsilea sp. might be available for As phytoremediation of paddy fields (Tripathi et al. 2012). The highest Cr concentrations were observed in I. aquatica. Accordingly, Gupta et al. (2008) determined that the Cr concentration was highest in I. aquatica > Marsilea sp. The results in this study clearly showed a trend of heavy metal concentration. Specifically, As concentrations were higher in aquatic plants (0.01–5.03 mg/kg) than in terrestrial plants (0.03–0.31 mg/kg). Similarly, the previous study of Tripathi et al. (2012) demonstrated that As concentration was higher in aquatic plant (5–60 mg/ kg) than in terrestrial plant species (4–19 mg/kg). Bioaccumulation factors of heavy metals in plant samples The BAF is more ecologically relevant because it accounts for environmental exposure. The BAF values >1 have been used to evaluate the potential of plant species for phytoextraction

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and phytostabilization of metals in soil (Li et al. 2007). This value is one of the two factors, the bioaccumulation factor (BAF) and translocation factor (TF), used to classify plants as hyperaccumulators (Sun et al. 2009). The results of this study indicated that different plants have different capacities to absorb heavy metals in soil. M. crenata has a high potential for absorbing all heavy metals, except for Pb and Cr. The results differ from Kumar et al. (2012) that noted M. minuta can be applied to remove Pb and Cr from contaminated water bodies. The potential to absorb toxicants may depend on different species. A previous study (Tripathi et al. 2012) showed the highest bioaccumulation coefficient (BC) of As in M. crenata (3.60), whereas a low level of BC was observed in C. asiatica (0.69). All plant species in this study area also showed low potential for absorbing Pb and Cr. However, L. spinosa, L. aromatic, C. asiatica, G. oppositifolius, and M. crenata demonstrated a high potential for absorbing Cd. Five plant species occurred in a habitat with sediment and low water levels, which indicated that the habitat was associated with Cd absorption. Cd hyperaccumulator plants in this study did not include I. aquatica, although several previous studies showed high accumulations of Cd in I. aquatica at 590 mg/kg (Theophile et al. 2005), 375–2,227 mg/kg in roots, and 45—144 mg/kg in shoots (Wang et al. 2008). Hyperaccumulator plants should be used as phytoremediators, but all plant species in this study were edible plants that people consumed. Thus, these plants might cause health problems in humans (Singh et al. 2011; Agil et al. 2017). Potential health risks of heavy metals via plant consumption EDI, HRI, and CR were the parameters used to assess human health risks from the consumption of food contaminated with heavy metals. HRI showed noncarcinogenic health risks, whereas CR showed carcinogenic health risks. The EDI values of heavy metals in this study were high and trended with HRI values. The HRI values in the majority of plant samples were higher than 1.0, except for in G. maderaspatana and L. flava, indicating that most plants in this study area could pose health risks to the consumers, particularly from As and Cd. These heavy metals are well established as being toxic for living systems and for their effects on humans. As promotes bladder, lung, and skin cancer. Cd can attack the kidneys, liver, bones, and affects the female reproductive system (Peralta-Videa et al. 2009). However, the HRI index values for Pb and Cr were less than 1 in all plants, indicating that Pb and Cr might not cause serious health problems in this study area compared to the other heavy metals. However, Cr concentrations in all plant species exceeded the standard for vegetables. Cr (III) is an essential element, relatively low concentration that recommended for daily intake in adult between 50 and 200 mg/day (ATSDR 1998). Cr has a low risk as compared with the other elements (Wang et al. 2005). Although low heavy metals concentrations were found in aquatic plants, the accumulated heavy metals could adversely affect human health from consumption. Exposure to low dose of Pb may result in subtle and non-specific change in the functioning of the brain (Baranowska-Bosiacka et al. 2013). In addition, childhood lead exposure is also an important public health problem. Children with low (