Disposal options for polluted plants grown on heavy metal contaminated brownfield lands – A review

Chemosphere 166 (2017) 8e20

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Review

Disposal options for polluted plants grown on heavy metal contaminated brownfield lands e A review Helga Kovacs*, Katalin Szemmelveisz
ros, 3515, Miskolc, Hungary University of Miskolc, Institute of Energy and Quality Affairs, Egyetemva

h i g h l i g h t s  This review analyzes the biological processes in plants accumulating pollutants from soil, to determine the heavy metal behavior during disposal.  This review summarizes and compares the disposal technologies and experiment results.  The phytoremediation (phytoextraction) technique of heavy metal contaminated soils were analyzed.  The behavior and distribution of heavy metals in plants were determined based on theoretical and experimental researches.Treatment and disposal options of contaminated biomass were critically analyzed and compared based on the literature.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 15 June 2016 Received in revised form 16 September 2016 Accepted 17 September 2016

Reducing or preventing damage caused by environmental pollution is a significant goal nowadays. Phytoextraction, as remediation technique is widely used, but during the process, the heavy metal content of the biomass grown on these sites special treatment and disposal techniques are required, for example liquid extraction, direct disposal, composting, and combustion. These processes are discussed in this review in economical and environmental aspects. The following main properties are analyzed: form and harmful element content of remains, utilization of the main and byproducts, affect to the environment during the treatment and disposal. The thermal treatment (combustion, gasification) of contaminated biomass provides a promising alternative disposal option, because the energy production affects the rate of return, and the harmful elements are riched in a small amount of solid remains depending on the ash content of the plant (1e2%). The biomass combustion technology is a wildely used energy production process in residential and industrial scale, but the ordinary biomass firing systems are not suited to burn this type of fuel without environmental risk. © 2016 Elsevier Ltd. All rights reserved.

Handling Editor: T. Cutright Keywords: Heavy metal Phytoextraction Ligneous plants Disposal options Thermal treatment

Contents 1. 2.

3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 1.1. Remediation of brownfield lands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 Toxic heavy metals in the plant system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 2.1. Effects of heavy metals on plant growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 2.2. Distribution of heavy metals in plant parts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 Treatment and disposal of biomass used for phytoextraction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 3.1. Composting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 3.2. Compaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 3.3. Pyrolysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 3.4. Direct disposal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 3.5. Leaching . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

* Corresponding author. Present address: University of Utah, Institute for Clean and Secure Energy, 870S 500W, Salt Lake City, UT, USA. E-mail address: [email protected] (H. Kovacs). http://dx.doi.org/10.1016/j.chemosphere.2016.09.076 0045-6535/© 2016 Elsevier Ltd. All rights reserved.

H. Kovacs, K. Szemmelveisz / Chemosphere 166 (2017) 8e20

3.6.

4.

Incineration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6.1. Gasification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6.2. Combustion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction 1.1. Remediation of brownfield lands During the last century less attention has been paid to environmental protection therefore the technology and techniques applied have generated and resulted in significant contamination. One of these toxic pollutions caused by industrial activities is the heavy metal pollution of soil and water. This type of contamination is very toxic and it typically occurs in areas surrounding mines (spoil-banks) and metal processing plants. The damage in most cases has no visible signs, although the vegetation might show signs of disease. In case of heavy metal polluted sites, the most important aim is to decrease pollutant levels and stop the spread of the contamination. There are several definitions (Fig. 1) used to describe brownfield lands (Alker et al., 2000) (Grimski and Ferber, 2001). The term brownfield land most commonly refers to abandoned, disused industrial or commercial sites that are difficult to redevelop due to existing pollution. Based on a report (Land Quality Management Group, 2006), the total area of brownfield lands was 11 000 ha in the Netherlands, 128 000 ha in Germany, 800 000 ha in Poland, and 900 000 ha in Romania. No specific data was available to describe the scale of brownfield land in Bulgaria, Greece, Hungary and the Slovak Republic, and there was no data on the total area of brownfield land in Denmark, Finland, Ireland and Sweden, Italy, Portugal or Spain. The density of the brownfield lands is generally between 0.25% and 0.5%, but in Poland and Romania, the density is particularly high (2.5e3.8%). These numbers are based on surveys, the real rate of contamineted lands could be significantly higher. Based on the different brownfield land definitions, it is clear that these data are not directly comparable, and include different kinds of site.

Fig. 1. Relationship between brownfield-related definitions (NICOLE Brownfield Working Group, 2011).

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13 14 14 17 17 17

The utilization of brownfield lands not only has economic benefits; it should also be an important part of regional (city) development. Nations worldwide handle the issue of these sites in different ways. The requirements of remediation, the limit values of the pollutants, and the methods used to rehabilitate the sites may vary form country to country. (Silverthorne, 2006). Locating and stopping the spread of the contamination in these areas can be expensive for the region and the country (Doick et al., 2009). The characteristics of the polluting materials determine which one of the numerous environmental remediation techniques available are used in any given situation, each having their advantages and disadvantages (Khan et al., 2004). A dominant factor in choosing the technology is the location of recultivation. If the remediation of polluted soil takes place at the contaminated site it is referred to as ‘in-situ’, if the remediation is carried out after relocation or transportation it is called an ‘ex-situ’ method. In cases where the requirements for in-situ processes are met, phytoremediation is the most commonly used technique. This method uses ligneous and herbaceous plants for the removal, accumulation and transfer of pollutants (Yao et al., 2012). The related processes are environmentally friendly and effective techniques widely used to clean heavy metal contaminated soil, water
nyi, 2007). Phytoextraction is and groundwater (Anton and Mura one of these processes. During phytoextraction, the plants accumulate heavy metals (for example lead, cadmium, zinc) from the soil, decreasing the concentration of the contaminants in the soil and rehabilitating the site (Yaapar and Binti, 2008). The polluting compounds and elements are transported into the roots and above ground parts of the plants, both of which can be easily harvested. The following short- and longterm studies (Table 1) have been carried out examining phytoextraction efficiency. The results prove the significance of this technology. At an abandoned mining site in Hungary, the remediation efficiency was attempted to be improved with soil treatments. In order to test the effects of the treatments, the accumulation ability of barley was examined (lat. Hordeum vulgare L.) (Tury et al., 2008). The experiments proved that certain soil treatments (for example compost, sewage sludge, and zeolite) have a positive effect on the plants grown in contaminated areas. The results showed that the plants accumulated and stored higher amounts of heavy metals in the roots. In the same area, other herbaceous plants (for example blackberry) were examined, and it results that - unlike other herbaceous plants - grasses store heavy metals mostly in the leaves (Kov
acs and
s, 2005). The bioconcentration factor and the heavy metal Tama accumulation ability of plants range widely in pot and field ex
nyi, 2007). Hyperaccumulators are for periments (Anton and Mura example corn (especially for cadmium), willow (cadmium, zinc), sorrel (cadmium, copper and zinc), radish (cadmium, zinc) and
nyi, 2007). elder (lead) (Anton and Mura At a mining site in the south of France, the accumulation rate of plants was examined in relation to the cadmium and zinc levels of the soil (Robinson et al., 1998). The results show, that if the zinc content of the soil reaches a certain level, the zinc accumulation

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H. Kovacs, K. Szemmelveisz / Chemosphere 166 (2017) 8e20

Table 1 Completed phytoextraction remediation experiments. Pollutants

Plants

Results, conclusions

Cu, Pb, Zn

Fescue (Festuca arundinacea), Indian mustard (Brassica juncea) Willow (Salix viminalis)

Hg

Wheat (Triticum aestivum) Barley (Hordeum vulgare) Lupinus „Chandelier” (Lupinus luteus) Chinese brake (Pteris vittata) Indian mustard (Brassica juncea)

Goal: The effect of EDTAa as a soil treatment was analyzed. Properties: 1 and 2 weeks' duration, examined samples: plant leaves, laboratory experiments, MayeSept 2002. Results: The heavy metal take up and the heavy metal content in leaves was increased by the extended soil treatment. The efficiency of phytoextraction was increased (Roy et al., 2005). Goal: Accumulation process analyzing. Properties: Field experiment, 3 years' duration. Results: The results show that industrial crops are able to accumulate mercury (Rodriguez et al., 2005).

As, Pb

Cd, Cr, Cu, Zn

Populus deltoides x maximowiczii-clone Eridano and P. x euramericana-clone I-214

As, Co, Cu, Pb, Zn

White poplar (Populus alba) Black poplar (Populus nigra) Aspen (Populus tremula) and White willow (Salix alba) Crack willow (Salix fragilis) Common osier (Salix viminalis)

Cd

As, Cd, Pb, Zn

a

Willow species (Salix spp.)

Goal: EDTA effects analyzing. Properties: Field and greenhouse experiment. Results: The research proves that soil treatment agents like EDTA are required for plants in order to improve lead accumulation (Salido et al., 2003). Goal: accumulation process analyzing. Properties: Field experiment. Results: In contaminated plants certain heavy metals (for example zinc, copper, and chrome) were detected, while the cadmium concentration was under the measurement limit (Sebastiani et al., 2004). Goal: accumulation process analyzing. Properties: Pot experiment (2004e2005) and field experiment (2005). Results: The nutrient concentration in the roots was much higher than in the above ground plant parts. The concentration was extremely high in the root-endings. Regarding the results it can be stated that the black pine (pinus nigra) and the white willow (salix alba) had the best accumulation ability under the given circumstances (Vamerali et al., 2009). Goal: soil treatment effects. Properties: Greenhouse experiment. Results: There is no correlation between the treatment and plant growth. High cadmium and zinc concentrations were measured in above-ground plant parts of both willow clones. Other elements (copper, chrome, iron, manganese, nickel and lead) were enriched mainly in the roots. The bioconcentration factor of leaves was highest in soil contaminated with low levels of cadmium and zinc. (Vandecasteele et al., 2005) Goal: yield apacity effects. Properties: Pot experiment. Results: Close correlation was determined between the accumulation of arsenic and cadmium, and yield-capacity. In various contaminated soils, higher yield-capacity was always accompanied by higher accumulation (Vyslouzilova et al., 2003).

Ethylenediaminetetraacetic acid, widely abbreviated as EDTA.

ability of plants starts to decrease. In the case of cadmium, the effect is less pronounced, but at very high cadmium levels, the cadmium accumulation of plants still significantly decreases. This means that the pollution rate of the soil directly affects the remediation efficiency of phytoextraction. This can be explained by the fact that plants have limited tolerance against pollutants. In this study, various soil treatments were applied in order to increase the accumulation rate and the solubility of pollutants. With these treatments, plants were able to accumulate higher amounts of contaminants. These findings were further confirmed by experiments carried out with other plants and pollutants (Rosselli et al., 2003). Hyperaccumulators have been defined by the calculation of the bioconcentration factor in several studies. The heavy metal content of these plants can be 1e5% (Raskin et al., 1997) depending on environmental, soil and plant characteristics. According to the most accepted definition, hyperaccumulators are plants that can take up high amounts of heavy metals at both low and high heavy metal levels in the soil (Ogundiran and Osibanjo, 2008) (Boularbah et al., 2006) ((Ginocchio and Baker, 2004). Further definition for hyperaccumulators is that plant species, which are capable of accumulating metals in above-ground tissues at higher concentrations than those present in the soil (Maestri et al., 2010). They have been termed hyperaccumulators when the metal concentrations are 50e100 times higher (McGrath and Zhao, 2003). Another standard definition of hyperaccumulation is the processes of metal uptake from the soil at high rates, translocation and accumulation of the same in plant shoot organs, stem and leaves (Maestri et al., 2010). Many species of hyperaccumulators are known, these are plants that can store store high amounts of heavy metals without suffering any damage (Van der Ent et al., 2012). These plants are mostly herbaceous which has its disadvantages: the reduced root system results in low remediation depth and the plants require frequent treatment. Less than 20% of hyperaccumulators are ligneous plants. The following hyperaccumulating species have been confirmed in

literature (Saladin, 2015):  Ni hyperaccumulators: Cassia siamea, Pycnandra acuminate,
et al., 2013) Rinorea niccolifera, (based on references (Jaffre (Callahan et al., 2008) ((Fernando et al., 2014)(Jambhulkar and Juwarkar, 2009));  Al hyperaccumulators: Stewartia monadelpha, S. pseudocamellia, Camellia sinensis, C. sasanqua, C. japonica, Cleyera japonica, Eurya japonica, Qualea grandiflora, Callisthene major, Vochysia pyramidalis (based on references (De Andrade et al., 2011) (Osawa et al., 2013));  Mn hyperaccumulators: Chengiopanax sciadophylloides, Maytenus cunninghamii, Gossia bamagensis, G. bidwillii, G. fragrantissima, G. sankowsiorum, G. gonoclada, Phytolacca acinosa, Grevillea exul var. exul, Schima superba (based on references (Fernando et al., 2006) ((Rabier et al., 2007) (Mizuno et al., 2008) (Yang et al., 2008) (Xue et al., 2010));  Cd hyperaccumulators: Ilex polyneura, Evodiopanax innovans, Rhododendron annae, Averrhoa carambola, Salix cathayana, S. dasyclados, Populus x canescens (based on references (Zu et al., 2004) (Li et al., 2011) (Dai et al., 2012) (Fischerova et al., 2006));  Zn hyperaccumulators: Rhododendron annae, Cassia siamea, Salix dasyclados (based on references (Fischerova et al., 2006) (Jambhulkar and Juwarkar, 2009) (Zu et al., 2004) (Li et al., 2011));  Pb hyperaccumulators: Ilex polyneura, Rhododendron annae, Sesbania drummondii (based on references (Zu et al., 2004) (Sahi et al., 2002) (Venkatachalam et al., 2009));  Fe hyperaccumulators: Cassia siamea (based on references (Jambhulkar and Juwarkar, 2009));  Hg hyperaccumulators: Sesbania drummondii (based on references (Sahi et al., 2002) (Venkatachalam et al., 2009)). Several studies have been carried out examining nonhyperaccumulating tree species that are able to store as much or

H. Kovacs, K. Szemmelveisz / Chemosphere 166 (2017) 8e20

more heavy metals than herbaceous hyperaccumulators. The ligneous plants studied for phytoextraction are especially fastgrowing trees such as poplar or willow (Di Lonardo et al., 2011) (Kovacs et al., 2013) (He et al., 2013). As several research proves, this remediation technique is widely used, but during the process, heavy metals are transferred from the soil into the plants resulting in decreased pollutant levels in the soil but increased levels in the plants. The goal of this review is to summarize and critically review the background of the disposal options, like liquid extraction, direct disposal, composting, or combustion. Before these technologies are analyzed, the main influential factors and processes are determined, like the effects of heavy metals on plant growth. 2. Toxic heavy metals in the plant system 2.1. Effects of heavy metals on plant growth Plants accumulate nutrients through the roots or leaves, but primarily through the root system. Several factors affect the nutrient uptake from the soil, for example the temperature, the
sz, 1988). The water content of the soil, the soil texture, and pH (Sza plants accumulate the water from the soil with the nutrients, and contaminants. The chemical composition of the biomass is an important factor for the remediation and the deposition processes. When chemical compositions of different biomass (dry sample) were compared, the results didn't show significant variation. The main chemical elements of biomass are (in decreasing order) C, O, H, N, Ca, K, Si, Mg, Al, S, Fe, P, Cl, Na, Mn and Ti (Vassilev et al., 2010). Both heavy metal nutrient deficiency and extremely high levels can cause metabolic dysfunction in plants (Gomes et al., 2014). Studies prove, that heavy metal accumulation in plants depends not only on the properties of the heavy metals and plants, but also on soil type and environmental circumstances (Gualab et al., 2010). The chemical balance of living organisms is a primary requirement for growth and development. This is the main reason why soil treatments (for example liming) are often necessary to keep plants alive (Ruttens et al., 2010) (Wilson et al., 2013) (Gray et al., 2006). The mobility and solubility of pollutants can be decreased with cement or Ca(OH)2 in a high pH soil environment ((Hale et al., 2012), but this affects to the accumulation factor of the plants. It means that this processes are required only in the case of the plant is not able to live on the contaminated soil without pretreatment. Toxic concentration is different in case of every nutrient. Some microelements important for plants (B, Cl, Cu, Fe, Mn, Mo, Ni, Zn) €nsch and Mendel, are not toxic in relative high concentrations (Ha 2009), but have affect to the plant growth adversely (Umesh et al., 2015). Other elements like cadmium, chromium, mercury, and lead do not interfere with plant growth in low concentration, but might be lethal in higher concentration. It is important to note that a certain amount of heavy metals can be stored in plants without any visible signs of toxicity (leaf atrophy, inhibition of plant growth, necrosis). Several studies have dealt with the effect of heavy metals on plant growth, and the toxic concentration of heavy metals for plants have been determined (Gangwar et al., 2014). Higher concentration of these elements have toxic effects on plants (Table 2). Studies proved that many plant species have some tolerance and some sort of detoxification mechanism against contaminants. Some plants, grown in highly polluted soil, did not contain high levels of metal in their shoots. In this case, the tolerance is achieved by the plant reducing metal transport from the roots to the shoots (Schat et al., 1999). Other species accumulate heavy metals in toxic concentration in the shoots, but survive with the help of a detoxification mechanism (Hall, 2001). The ability of plants to permit

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contaminants of a certain structure, lipophilicity, molecular mass and charge to enter their intercellular space is an important indicator of their detoxification potential (Kvesitadze et al., 2006). The main detoxification mechanisms are listed below (Hall, 2001) (Marschner, 2012):  Mycorrhiza: Colonisation of maize roots by mycorrhiza can reduce the heavy metal concentration in plants or increase accumulation from the contaminated soil (Weissenhorn et al., 1995),  The cell walls and root exudates: The root cells are in direct contact with metals in the soil solution, by limiting adsorption onto the cell wall metal activity (absorption, bonding) on the surface of the plasma membrane can be reduced.  Plasma membrane: The plant plasma membrane may be regarded as the first ‘living’ structure targeted by heavy metal toxicity. Plasma membrane function may be rapidly affected by heavy metals; the increased leakage from cells detectable in the presence of high concentration of heavy metals confirms this  Heat shock proteins: There are several reports of an increase in heat shock protein expression in plants in response to heavy metal stress.  Phytochelatins: Chelation of metals in the cytosol by highaffinity ligands is potentially a very important mechanism of heavy metal detoxification and tolerance.  Vacuolar compartmentalization: Efflux of ions at the plasma membrane or transport into the vacuole are two ways of reducing the levels of toxic metals in the cytosol and so are potentially important mechanisms of heavy metal tolerance. Most of these mechanisms have quite limited capacity. Many studies (Borgegard and Rydin, 1989) (Kopponen et al., 2001) have been carried out developing and testing special tree species in heavy metal contaminated areas with the aim to find the perfect plant for phytoextraction. This area is very important in phytoremediation research, because heavy metal tolerance is a key factor in the process. Remediation can only be carried out if the plants survive and grow in the contaminated soil. One potential area of research is the development of plants with high tolerance and efficient detoxification mechanisms for phytoextraction under specific circumstances. This is called genetic engineering. 2.2. Distribution of heavy metals in plant parts After successful remediation, every part of the plant contains heavy metal pollutants due to the transport processes. The concentration of heavy metals are the highest in the below ground parts, usually higher than in the above ground parts (stems, leaves, flowers) (Chakraborty et al., 2013) (Peters et al., 1997) (Jiang et al., 2015). Several studies verify that heavy metals accumulate in actively growing tissues such as sprouts, young leaves and bark (Chakraborty et al., 2013) (Mertens et al., 2006) (Tlustos et al., 2006). Pulford and Watson proved that the zinc and cadmium concentrations are highest in the foliage. The highest copper, lead, and chromium concentrations were measured in the trunk of willow species grown in sludge-treated soil, while zinc, cadmium, and nickel were accumulated mostly in the foliage ((Pulford and Watson, 2003). The distribution of heavy metals is important to know because the remediation of contaminated lands with plants may result in potentially hazardous biomass. This biomass with high heavy metal concentration needs to be disposed of carefully. Treatment options for these types of plants are discussed below. The general chemical composition of a plant is: 40e50% m/m carbon, 35e45%m/m oxygen and 5e6% m/m hydrogen (Shen et al., 2010). The remaining 1%

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H. Kovacs, K. Szemmelveisz / Chemosphere 166 (2017) 8e20

Table 2 Toxic effects of heavy metals on plants (Umesh et al., 2015). Heavy metal

Effects on plants

As Cd Cr

Inhibits photosynthesis, inhibits growth, biomass, and yield; death Chlorosis, growth inhibition, reduction in photosynthesis, water and nutrient uptake, browning of root tips, death Alteration in germination, inhibition of plant growth, chlorosis, nutrient imbalance, wilting of tops, root injury, inhibition of chlorophyll biosynthesis, photosynthesis, yield Chlorosis, necrosis, stunting, and inhibition of root and shoot growth. Inhibition of enzyme activity or protein function, impaired cell transport processes, and oxidative damage and metabolic disturbances Morphology, growth, photosynthesis, inhibition of enzyme activities, water imbalance, alteration in membrane permeability, oxidative stress Obstruction of water flow, interference of mitochondrial activity, oxidative stress, disruption of biomembrane lipids and cellular metabolism, affects photosynthesis Inhibits chlorophyll biosynthesis, chlorosis, necrosis, water and nutrient imbalance, disorder of cell membrane functions, wilting, browning of root tips Inhibition of root growth, senescence, chlorosis, oxidative stress

Cu Pb Hg Ni Zn

composition was: 90 kg water hyacinth, 45 kg cattle manure and 15 kg sawdust with 0, 1, 2 and 3% of lime. The lime treatment however had no effect on the increase in total heavy metal concentration of the samples (for example Zn concentration in Fig. 2) because of the volume reduction and mineralization processes (Singh and Kalamdhad, 2013) (Singh and Kalamdhad, 2012).

m/m is formed by other metallic and non-metallic elements. In plants, the distribution of metals is uneven with some plant parts accumulating higher amounts of certain elements. This distribution can be best observed in trees (foliage, trunk, bark, roots). 3. Treatment and disposal of biomass used for phytoextraction

3.1. Composting The composting technology is an accepted treatment for contaminated plants (Garbisu and Alkorta, 2001) used as a volume reducing method. Since American researchers have shown the water solubility of bioaccumulated zinc and other metallic components (Zhao et al., 2000) however, this method can only be applied under strict monitoring. The end product of the composting process may contain excessively high amounts of heavy metals, preventing agricultural utilization of the compost. There is some research aimed at developing treatment techniques that would  et al., 2012). Two methods have produce non-hazardous waste (Syc been studied so far:  Mixing with other compost material: Total heavy metal content can be minimized by mixing the metal-enriched biomass with high proportions of uncontaminated dry matter and other biodegradable substances. The technology requires the close and continuous monitoring of mixture composition. The positive aspect of this method is that the phytoextracted metals are returned into the soil in small doses which contributes to nutrient recovery. Ex-situ composting post-harvest was proposed as a more effective method for the disposal of hazardous biomass (Guangwei et al., 2009).  Decrease the leachable metals in the compost: A 30 days composting experiment proved, that the addition of lime significantly reduces the water soluble metals (Zn, Cu, Fe and Cr), penetric acid extractable metals (Zn, Cu, Fe, Ni and Cr) and leachable metals (Zn, Fe, Ni, Cr and Cd) during water hyacinth composting (Singh and Kalamdhad, 2013). The compost

The main advantages of composting are the volume and water content reduction, but it takes a long time (several months), and requires special equipment. If basic composting technology was used the product would still require treatment prior to disposal. 3.2. Compaction Compaction of harvested, contaminated plants provides another solution, but exact data or experiment results are hard to find in this area of research. The compaction (pelletization) process is a complex interaction between particles, the compacted product is produced by pressure, and the leachate is collected seperately. Knowledge of the fundamental compaction properties of particles of different biomass species, sizes, shapes, chemical compositions, bulk densities and particle densities is essential to optimize densification processes (Thomas and van der Poel, 1996) (Mani et al., 2006). To compact the material a container is required. The end products of this method still need to be treated as hazardous waste. 3.3. Pyrolysis Pyrolysis can be used for the disposal of heavy metal contaminated biomass (Bridgwater, 1999) (Chami et al., 2014) (Stals et al., 2010) (Lievens et al., 2008a) (Lievens et al., 2008b). The products of pyrolysis are divided into a solid fraction, a liquid fraction and a

Zn concentraƟon, mg/kg

Remediation with phytoextraction decreases the heavy metal content of the soil, thereby moderating the environmental risk caused by the toxic elements. During this process, the pollutants are transferred into the plants; creating an environmental hazard of a different nature. Soil remediation and polluted biomass formation occur simultaneously. The treatment of this contaminated biomass is required. In 2004 a study (Sas-Nowosielska et al., 2004) determined the following disposal options: composting, compaction, pyrolysis, direct disposal, leaching, and incineration (combustion and gasification).

350 300 250 200

0 % lime

150

1 % lime

100

2 % lime

50

3 % lime

0 0

6

12

18

24

30

ComposƟng days Fig. 2. Changes in Zn concentration during composting process, based on reference (Singh and Kalamdhad, 2013).

H. Kovacs, K. Szemmelveisz / Chemosphere 166 (2017) 8e20

13

 TCLP - Prior to extraction; 20:1 liquid to solid (L/S) ratio; mixing for 18 h at 30 rpm; filtering;  ASTM leaching procedure - 4:1 liquidesolid ratio (L/S) ratio; the pH of the solution was the same with distilled water;  Synthetic precipitation leaching procedure (SPLP) (US EPA Method 1312) - 20:1 liquidesolid ratio (L/S) ratio; the extraction fluid consists of slightly acidified de-ionized water that is formulated to simulate natural precipitation; mixing for 18 h at 30 rpm;  The field leach test is used to predict, assess, and characterize the geochemical interactions between water and a broad variety of geologic and environmental matrices;  Leaching extraction procedure (LEP) is used to investigate the leaching potential of toxic components into the environment by extraction with an acidic medium.

gas fraction (Stals et al., 2010). In the case of heavy metal contaminated plant pyrolysis, the main goal is to reach the highest pollutant concentration in the solid fraction, and the lowest in the liquid and gaseous phases. Fast pyrolysis of biomass results in maximum amount of liquid and minimum amount of gaseous products. Intermediate pyrolysis produces high quality solids and tar free vapors (Hornung et al., 2011) (Chami et al., 2014) making it theoretically the optimal process for heavy metal polluted biomass. Fast pyrolysis however produces a better quality liquid phase, and for this reason, it is often used for pyrolysis experiments carried out with contaminated biomass (Bridgwater, 1999). Since pyrolysis temperatures are lower than in case of other thermic processes like combustion or gasification, fast pyrolysis prevents metal volatilization in the reaction zone (Kuppens et al., 2015). The processes in the pyrolysis reactor (temperature, volatilization of heavy metals) have been analyzed by many researchers (Dilks et al., 2016) (Mayer et al., 2012a) (Fahmi et al., 2008) (Mayer et al., 2012b) (Debela et al., 2012). A study (Freddo et al., 2012) analyzed the heavy metal content of biochar produced from bamboo, redwood, and maize (low toxicity provenance) at temperatures of 300  C and 600  C (Table 3). The results show that there is no significant difference between the Cd, Cr, Cu, Ni, Pb, Zn, and As content of biochar produced at the different examined temperatures. An experiment proved that 383  C is the ideal pyrolysis temperature with minimal amounts of Zn and Cd transferred into the obtained pyrolysis oil. At 440  C significantly higher levels of volatile metal was measured in the pyrolysis products (Stals et al., 2010). Tom Kuppens et al. made a techno-economic assessment analysis, and verified that fast pyrolysis is a potential technique to be used for heavy metal contaminated biomass disposal (Kuppens et al., 2015).

If limit values are in force in a country, they are usually set out in the soil protection regulations. 3.5. Leaching This disposal technology is based on the tendency of soluble metals to percolate through the carrying medium e which is the very property that accounts for the categorization of metal contaminated biomass as hazardous waste (Kovacs et al., 2013). After enrichment, toxic metals are leached with different solvents from the compacted biomass (Mulligan et al., 2001). The leached product (residual biomass matter) can be treated as non-hazardous material (Sas-Nowosielska et al., 2004). There are relatively highcost technologies available to recover the metallic components from the leached solution (Mulligan et al., 2001). The leachability (i.e. recovery rate) of toxic metals from biomass is generally determined as a function of time and pH value (Saeed et al., 2005). Several leaching techniques are described in Section 3.4.

3.4. Direct disposal

3.6. Incineration

This process is time-effective, but it has high costs, and the reduction of contaminated biomass is slow. The direct disposal of the harvested biomass waste would cause environmental problems  et al., 2012) (Kovacs et al., 2013). The therefore, it is forbidden (Syc main problem is the leachable pollutant content of the contaminated plants. Several leaching tests exist and in some countries, leaching or solubility test methods and limit values are applied to assess and control the danger associated with the direct disposal option. To determine the metal composition of the solid material, specific extractors are used. Different agents solubilize different elements. The most frequently used leaching agents are distilled water, acids (acetic acid, nitric acid, sulfuric acid, hydrochloric acid) and sodium hydroxide. A few testing methods are summarized below (Çoruh et al., 2013):

This process is based on the thermal degradation (combustion, gasification) of contaminated woody biomass into manageable volumes of metal-containing ash. The difference between incineration and pyrolysis is that after combustion and gasification, the solid remains contain only ash (under optimal circumstances). The other difference is that the temperature of the incineration processes is higher than the temperature used for pyrolysis. The incineration of heavy metal contaminated biomass is a promising yet not fully developed technology. Various combustion systems are currently under development for field-scale application. In the near future, this method will likely provide an environmentally sound and economically acceptable alternative (SasNowosielska et al., 2004). Disposal through incineration is an excellent option to replace the expensive treatment and costly transportation of the harvested

Table 3 Concentrations (mg/kg) of metals and metalloids in biochar at 300  C or 600  C pyrolysis temperature (Freddo et al., 2012). Heavy metal

Bamboo 

Cd Cr Cu Ni Pb Zn As

Redwood 



300 C

600 C

300 C

0.03 ± 0.001 4.3 ± 0.06 10.0 ± 8.1 1.37 ± 0.55 1.92 ± 0.15 124 ± 2 0.27 ± 0.01

0.03 ± 0.003 4.39 ± 0.21 6.31 ± 0.01 1.25 ± 0.22 3.87 ± 1.08 207 ± 3 0.29 ± 0.01

0.94 4.51 2.03 0.42 0.64 38.5 0.12

± ± ± ± ± ± ±

Maize 

300  C

600 C 0.01 0.23 0.06 0.03 0.06 3.5 0.02

0.02 3.42 2.06 0.57 0.87 38.5 0.16

± ± ± ± ± ± ±

0.002 0.19 0.07 0.24 0.11 3.8 0.03

0.03 5.09 10.6 0.37 0.06 92.0 0.25

± ± ± ± ± ± ±

600  C 0.003 0.27 0.5 0.04 0.11 2.3 0.03

0.03 6.48 13.2 0.59 1.07 53.9 0.21

± ± ± ± ± ± ±

0.01 1.79 0.27 0.09 0.1 3.3 0.01

14

H. Kovacs, K. Szemmelveisz / Chemosphere 166 (2017) 8e20

biomass to hazardous waste disposal facilities. Using these methods up to 99% volume reduction of the contaminated material can be achieved with the pollutants concentrated in the solid combustion residues (ash, fly ash). The final product is easy to mobilize and handle in a controlled, environmentally acceptable manner.

3.6.1. Gasification The aim of biomass gasification is to produce valuable gaseous material with high CO and H2 concentration. In the case of contaminated biomass, the syngas will most likely contain toxic heavy metals. During the utilization of syngas, this pollutant content causes technological and environmental problems. In gas engines, it generates fouling and corrosion problems and affects the catalyst (Salo and Mojtahedi, 1998) (Pudasainee et al., 2014). Heavy metal volatilization temperatures vary significantly in a multi-phase equilibria system involving multiple elements such as gasification. Furthermore, the volatilization temperature depends on pressure, the gasifying agent and fuel composition (Vervaeke et al., 2006) (Jiang et al., 2015). In a study (Jiang et al., 2015), concentrations of K, Na, Ca, Al, Mg, Mn, Cr, Co, Se, Pb, Cd, Cu, Zn, Ni, Hg and As were analyzed based on thermodynamic modeling, Scientific Group Thermodata Europe (SGTE) database information and results of 5 biomass chemical analysis. A typical steam to oxygen ratio of 2:1 was selected for the model and the simulation was carried out at atmospheric pressure. It was determined that As, Cd, Zn and Pb tend to transform into their gaseous forms at relatively low temperatures (<1000  C), other elements (Mn, Cu, Co, Ni) are moderately volatile (Table 4). Another result was that an increase in pressure lead to higher phase transition temperatures (Jiang et al., 2015), this had been verified in previous studies (Liu et al., 2006) (Froment et al., 2013). Froment et al. (2013) carried out thermodynamic equilibrium calculations with FactSage software to calculate the volatilization and condensation temperature of heavy metals (As, Zn, Hg, Pb, Cd, Se, Ag, Cu, Mn, Cr, Fe, Mg). The elementary composition tested was of a typical wood biomass. The reactor pressure was 1e10 bar, the reactor temperature ranged from 500 to 1500  C. Experiments analyzing the heavy metal content of syngas and solid remains (ash, fly ash) produced by gasification (Wu et al., 2014) (Marrero et al., 2004) (Kim, 2009) (Pudasainee et al., 2014) are rare in literature. In a gasification experiment (Vervaeke et al., 2006) the heavy metal distribution was examined in a fixed bed downdraft gasifier (100 kW thermal power, equipped with a hot cyclone and a water scrubber, which acted as a cooling tower in order to remove smaller ash fractions). Three experiments were carried out; a heavy metal contaminated willow species (Salix viminalis L. clone) was used as fuel. The results show that the total amount of analyzed heavy metals could not be detected (except Zn e test 2) in the solid material flows, which means that a large amount of toxic elements was in volatile form in the synthesis gas (Fig. 3). Wu et al. (2014) proved the following connections:  The concentrations of Cr, Pb, and Cd in the fly ash increase with increasing operating temperatures during gasification.  When the operating-gas velocity increases, the heavy metal content of the bed material also increases.  The amount of heavy metals in the fly ash increases with increasing bed-material particle size  The total amount of heavy metals in the bed material increases as the operating temperature and bed-material particle size decreases; and in contrast, as the operating-gas velocity increases.

3.6.2. Combustion Combustion of heavy metal contaminated biomass not only results in regular emissions (CO, NOx, fly ash), but also produces solid and gaseous metal compounds. Further examination of these compounds during combustion of unpolluted biomass fuels would be important, because certain studies prove, that environmental problems caused by heavy metal emission could arise even if the r, 2012) (Steenari biomass comes from an unpolluted area (Sarabe and Lindqvist, 1999) (Nzihou and Stanmore, 2013). Heavy metals entering the combustion chamber exit in one of three forms: solid remains in the combustion chamber (bottom ash); solid particles in the flue gas (fly ash); and the exhausted gas (flue gas). Due to their solubility, heavy metals are enriched in the bottom ash after combustion. This limits the disposal options of the ash. The leached heavy metals may cause environmental damage at waste yards (Christensen et al., 2001) (Kjeldsen et al., 2002). Heavy metal compounds are volatile at the combustion temperature (Cenni et al., 1998) (Karimanal and Hall, 1996). As the flue gas flows across the off-take system the temperature decreases, and the toxic compounds condensate on surrounding solid particles
l, 1999). The heavy metal compounds can be detected in two (Pa forms at the end of the chimney (depending on the temperature):  submicron ash  vapor form. The final distribution of heavy metals is shown in Fig. 4. Several studies deal with the heavy metal content of bottom ash and fly ash produced during biomass combustion (Toledo et al., €ykio € et al., 2016) (Nzihou and Stanmore, 2013) (Li et al., 2005) (Po 2012) (Xiao et al., 2015) (Zhong et al., 2015) (Wu et al., 2014) (Kovacs et al., 2015) (Kovacs et al., 2016) and other solid fuel combustion (Wu et al., 2014) (Sun et al., 2016) (Ryua et al., 2006) (Simoneit et al., 1993). The distribution of heavy metals in solid and gaseous burning residues is referred to as partition of metals (Randall Seeker, 1991). These studies prove that the solid remains of contaminated biomass combustion are potential environmental pollutants. Toledo et al. verified this theory with experiments in a bubbling fluidized bed incinerator equipped with cyclone and hot ceramic filters. They proved that  the distribution of the heavy metals (Ni, Zn, Pb, Cu, Cd, Cr) is governed by kinetics and by fluid-dynamic factors (gas velocity in the incinerator and the particle size of the ash);  the amount and/or percentage of chlorine in the feedstock has an important influence on the specific heavy metals, like Cd and Pb;  the fate of the heavy metals (Ni, Zn, Pb, Cu, Cd, Cr) depends on the residence times of the ashes and particulates at high temperature (Toledo et al., 2005). Fly ash samples coming from municipal solid waste burners were analyzed by X-ray scattering and the following compounds were detectable in flue gas at 420  C (the burning temperature was 953  C).  oxides: Al2O3, MnO, Pb3SiO5, Pb3Sb2O7, PbSiO4, Fe3O4, Fe2O3,  others: Pb3O2SO4, Cd5(AsO4)3Cl, CdSO4, K2ZnCl4, ZnCl2, ZnSO4 (Evans and Williams, 2000). In every respect, the solubility of metals is a very important factor. The metals could be solubilized with chemicals from the solid remains (bottom ash, fly ash), but the solubility is influenced

H. Kovacs, K. Szemmelveisz / Chemosphere 166 (2017) 8e20

15

Table 4 Calculated and simulated solidegaseous phase transition of heavy metals by biomass gasification. Heavy metal

Transition starting temperature (solid/gaseous),  C

Element/compound exists completely in gaseous form above this temperature,  C

As

~600 <500

~980 ~1050

~510 ~540 ~410e490

~640 ~650 ~600 <500 <500 <500

Zn Pb Hg Se

Cd Ag

~720

~220 <500 ~900

Ni Cu

~1080 ~900 ~860 ~820 ~1050 ~1020 ~1200 ~1150

~1320 ~1200 ~1050 ~1010 1250 ~1250 ~1420 ~1370

~1600 ~1250 ~1200

>1800 ~1610 ~1450

~1350 ~1280

~1550 >1500

Mn Co Cr

Al Fe

Mg

~190

Condensation temperature

1050 (CuAs) 250 (As2S2) 625 (ZnS) 475 (PbSe) 75 (HgSe) 475 (PbSe) 375 (CdSe) 150 (Sb2Se3) 75 (HgSe) 375 (CdSe) 775 (Ag3Sb) 875 (Ag)

1050 (CuAs) 1275 (MnO)

1275 (MgO)(Cr2O3) 875 (Na2O)(Cr2O3)

1275 (Fe) 1150 (Ca2Fe2O5) 900 (FeCr2O4) 650 (FeO) 625 (Fe3O4) 1275 (MgO) 1275 (MgO)(Cr2O3)

Reference

(Jiang et al., 2015) (Froment et al., 2013) (Jiang et al., 2015) (Froment et al., 2013) (Jiang et al., 2015) (Froment et al., 2013) (Froment et al., 2013) (Froment et al., 2013)

(Jiang et al., 2015) (Froment et al., 2013) (Froment et al., 2013) (Jiang et al., 2015) (Jiang et al., 2015) (Froment et al., 2013) (Jiang et al., 2015) (Froment et al., 2013) (Jiang et al., 2015) (Jiang et al., 2015) (Froment et al., 2013) (Jiang et al., 2015) (Jiang et al., 2015) (Froment et al., 2013)

(Jiang et al., 2015) (Froment et al., 2013)

Fig. 3. The distribution of heavy metal in measured solid material flows (bottom ash, cyclone ash, and filter fly ash) in a fixed bed downdraft gasifier, based on reference (Vervaeke et al., 2006).

by the combustion technology (Randall Seeker, 1991) (Tao et al., 2014) (Izquierdo and Querolb, 2012), the metal compound's properties and other circumstances as well (Van der Bruggen et al., 1998). Zhong et al. analyzed hyperaccumulator biomass combustion in a horizontal tube furnace. They verified that the most likely chemical forms of Pb under combustion conditions are the elemental metal and its oxide in both the fly ash and bottom ash. For Cd and Zn, possible components are the elemental metals, their

oxides and carbonates, and silicate compounds may be found under low temperature conditions (Zhong et al., 2015). Ljung et al. made equilibrium calculations considering nutrints and heavy metals. They used CHEMSAGE 3.0 for modeling the fate of the elements. The effect of S and Cl availability was also analyzed, and the following results are summarized (Ljung and Nordin, 1997):  Cadmium: S and Cl availablity influence: yes. By 50e100% of the S and Cl in the fuel are available for reaction with Cd, the solid

16

H. Kovacs, K. Szemmelveisz / Chemosphere 166 (2017) 8e20

Fig. 4. Partition between the four exit flows of the solids generated in a bubbling fluidized bed incinerator equipped with a cyclone and hot ceramic filter (Toledo et al., 2005).











sulfate will be the stable species at low temperatures, and CdCl2(g) may be found vaporized in the temperature range of 600e800  C. At higher temperatures, elemental Cd(g) will form. Copper: S and Cl availablity influence: yes. If S and Cl are available, the volatilization temperature of CuCl(g) may be as low as 900  C. Chromium: S availablity influence: yes, Cl availablity influence: no. Cr will form CrSO4(c) and Cr2O3(c) up to 1000  C if S is available. At this temperature, CrO3(g) will start to form, and at 1250  C it is the predominant species, although the amount of CrO2(g) increases with increasing temperature. No chromium chlorides were formed at any of the studied Cl concentrations. Lead: S and Cl availablity influence: yes. For higher amounts of S and Cl, a gaseous chloride was unexpectedly formed at temperatures even below 100  C, probably due to some inaccuracy of thermochemical data of PbCl4(g). If S and Cl concentrations higher than 10% were used, PbCl4(g) was formed around 700  C. Nickel. Ni will form NiO(c) at temperatures as high as 1500  C, irrespective of the concentrations of Cl. If S is available, NiSO4(c) will form at the low temperatures. Nickel will thus be condensed at temperatures up to about 1450  C. Zinc. The behavior of Zn is quite similar to Ni, although the volatilization temperature is somewhat lower (1170  C).

Based on the theoretical calculations and rare experimental results, the volatilization and condensation of heavy metals requires further examination. Besides the decreasing flue gas temperature, the gaseous-solid transition (particle formation) is controlled by two mechanisms. The condensation can be activated in two ways: heterogeneous or

€ ller et al., 2007) (Mcnallan et al., homogeneous condensation (Jo 1981) (Fan et al., 2013). Heterogeneous condensation takes place on a foreign solid surface. To maintain the process, the vapor pressure must be higher than or equal to the saturation pressure. During homogeneous condensation, nuclei are formed in the midst of a gas environment. This process requires a gas/vapor pressure higher than the saturation pressure (Bae et al., 2010). Heterogeneous condensation, which occurs on particles, is much more common in thermal treatment processes of biomass, because the energy barrier is lower than in the case of homogeneous condensation (Fan et al., 2013). Heterogeneous condensation is not just a form of condensation. It is also used as a preconditioning technique because during this process, vapor condensates on ultrafine particles creating a more coarse liquidesolid aerosol, which can be used to improve the performance of traditional particle collection devices (Tammaro et al., 2012). As soon as the metal vapors reach the state of supersaturation (a state of a vapor of heavy metal compounds that has a higher (partial) pressure than the vapor pressure of that compound), the condensation begins and it contributes to the formation of ultra-fine particles (Jiao et al., 2013). The effect of temperature on the heavy metal (Cu, Pb, Zn, Cd, and Mn) content of flue gas was examined during sewage sludge combustion experiments. The results proved that temperature increase results in higher compound content in the flue gas (Hu et al., 2014). The effect of temperature on the distribution of heavy metals (ash, fly ash, flue gas) during biomass combustion was analyzed by several researchers (Tang et al., 2015). The results of these studies show the same connection between the temperature and reaction of the metals.

Table 5 Volatility temperatures and chemical formula of metals at 1 Pa operating pressure (Randall Seeker, 1991). Heavy metal

No chlorides

With 10% of chlorides 

Cr Ni Pb Cd

Volatility temperature ( C)

Form

Volatility temperature ( C)

Form

1613 1210 627 214

CrO2/CrO3 Ni(OH)2 Pb Cd

1610 693 15a 214

CrO2/CrO3 NiCl2 PbCl4 Cd

a PbCl4 has a tetrahedral structure, which is held together by weak van der waals forces. Because o f this all the compounds have low boiling points and are liquids at room temperature. This compound is a volatile liquid with high vapor pressure at room temperature, and with a volatility temperature of - 15  C (similar to SnCl4: 33  C, SiCl4: 70  C) (Madan and Prakash, 1987) (Greenwood and Earnshaw, 2012).

H. Kovacs, K. Szemmelveisz / Chemosphere 166 (2017) 8e20

Metal levels in the flue gas are also affected by the presence of different types of chlorine-, sulfide-, carbon-, nitrogen- and other compounds in the combustion chamber and flue gas. Hu et al. carried out sewage sludge combustion experiments proving that the Zn and Pb content of flue gas could be decreased with higher moisture content (Hu et al., 2014). They also verified that the increase of chlorine content in the combustion chamber could cause higher Cd, Zn, and Pb concentrations in the flue gas (Hu et al., 2014). Randall Seeker (Randall Seeker, 1991) analyzed the effects of chlorides in the burning system on volatility temperature of Cr, Ni, Pb, Cd at 1 Pa pressure using thermochemical calculations. The results verified the increase of concentration in the flue gas caused by the decreasing volatility temperature (Table 5). A reducing atmosphere around the burning fuel particles seems to accelerate heavy metal volatilization because the formation of less volatile metal oxides is limited by the lack of oxygen (Obernberger et al., 2006). Further treatment of the solid remains (ash, fly ash) is a complex problem, several studies have been carried out to compare or analyze these techniques (Quina et al., 2008) (Sabbas et al., 2003) (van der Sloot et al., 2001) (Yu et al., 2015), most of the research examines ash and fly ash during municipal solid waste incineration. The most commonly used method  to extract heavy metals from remains for further recovery (Quina et al., 2008) is leaching (Zhang and Itoh, 2006) (Mangialardi, 2003) (Shemi et al., 2015),  ova
 for the disposal of the remains is thermal treatment (Kubon et al., 2013) and stabilization (Mangialardi, 2003). The stabilization can be improved by using cement or a chelating polymer. The aim of thermal treatment is the convert the fly ash into slag, but the heavy metals evaporate during this process creating a subsequent environmental problem. Combustion as a disposal option requires careful consideration as it may lead to environmental pollution. A method that would guarantee completely safe treatment has not been developed yet. Its advantage is that this process is not only a disposal option, but also has energy producing potential. In case of combustion of metal contaminated biomass however, the hazard of the solid remains (bottom ash, fly ash) and the flue gas must be evaluated. Measuring the amount of metals in volatile form in the flue gas presents a significant technological challenge, while developing technology that would minimize or eliminate metal emission is the biggest environmental task. Using a dust (and condensed metal) extractor for the flue gas is an obvious, but imperfect solution. The dust extractor can only eliminate metal emission if the flue gas temperature is low enough and the condensation of metal compounds finishes before the separator, allowing it to separate the fine dust. If these conditions are not met, the extractor system is unsuitable for metal separation. In this case additional flue gas cleaning techniques are required. 4. Conclusion Heavy metal contaminated biomass combustion is a diversified topic, and it can be approached in many ways. The first aspect of research is the analysis of the source of these polluted plants, but the phytoextraction as remediation technology and plant accumulation processes are well-researched areas. The second part is to examine the behaviors of heavy metals in the plant ecosystem with the aim to influence the remediation process (maximizing accumulation). The third area of research is to develop the optimal disposal option for these contaminated plants. Several disposal options are known and have been tested, but the comparison of

17

various techniques is a complex task, because the methods depend on many different factors (type of metal and plant, the aim of the treatment, environmental circumstances). All of the technologies have environmental effects, for example the wastewater created by leaching, the compost produced by composting or the solid and gaseous compounds produced by incineration. Biomass combustion is a known alternative for disposal, but experiments examining emissions have only been performed in the last few years. This area of research is also important because of energy production, as in this age of high energy consumption every potential energy source must be considered. Reviewing the literature, it can be stated, that the combustion of contaminated biomass is not an ordinary biomass firing process. The particles in the flue gas contain metal compounds, which makes the application of an efficient air cleaning system necessary. The studies presented examine these problems, and analyze the behavior of heavy metals during the thermal treatment processes, but further experimental examinations and development of new firing systems for heavy metal contaminated biomass are required in order to prevent environmental pollution. The disposal options discussed in this review produce toxic or hazardous materials with high heavy metal content. The design and implementation of these processes require careful consideration and monitoring. Acknowledgements This research was carried out in the framework of the Center of Excellence of Sustainable Resource Management at the University of Miskolc. References Alker, S., Joy, V., Roberts, P., Smith, N., 2000. The definition of brownfield. J. Environ. Plan. Manag. 43 (1), 49e69.
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anyi, A., 2007. Effective Phytoremediation (Hungarian: Hate
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) (Budapest). Fitoremedia Bae, H., Kim, I., Kim, E., Lee, J., 2010. Generation of nano-sized AreN2 compound particles by homogeneous nucleation and heterogeneous growth in a supersonic expansion. J. Aerosol Sci. 41 (3), 243e256. Borgegard, S., Rydin, H., 1989. Biomass root penetration and heavy metal uptake in birch in a soil cover over copper tailings. J. Appl. Ecol. 26 (2), 585e596. Boularbah, A., Schwartz, C., Bitton, G., Aboudrar, W., Ouhammou, A., Morel, L., 2006. Heavy metal contamination from mining sites in South Morocco: 2. Assessment of metal accumulation and toxicity in plants. Chemosphere 63, 811e817. Bridgwater, A., 1999. Principles and practice of biomass fast pyrolysis processes for liquids. J. Anal. Appl. Pyrolysis 51 (1), 3e22. Callahan, D., Roessner, U., Dumontet, V., Perrier, V., Wedd, A., O'Hair, R., Kolev, S., 2008. LCeMS and GCeMS metabolite profiling of nickel(II) complexes in the latex of the nickel-hyperaccumulating tree Sebertia acuminata and identification of methylated aldaric acid as a new nickel(II) ligand. Phytochemistry 69, 240e251. Cenni, R., Frandsen, F., Gerhardt, T., Splietho, H., Hein, K., 1998. Study on trace metal partitioning in pulverized combustion of bituminous coal and dry sewage sludge. Waste Management 18, 433e444. Chakraborty, D., Bhar, S., Majumdar, J., Santra, S., 2013. Heavy metal pollution and Phytoremediation potential of Avicennia officinalis L. in southern coast of the Hoogly estuarine system. Int. J. Environ. Sci. 3 (6), 2291e2303. Chami, Z., Amer, N., Smets, K., Yperman, J., Carleer, R., Dumontet, S., Vangronsveld, J., 2014. Evaluation of flash and slow pyrolysis applied on heavy metal contaminated Sorghum bicolor shoots resulting from phytoremediation. Biomass Bioenergy 63, 268e279. Christensen, T., Kjeldsen, P., Bjerg, P., Jensen, D., Christensen, J., Baun, A., Heron, G., 2001. Biogeochemistry of landfill leachate plumes. Appl. Geochem. 16, 659e718. Çoruh, S., Elevli, S., Ergun, O., Demir, G., 2013. Assessment of leaching characteristics of heavy metals from industrial leach waste. Int. J. Mineral Process. 123, 165e171. Dai, H., Wei, Y., Zhang, Y., Wei, A., Yang, T., 2012. Subcellular localization of cadmium in hyperaccumulator Populus x canescens. Afr. J. Biotechnol. 11 (16), 3779e3787. De Andrade, L., Barros, L., Echevarria, G., Velho do Amaral, L., Cotta, M., Rossatto, D., Franco, A., 2011. Al-hyperaccumulator Vochysiaceae from the Brazilian Cerrado store aluminum in their chloroplasts without apparent damage. Environ. Exp. Bot. 70, 37e42. Debela, F., Thring, R., Arocena, J., 2012. Immobilization of heavy metals by copyrolysis of contaminated soil with woody biomass. Water, Air, & Soil Pollut.

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