Antizar Et Al. (2004) Bioremediation of Polycyclic Aromatic Hydrocarbon (PAH) - Contaminated Waste Using Composting Approaches

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Critical Reviews in Environmental Science and Technology, 34:249289, 2004

Copyright Taylor & Francis Inc.
ISSN: 1064-3389
DOI: 10.1080/10643380490434119
Bioremediation of Polycyclic Aromatic

Hydrocarbon (PAH)-Contaminated Waste Using
Composting Approaches
Downloaded by [Texas State University - San Marcos] at 17:29 24 April 2013
B. ANTIZAR-LADISLAO, J. M. LOPEZ-REAL, and A. J. BECK

Imperial College London, Wye Campus, Wye, Ashford, Kent, United Kingdom
Environmental pollution and in particular contaminated waste

due to polycyclic aromatic hydrocarbons (PAHs) are of current
environmental concern. In an effort to find solutions, bioremediation techniques have shown promising results in the treatment of
contaminated wastes. Composting approaches as a bioremediation
technology to treat contaminated waste were first reported in the
1980s. This article provides a comprehensive review of research
to date on the use of composting approaches for bioremediation
of PAH-contaminated waste. It critically evaluates the existing research in an effort to assess the relative effectiveness of different
composting approaches, determine optimal composting operation
conditions, and identify the limitations and advantages of using
composting approaches relative to other solutions, and recommends
areas of further research effort.
KEY WORDS: bioremediation, composting, polycyclic aromatic
hydrocarbons
I. INTRODUCTION
Polycyclic aromatic hydrocarbons (PAHs) are a class of organic chemicals
consisting of two or more benzene rings fused in a linear, angular, or cluster
arrangement. Their occurrence in the environment is partly the result of
natural processes including forest fires and volcanic eruptions, and partly
due to anthropogenic activities including the incomplete combustion of fossil
fuels, accidental discharge during transport, use and disposal of petroleum
Address correspondence to Blanca Antizar-Ladislao, Imperial College London, Wye
Campus, Wye, Ashford, Kent, TN25 5AH, United Kingdom. E-mail: b.antizar@imperial.ac.uk
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B. Antizar-Ladislao et al.
products, and incineration of refuse and wastes (Dyke et al., 2003; Fernandez
et al., 2002; Beck et al., 1996). Thus, in areas of high population density and
industrial activity, PAH releases to soils and the wider environment have
led to higher concentrations of these contaminants than would be expected
from natural processes alone. The problem is exacerbated because PAHs
have accumulated in soils, sediments, and animals after their release to the
environment because of their hydrophobicity. This gives cause for concern
because they have been implicated in many adverse effects on wildlife and
human healthmost notably carcinogenesis (Brandt et al., 2002; Brenner
et al., 2002; Yu, 2002; VanBrummelen et al., 1996). As a result, there is a need
to identify and cleanup sites that have become heavily contaminated so that
they do not pose unnecessary risks to health. A further incentive for cleanup
is the presence of many highly contaminated sites on the premises of former
manufactured gas plants (MGP), which were typically found on land close to
the center of towns and cities, land that is often now a valuable capital asset
if it can be cleaned up to a salable condition (Haeseler et al., 1999). Thus, the
potential of using physical, chemical, or biological technologies (or hybrid
combinations of these) to remediate PAH-contaminated sites has received
much attention in recent years (Maini et al., 2000; Zeng et al., 2000; Thomas
and Lester, 1993). Since the 1970s, research on the biological degradation
of PAHs has demonstrated that bacteria, fungi, and algae possess catabolic
abilities that may be used for the bioremediation of PAH-contaminated waste
and water (Eriksson et al., 2003; Dean-Ross et al., 2002; Bhatt et al., 2002; Lei
et al., 2002). Bioremediation technologies such as phytoremediation (Joner
and Leyval, 2003; Mougin, 2002), land farming (Picado et al., 2001), and
composting (Sasek et al., 2003b; Canet et al., 2001; Potter et al., 1999) have
been used for biodegradation of PAH-contaminated wastes.
Composting of soils contaminated with hazardous materials is still an
emerging ex situ biotreatment technology. However, interest is increasing and
it has been shown to be effective in biodegrading PAHs (Sasek et al., 2003b;
Canet et al., 2001; Potter et al., 1999), chlorophenols (Laine and Jrgensen,
1997), polychlorinated biphenyls (Michel et al., 2001), explosives (Gunderson
et al., 1997), and petroleum hydrocarbons (Jrgensen et al., 2000; Namkoong
et al., 2002) at the laboratory and/or field scales. There are several reports
on soil compostingbioremediation using a variety of composting systems
such as open-air systems, which include mechanically turned windrow and
static aerated piles, and enclosed systems, which include modular containers
and tunnels or buildings (Potter et al., 1999; Jrgensen et al., 2000; Sasek
et al., 2003b). The use of composted materials to ameliorate contaminated
waste has recently been reviewed by Semple et al. (2001), Buyuksonmez
et al. (1999) have reviewed the occurrence, degradation and fate of pesticides
during composting, and Ro et al. (1998) have reviewed the use of composting
in the bioremediation of explosives-contaminated waste. However, as yet
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Bioremediation of Polycyclic Aromatic Hydrocarbon
there is no single source that reviews the success of composting in treatment

of PAH-contaminated wasteshence, the purpose of this article.
Our primary objective is to provide a comprehensive review of research
to date on the use of composting approaches for bioremediation of PAHcontaminated waste. In doing so we critically evaluate the existing research
in an effort to determine optimal composting operation conditions, assess
the relative effectiveness of different composting approaches, identify the
limitations and advantages of using composting approaches relative to other
solutions, and recommend areas of further research effort.
II. BIOREMEDIATION OF POLYCYCLIC AROMATIC

HYDROCARBONS
A. Regulatory Considerations
Regulatory objectives and priorities relating to the clean up of PAHcontaminated soils vary by country. In the United Kingdom there is an action level of 500 mg PAH kg1 air-dried soil for land used for recreation
and 10,000 mg PAH kg1 air-dried soil for land with a hard covering. The
United Kingdom takes the view that land should be cleaned to make it fit for
its intended use. By contrast, the United States and the Netherlands adopt
a multifunctional approach whereby land must be fit for any use. Consequently, soil quality limits are much lower than in the United Kingdom; for
example, the Netherlands has an action level of 40 mg PAH kg1 air-dried
soil (Wilson and Jones, 1992). Table 1 shows trigger concentrations of PAHs
given by the Interdepartmental Committee on the Redevelopment of Contaminated Land (ICRCL, 1987) in the United Kingdom, and Table 2 shows
the optimum and action concentrations for soil, sediments, and groundwater adopted by the Dutch List. In addition, the United States, among other
countries, has international obligations under the United Nations (UN) ECE
Persistent Organic Pollutants (POPs) Protocol (UN ECE POPs, 2003) to report
releases of four PAHs. As compared with the existing procedure in the United
States, Europe has more uniform criteria, established as the Dutch List.
TABLE 1. Interdepartmental Committee on the Redevelopment of Contaminated Land
(ICRCL) 59/83 Trigger Concentrations
Trigger values
(mg kg1 air-dried soil)
Contaminant
Polyaromatic
hydrocarbonsa,b
a Used
b See
Planned use
Threshold
Action
Domestic gardens, allotments, play areas

Landscaped areas, buildings, hard cover
5
1000
500
10,000
as a marker for coal tar. See CIRIA (1988, Annex 1).

CIRIA (1988) for details of analytical methods.
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TABLE 2. The New Dutch List
Soil sediment
(mg kg1 dry weight)
PAH
Anthracene
Benzo[a]pyrene
Fluoranthrene
Naphthalene
Phenanthrene
Benzo[a]anthracene
Chrysene
Benzo[a]fluoranthrene
Benzo[k]fluoranthrene
Benzo[g,h,i]perylene
Indeno[1,2,3-cd]pyrene
Total PAH a,b
Groundwater
(g L1 )
Optimum
Action
Optimum
Action
40
0.02
0.001
0.005
0.1
0.03
0.002
0.002
0.003
0.001
0.0002
0.0004
5
0.5
1
70
5
0.5
0.05
0.5
0.05
0.05
0.05
Note. From the Ministry of Housing, Spatial Planning and Environment, Directorate-General
for Environmental Protection, Department of Soil Protection (625), the Hague, the Netherlands.
a PAH (total of 10) is the total of anthracene, benzo[a]anthracene, benzo[a]fluoranthrene,
benzo[g,h,i]perylene, benzo[k]fluoranthrene, chrysene, fluoranthrene, indeno[1,2,3cd]pyrene, naphthalene, phenanthrene.
b If contamination is due to only one compound, the value used is the intervention value
of that compound. Where there are two or more compounds the value for the total of
these compounds applies.
Regulatory objectives and priorities relating to composting of biodegradable waste also vary by country. In the United Kingdom, composting is classified as a waste recovery operation under the Waste Framework Directive.
In addition, composting of waste is a vital component of meeting the Waste
Strategy 2000 (DETR, 2000) targets for recycling and composting set at 25%
by 2005, 30% by 2010, and 33% by 2015. In Europe, the European Community (EC) Landfill Directive 1999 (EC, 1999) sets a target for reduction
of biodegradable waste to landfill of 25% by 2010, 50% by 2013, and 65%
by 2020. In recent years an increasing tendency to compost green (garden)
waste has become apparent (Slater and Frederickson, 2001). In relation to
the longer term requirements of the EC Landfill Directive, composting of
kitchen waste, green waste, and in general biodegradable organic waste,
which might include contaminated soil, will probably have an important
role to play (Burnley, 2001; Phillips et al., 2001). Recent European Union
(EU) regulation (EU Animal By-Products Regulation, 2003) requires that the
composting of catering waste containing meat must take place in a closed
composting reactor operated at least 70 C for 1 h. This means that catering
waste containing meat cannot be treated in an open windrow, except as a
second stage after it has first been treated in a closed reactor.
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FIGURE 1. Regulatory considerations for bioremediation of PAH-contaminated soil using

composting approaches.
Figure 1 summarizes the regulations to consider at the different stages

of the application of composting-bioremediation to PAH-contaminated waste.
A indicates regulations setting up an action concentration of PAHs present
in soil, that is, the New Dutch List. B indicates regulations dealing with
organic wastes to compost, that is, the EC Landfill Directive. C indicates
regulations to the specific operational parameters required for composting
of catering waste or waste where animal by-products are present, that is, the
EU Animal By-Products Regulation.
B. PAHs in the Environment

PAHs are present in contaminated soils and sediments at varying concentrations depending on the nature of the industrial sites and sources of contamination to the environment (Mueller et al., 1996). Typical concentrations
of PAHs in contaminated soils from creosote production, wood preserving,
MGP, and petrochemical sites are given in Table 3. Total concentration of
PAHs at wood preserving sites (WPs) can be high when compared to the
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TABLE 3. Examples of PAH Concentrations in Contaminated Soils from Industrial Sites

PAH concentration (mg kg1 soil) in PAH-contaminated
soils/sediment
PAH
Naphthalene
Acenaphthylene
Acenaphthene
Fluorene
Phenanthrene
Anthracene
Fluoranthene
Pyrene
Benzo[a]anthracene
Chrysene
Benzo[b]fluoranthene/
benzo[k]fluoranthene
Benzo[a]pyrene
Dibenzo[a,h]anthracene
PAH
CP
1131
33
650
1595
334
682
642
614
WP
500
7100
1900
6400
2500
2200
1000
300
1000
560
60
5863
<30
<30
23,600
SFMn
GW
PC
MGP
SFMs
186
10
6
46
16
84
6
62
51
20
21
48
673
79
705
32
266
2
419
10
21
5
16
352
224
64
27
106
46
3815
974
6494
3651
21,319
2497
7902
1440
10,053
9481
1670
2392
2271
2
225
379
156
2174
491
317
345
498
43
87
156
53
137
99
33
536
120
192
92
207
2451
15
70,633
7337
821
12
496
305
513
COGEMA
28
2
4
51
58
195
173
88
52
99
Note. CP, creosote production site (Ellis et al., 1991); WP, wood preserving site (Ahtiainen et al., 2002);
SFMn, Superfund site Minnesota, (U.S. EPA, 1995a); GW, gas works site (Bewley et al., 1989); PC, petrochemical site (Juhasz and Naidu, 2000); MGP, manufacturing gas plant site (Birnstingl, 1997); SFSMs,
Superfund site, Mississippi (U.S. EPA, 1995b); COGEMA, French MGP site (Bogan et al., 1999).
concentration of PAHs at MGP sites. In addition, MGP are well known to

have concentrated and diffuse areas of contamination (Birnstingl, 1997) .For
example, in the sites mentioned in Table 3, PAHWPs is 67 times higher than
PAHMGPs . The nature of different sites will also influence the concentration of particular PAHs associated with contaminated soils. For example, in
a soil from a WP site, Ahtiainen et al. (2002) reported a total PAH concentration of 23,600 mg kg1 , and benzo[a]pyrene comprised 0.3% of the total
PAH content of the soil, but indeno[1,2,3-cd]pyrene was not detected. At an
MGP site, benzo[a]pyrene and indeno[1,2,3-cd]pyrene comprised 1.3% and
2.8%, respectively, of the total PAH content of the soil, and fluoranthene and
dibenzo[a,h]anthracene comprised 30% and 33%, respectively (Bewley et al.,
1989). These differences in PAH concentrations in soils from different sources
should be considered when optimization of composting conditions need to
be achieved for maximum PAH removal.
C. Physicochemical Properties of PAHs

Biodegradation of different PAHs, regardless of the bioremediation technology applied, occurs to different extents and at variable rates depending on
their physicochemical properties, waste characteristics, and environmental
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conditions. Table 4 outlines some physicochemical properties of the 16 U.S.

Environmental Protection Agency (EPA) regulated PAHs. Among the most
important physicochemical properties to be considered during biodegradation processes appears to be water solubility. PAH water solubility decreases
(and hydrophobicity increases) with an increase in number of fused benzene rings, and with angularity (Harvey, 1997). Thus, high-molecular-weight
PAHs are more slowly desorbed and dissolved than low-molecular-weight
PAHs and therefore are less available for microbial degradation (Cerniglia,
1992). In addition, volatility is an important physicochemical property, especially during elevated temperatures that occur in composting (>50 C), which
facilitates volatilization of PAHs. Volatilization generally decreases with an increasing number of fused rings. The number of aromatic rings, structure of
the PAHs, and resonance energy might also affect the degradation rate of
PAHs (Kastner and Mahro, 1996).
D. Biodegradability of PAHs
The recalcitrance of PAHs to microbial degradation generally increases with
their molecular weight and their octanolwater partitioning coefficient (log
K ow ). In addition, many high-molecular-weight PAHs are only degraded with
difficulty or not at all, due to their low water solubility, high resonance energy, and toxicity (Cerniglia, 1992). The microbial degradation of PAHs has
been reviewed (Juhasz and Naidu, 2000; Cerniglia, 1992). There are numerous genera of microorganisms, some of them present during composting
processes, that have been observed to degrade PAHs (in der Wiesche et al.,
2003; Bhatt et al., 2002; Dean-Ross et al., 2002; Canet et al., 1999), but mechanisms of metabolism vary (Cerniglia, 1992, 1997) (Table 5). The different
pathways used by bacteria, mammals, and fungi in the metabolism of PAHs
are summarized in Figure 2.
Bacteria initially oxidize PAHs by incorporating both atoms of molecular oxygen into the PAH nucleus to form cis-dihydrodiols (dioxygenase).
The initial ring oxidation is usually the rate-limiting step. cis-Dihydrodiols
are then rearomatized through a cis-dihydrodiol dehydrogenase to yield a
dihydroxylated derivative. Further oxidation of the cis-dihydrodiols leads to
the formation of catechols, which are substrates for other dioxygenases that
bring about enzymatic cleavage of the aromatic ring. Catechol can be oxidized via two pathways. The ortho pathway involves cleavage of the bond
between carbon atoms of the two hydroxyl groups. The meta pathway involves cleavage of the bond between a carbon atom with a hydroxyl group
and the adjacent carbon atom with a hydroxyl group. Ring cleavage results
in the production of sucinic, fumaric, pyruvic, and acetic acids and aldehydes, all of which are utilized by the microorganisms for the synthesis of
cellular constituents and energy. A by-product of these reactions is the production of carbon dioxide and water. PAHs such as phenanthrene, pyrene,
256
128
152
154
166
178
178
202
202
228
Naphthalene
Acenaphthylene
Acenaphthene
Fluorene
Anthracene
Phenanthrene
Fluoranthene
Pyrene
Benzo[a]anthracene
1.3 105
1.2 106
1.8 102
2.54 101
8.86 104
7.3 106
7.2 103
1.3 103
C18 H20
C16 H10
7.2 104
393
425 5.615.70
160.7
4.90
4.90
150.4
383
108.8
C16 H10
4.45
338
100.5
C14 H10
2.0 104
0.07
547 4.464.76
264
C14 H10
1.9 103
2.7 104
7.4 105
8.86 102
4.18
2.4 104
5.96 101
1.2 102
5.96 101
3.70
4.5 103
10.9
2.313
2.099
2.184
1.924
1.325
1.325
Solubility Vapor pressure Henry constant Resonance

(mmol L1 ) (Pa at 25 C) (atm m3 mol1 ) energy (eV)
279 3.925.07 2.9 102
270
115116 294
96.2
C12 H10
log
K ow
218 3.004.00 2.4 101
b.p.
( C)
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C13 H10
95
C12 H8
m.p.
( C)
81
Structure
C10 H8
Molecular
weight Formula
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TABLE 4. Structure and Physico-Chemical Properties of 16 U.S. EPA Regulated PAHs
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252
278
276
276
Benzo[b]fluoranthene
Benzo[k]fluoranthene
Benzo[a]pyrene
Dibenzo[a,h]Anthracene
536
542
178.1
266.6
163
278.3
C20 H12
C20 H12
C22 H14
C22 H12
C22 H12
C20 H12
535
496
7.23
7.66
5.806.50
6.04
6.84
6.57
5.61
6 108
2 105
3.7 1010
1.8 106
8.4 107
1.5 105
5.7 107
1.3 105
2 107
2 109
2.7 107
6.7 107
3.098
2.958
2.579
2.477
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253.8
C18 H20
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Note. From ISPAC (2003).
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TABLE 5. Microorganisms Degrading PAHs

PAH
Naphthalene
Organism
Bacteria: Acinetobacter calcoaceticus, Alcaligenes denitricans,
Brevundimonas vesicularis, Burkholderia cepacia, Comamonas
testosteroni, Corynebacterium renale, Cycloclasticus sp., Neptunomonas
naphthovorans, Moraxella sp., Mycobacterium sp., Pseudomonas sp.,
P. Fuorescens, P. marginalis, P. putida, P. saccharophila, P. stutzeri,
Sphingomonas paucimobilis, Streptomyces sp., Rhodococcus sp.
Fungi: Absidia glauca, Aspergillus niger, Basidiobolus ranarum, Candida
utilis, Choanephora campincta, Circinella sp., Claviceps paspali,
Cokeromyces poitrassi, Conidiobolus gonimodes, C. bainieri, C. elegans,
C. japonica, Emericellopsis sp., Epicoccum nigrum, Gilbertella
persicaria, Gliocladium sp., Helicostylum piriforme, Hyphochytrium
catenoides, Linderina pennispora, Mucor hiemalis, Neurospora crassa,
Panaeolus cambodginensis, Panaeolus subbalteatus, Penicillium
chrysogenum, Pestalotia sp., Phlyctochytrium reinboldtae, Phycomyes
blakesleeanus, Phytophthora cinnamomi, Psilocybe cubensis, Psilocybe
strictipes, Psilocybe stuntzii, Psilocybe subaeruginascens, Rhizophlyctis
harderi, Rhizophlyctis rosea, Rhizopus oryzae, Rhizopus stolonifer,
S. cervisiae, Saprolegnia parasitica, Smittium culicis, Smittium
culisetae, Smittium simulii, Sordaria micola, Syncephalastrum
racemosum, Thamnidium anomalum, Zygorhynchus moelleri
Acenaphthylene
Acenaphthene
Bacteria: Alcaligenes eutrophus, Alcaligenes paradoxus, Beijerinckia sp.,
Bu. cepacia, Cycloclasticus sp., Neptunomonas naphthovorans,
Pseudomonas sp., P. fluorescens, P. putida
Fungi:Cunninghamella elegans, T. versicolor
Fluorene
Fungi: Cunninghamella elegans, Phanerochaete chrysosporium,
Pleurotus ostreatus
Anthracene
Bacteria: Acinetobacter calcoaceticus, Arthrobacter sp., Beijerinckia sp.,
Bu. cepacia, Comamonas testosteroni, Cycloclasticus pugetii,
Cycloclasticus sp., Flavobacterium sp., Gordona sp., Mycobacterium
sp., P. fluorescens, P. marginalis, P. putida, Rhodococcus sp.,
Sphingomonas sp., Sp. paucimobilis, Sp. Yanoikuyae
Fungi: Bjerkandera sp., Bjerkandera adjusta, Ceriporiopsis subvermispora,
Cladosporium herbarum, Coriolopsis polyzona, Curvularia lunata,
Curvularia tuberculata, Cryphonectria parasitica, Cylindrocladium
simplex, C. elegans, Daedaela quercina, Drechslera spicifera,
Flamulina velutipes, Fusarium moniliforme, Laetiporus sulphureus,
Marasmiellus sp., Monosporium olivaceum, Oxysporus sp., Penicullium
sp., Pleurotus ostreatus, P. chrysosporium, P. laevis, Ramaria sp.,
Rhizopus arrizus, R. solani, Trametes versicolor, Verticillium lecanii
Phenanthrene
Bacteria: Acidovorax delaeldii, Acinetobacter calcoaceticus, Aci. sp.,
Aeromonas sp., A. faecalis, A. denitricans, Agrobacterium sp.,
Arthrobacter polychromogenes, Bacillus sp., Beijerinckia sp.,
Burkholderia sp., Comamonas testosteroni, Cycloclasticus pugetii,
Cycloclasticus sp., Flavobacterium gondwanense, Flavobacterium sp.,
Halomonas meridiana, Micrococcus sp., Mycobacterium sp., Nocardia
sp., Nocardioides sp., P. aeruginosa, P. fluorescens, P. putida,
P. saccharophila, P. stutzeri, Rhodococcus sp., Rhodotorula glutinis,
Sp. paucimobilis, Streptomyces sp., S. griseus, Stenotrophomonas
maltophilia, Gordona sp., Sphingomonas sp., Sp. yanoikuyae,
Sphingomonas sp., Pseudomonas sp., Vibrio sp.
(Continued on next page)
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TABLE 5. Microorganisms Degrading PAHs (Continued)

PAH
Phenanthrene
Fluoranthene
Pyrene
Benzo[a]anthracene
Chrysene
Benzo[a]pyrene
Organism
Fungi: Agrocybe aegerita, Aspergillus niger, Bjerkandera adjusta,
Curvularia lunata, Curvularia tuberculata, Cylindrocladium
simplex, C. elegans, Daedaela quercina, Flamulina velutipes,
Kuehneromyces mutabilis, Laetiporus sulphureus, marasmiellus
sp., Monosporium olivaceum, P. chrysosporium, P. laevis,
Penicullium sp., Pleurotus ostreatus, Syncephalastrum
racemosum, Trametes versicolor
Bacteria: Acinetobacter calcoaceticus, Acidovorax delaeldii,
Alcaligenes denitrificans, Burkholderia cepacia, Flavobacterium
sp., Gordona sp., Mycobacterium sp., Pseudomonas sp.,
P. putida, Rhodococcus sp., Sphingomonas sp., Sp. paucimobilis,
Stenotrophomonas maltophilia, P. saccharophilia,
Pasteurella sp.
Fungi: Aspergillus terreus, Beauveria alba, Bjerkandera adjusta,
Cryptococcus albidus, Cicinobolus cesatii, C. elegans,
C. blackesleeana, C. echinulata, Daedaela quercina, Flamulina
velutipes, Laetiporus sulphureus, Marasmiellus sp., Mortierella
ramanniana, Penicullium sp., Pestalotia palmarum, Pleurotus
ostreatus, Rhizopus arrhizus, Sporormiella australis
Bacteria: Acinetobacter calcoaceticus, Alcaligenes denitrificans,
Burkholderia cepacia, Flavobacterium sp., Gordona sp.,
Mycobacterium sp., P. putida, P. saccharophilia, Rhodococcus
sp., Sphingomonas sp., Sp. paucimobilis, Stenotrophomonas
maltophilia
Fungi: Agrocybe aegerita, Bjerkandera adjusta, C. elegans,
Dichomitus squalens, Flammulina velutipe, Kuehneromyces
mutabilis, Laetiporus sulphureus, Phanerochaete chrysosporium,
Penicillium sp., P. janthinellum, P. glabrum, Pleurotus ostreatus,
Pleurotus sp., Syncephalastrum racemosum, Trammetes
versicolor
Bacteria: Agrobacterium sp., Alcaligenes denitrificans, Bacillus sp.,
Beijerinckia sp., Burkholderia cepacia, Burkholderia sp.,
Pseudomonas sp., P. putida, P. Saccharophilia, Sphingomonas
sp., Sp. paucimobilis, Sp. yanoikuyae, Stenotrophomonas
maltophilia.
Fungi: C. elegans, P. laevis, P. janthinellum, Trametes versicolor.
Bacteria: Acinetobacter calcoaceticus, Agrobacterium sp., Bacillus
sp., Burkholderia sp., Pseudomonas sp., P. marginalis,
P. saccharophilia, Rhodococcus sp., Sphingomonas sp.,
Sp. paucimobilis, Stenotrophomonas maltophilia
Fungi: Penicillium sp., P. janthinellum, Syncephalastrum
racemosus
Bacteria: Alcaligenes denitrificans, Sp. paucimobilis
Bacteria: Beijerinckia sp., Mycobacterium sp., Pseudomonas

NCIB 9816, Sphingomonas paucimobilis
Fungi: Chrysosporium pannorum, Cunninghamella elegans,
Phanerochaete chrysosporium, Stropharia coronilla
Dibenzo[a,h]Anthracene Bacteria: Sp. paucimobilis, Stenotrophomonas maltophilia.
Fungi: Trametes versicolor, P. janthinellum.
Indeno[1,2,3-c,d]pyrene
Note. Adapted from Cerniglia (1992, 1997) and Kanaly and Harayama (2000).
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FIGURE 2. Different pathways used by bacteria, mammals, and fungi in the metabolism of
PAHs.
and benzo[a]pyrene have complex fused ring structures so bacteria metabolize them at multiple sites to form isomeric cis-dihydrodiols (van Herwijnen
et al., 2003; Juhasz and Naidu, 2000; Kanaly and Haramaya, 2000).
Mammals incorporate one atom of molecular oxygen into the PAH to
form arene oxides that can either undergo enzymatic hydration by epoxide
hydrolase to form trans-dihydrodiols or else rearrange nonenzymatically to
form phenols (Lei et al., 2002). Exposure to PAH-contaminated waste increases the risk of cancer in mammals. The carcenogenicity of PAHs is associated with the complexity of the molecule, and with metabolic activation to
reactive diol epoxide intermediates and their subsequent covalent binding to
critical targets in DNA (Bostrom et al., 2002).
A diverse group of ligninolytic and nonligninolytic fungi have the ability
to oxidize PAHs. In contrast to bacteria, nonligninolytic fungi and prokaryotic
algae (cyanobacteria) metabolize PAHs in pathways that are generally similar
to those used by mammalian enzyme systems (Cerniglia, 1992). Enzymes
from both fungal and mammalian systems oxidize PAHs to arene oxides by
the cytochrome P-450 enzyme system. Then the oxides can isomerize to
yield phenols or undergo enzymatic hydration to yield trans-dihydrodiols.
Lignin degradation is carried out by mechanisms related to the production
of highly reactive intermediates by enzymes, such as lignin peroxidase and
manganese-dependent peroxidase. Most degradative mechanisms reported
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are cometabolic, where an alternate carbon source is utilized for energy

and growth, while the PAH is transformed as a consequence of this growth
(Cerniglia, 1997; Mueller et al., 1996).
While there are many organisms capable of degrading the lowmolecular-weight (LMW: two- and three-ring) PAHs, relatively few genera
have been observed to degrade high molecular weight (HMW: four-,
five-, and six-ring) PAHs. There are still very few reports of bacteria outside the nocardioform actinomycetes group capable of growing on highmolecular-weight PAHs (Kastner et al., 1994); however, a variety of nonactinomycete bacteria (Pseudomonas putida, P. aeruginosa, Flavobacterium
sp., Burkholderia cepacia) have also been reported to metabolize fluoranthene, pyrene, chrysene, and benzo[a]anthracene. Currently, there is only limited information regarding the bacterial biodegradation of five- and six-ring
PAHs in environmental samples and pure or mixed cultures. Benzo[a]pyrene
biodegradation by pure and mixed cultures of bacteria has been shown to
occur, although bacteria capable of utilizing benzo[a]pyrene as a sole source
of carbon and energy have not been demonstrated yet.
Numerous genera of fungi with the ability to oxidize naphthalene have
been identified. Most degradative mechanisms reported are cometabolic. The
white-rot fungus Phanerochaete chrysosporium has been reported to mineralize phenanthrene, fluorine, fluoranthene, anthracene, and pyrene in nutrientlimited cultures (Steffen et al., 2003; Bumpus, 1989). Other white-rot fungi,
such as Trametes versicolor, Bjerkandera sp., and Pleurotus ostreatus, have
been shown to metabolize PAHs such as phenanthrene, anthracene, pyrene,
benzo[a]pyrene, and fluorine (Cerniglia, 1997). The basidiomycete Pleurotus
ostreatus can degrade a wide range of PAHs, including anthracene, phenanthrene, pyrene, fluorene, and benzo[a]pyrene (Bezalel et al., 1997).
III. COMPOSTING APPROACHES

Composting is an aerobic process where organic materials are biologically decomposed. Heat produced during this process leads to elevations in temperature characteristic of composting. Composting processes typically comprise
four major microbiological stages in relation to temperature: mesophilic, thermophilic, cooling, and maturation, during which the structure of the microbial
community also changes (Bolta et al., 2003; Liang et al., 2003; VanderGheynst
and Lei, 2003).
Composting systems are generally divided into three categories:
windrow, static pile, and in-vessel. In the windrow approach, the solid waste
mixtures are composted in long rows and aerated by convective air movement and diffusion. The mixtures are mechanically turned periodically to
expose the organic matter to ambient oxygen. This approach to composting
leads to a characteristic fluctuating temperature regime, as core temperatures
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FIGURE 3. Variation of compost core temperature with the windrow system.
will fall on turning due to introduction of cooler masses of air and release
of entrapped heated air, followed by a subsequent rise in temperature and
a new temperature peak as maximum microbial activity resumes. Over time
the peak temperatures fall as the level of substrates declines. Recording of
temperature fluctuations results in the characteristic jagged tooth pattern of
windrowing (Figure 3). Windrowing is a simple mechanical system with no
effective control of either oxygen or temperature levels within the organic
mass undergoing decomposition. The technique, though popular commercially due to its ease of implementation and relative low cost of installation, has been criticized microbiologically since considerable periods of time
elapse when either oxygen or temperature or both will become limiting on
microbial diversity and decomposition.
In the static pile approach, piles of solid waste mixture, often with bulking agents (wood chips, straw) as a matrix improver, are aerated using a
forced aeration system, which is installed under the piles, to maintain a minimum oxygen level throughout the compost mass. The forced aeration system
may be in either the positive or negative modes, which leads to maximum
core temperatures slightly above or below the central point, respectively.
Aeration may be on a timed basis (Epstein, 1997), leading to high core
temperatures and a severely restricted microbial diversity or by temperature feedback control (Finstein et al., 1986). This latter approach is based on
a greater understanding of the microbial ecology involved; for this approach
the control of air flow is dictated by reference to an upper temperature limit
above which the fans blow continuously until heat loss through latent heat
of vaporization of water (seen as steaming) reduces the core temperature to
an acceptable operational level. In both the Epstein (1997) and the Finstein
et al. (1986) static systems there are substantial variations in temperature
throughout the composting mass, and the cooler edges are routinely covered
with a thick layer of finished compost acting as a thermal blanket to ensure
that these edges reach regulatory temperature levels. Although the Finstein
et al. (1986) system allows for the control of maximum core temperature,
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and in theory supplies excess of oxygen for decomposition, both static approaches suffer from this gradation of temperature (and oxygen) throughout
the organic waste mass. In static systems active composting will occur over a
3- to 4-week period depending on the nature of the substrate being processed. This active phase is often followed by a 2- to 3-month period of
maturation.
In-vessel composting takes place in a partially or completely enclosed
container in which environmental conditions can be controlled. Enclosed
vessels more closely approximate a laboratory incubator, where the organic
mass and its associated microflora should be exposed to a more even temperature profile. Control of temperature in in-vessel systems is usually achieved
through recycling of exhaust gases with intermittent mixing of fresh air to
maintain an agreed temperature (Antizar-Ladislao et al., 2003; Seymour et al.,
2001; Fraser and Lau, 2000). In theory, such systems should allow for excellent control of temperature within the vessel and considerably less variation
of temperature through the composting mass. However, in-vessel systems
have serious limitations in general composting due to limited throughputs
and high installation costs (Das and Keener, 1997). Because of this, they
are often used as a form of pretreatment bioreactor for up to 5 days prior
to conventional composting (usually windrowing), where further decomposition, stabilization, and degassing take place (S asek et al., 2003b; Epstein,
1997; Haug, 1993).
The capability of microorganisms to biodegrade specific contaminants
may not differ significantly from the ambient soil environment to that of composting, but the transformation potential differs for several reasons (Williams
and Keehan, 1993). First, elevated temperatures of composting (>50 C) can
increase the enzyme kinetics involved in biodegradation processes. Second,
co-oxidation may be enhanced due to the range of alternative substrates
present. Third, modifications in the physical and chemical microenvironments within the composting mass can serve to increase the diversity of
the microflora to which the contaminant is exposed. Last, high temperatures
will typically increase the solubility and mass transfer rates of the contaminant, thereby making them more available to metabolism. However, some of
these positive attributes just listed may be in conflict with the overall impact
of temperature and microbial activity.
Over the past two decades there has been much discussion concerning
the appropriate levels of temperature for maximizing decomposition rates in
composting (Walter et al., 1992; Finstein et al., 1989). Reviews of the literature during this period established unequivocally that lower temperatures
favor more efficient composting (Bardos et al., 1989). In practice, however,
composting processes are often subject to regulatory levels of temperature
(e.g., 70 C during 1 h; 55 C during 72 h) in order to meet UK national levels
of pathogen reduction (EC, 2003; DETR, 2000). Emphasis is therefore placed
on pathogen reduction before composting process efficiency. The impact of
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this approach to composting is important when considering organic wastes

that are likely to be nonpathogen- or low-pathogen-containing materials and
whose contaminant substrates are often complex, requiring multiple enzyme
systems for degradation. Research into bioremediation of PAH contaminated
wastes has clearly shown that the most effective degraders of such substrates
belong in the fungal class (Sasek, 2003; Sasek et al., 2003a; Bhatt et al.,
2002; Eggen and Sasek, 2002; Canet et al., 1999, 2001). More specifically, the
majority of these belong to the Basidiomycota, which contain the fungal genera responsible for wood decomposition and hence possess the necessary
complex array of ligninolytic enzymes and nonenzymatic mechanisms for
the degradation of lignin whose basic chemical structures are similar to the
PAHs. Lignin degraders have been shown to be amongst the most potent degraders of PAHs epitomized by Phanaerochaete chrysosopoium (Canet et al.,
1999).
The relationship of these organisms to temperature in the context of
composting as a bioremediation technology therefore becomes critical. Microorganisms exhibit a wide range of temperature adaptation and evolution. Microorganisms are found in the coldest and hottest regions of Earth
(Ferguson et al., 2003; Cavicchioli, 2002; Cowan et al., 2002). At the extreme
ends of this range are a very few highly specialized genera whose wall and
cell membrane modifications allow them to survive and multiply in such
conditions. Figure 4 is a hypothetical diagram relating microbial diversity to
temperature. At specific points on this temperature range not only species
or genera but whole phyla will disappear as their maximum temperature
limits are reached. As has been pointed out in this review, current composting approaches and technologies tend to emphasize the higher end of the
range (>70 C) in order to meet regulatory requirements for pathogen control.
Such temperatures, which will be easily reached in uncontrolled operations,
such as windrowing (Epstein, 1997), severely inhibit the microbial diversity
and hence enzymatic potential of the system. Those organisms of particular
interest in PAH degradation will be eliminated above approximately 45 C.
FIGURE 4. Microbial diversity and temperature.
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Some speculation has been given to the temperature range at which microbial diversity is maximized. What little research has been done suggests
that the range between 40 and 45 C allows for such maximum diversity to
be expressed for both, bacteria, actinomycetes, and fungi (Antizar-Ladislao
et al., 2003; Walter et al., 1992). It is of interest to note that this range represents an overlap point at which both mesophilic and thermophilic microorganisms will be viable and active. A strategy of temperature control at this
range would seem therefore to be appropriate for the bioremediation of
PAH-contaminated waste.
A. Composting Bioremediation of PAHs-Contaminated Wastes

Composting bioremediation approaches consist of the addition of compost
ingredients to a contaminated waste, where the compost matures in the presence of the contaminated waste. Composting is a relatively new bioremediation approach, so few investigations have been conducted and most of them
have been performed at the laboratory scale. In this review, investigations
on composting bioremediation of PAH-contaminated waste are presented in
a chronological approach, with emphasis on the progressive development
of this technology on the treatment of PAHs either as single pollutants or a
mixture of pollutants.
Crawford et al. (1993) were one of the earliest research groups to report
on a composting bioremediation approach to remove PAHs from a contaminated soil. They reported a controlled composting study in the United States
at the beginning of the 1980s, although they do not give details on the technology, scale, or conditions used. In their study, naphthalene, pyrene, and
benzo[a]anthracene, at initial concentration of 500 mg kg1 , showed varying
degrees of degradation. Naphthalene was completely removed during the
first 7 days of composting; benzo[a]anthracene showed 25% removal during
the first 7 days and 42% total removal over 30 days of composting; pyrene
showed no decrease during the first 7 days of composting and a moderate removal (not percentage removal available) during the last 23 days of
experiment.
Racke and Frink (1989) studied the fate of phenanthrene during sewage
sludge composting at laboratory scale, using radiolabeled phenanthrene
(1.31.6 mg kg1 dry weight), which allowed them to study the fate of
phenanthrene. After 1820 days of composting, between 10 and 11% of
the phenanthrene was degraded and between 15 and 17% of unextractable
phenanthrene metabolites remained in the compost. Unextractable phenanthrene residues formed were either bound to organic matter or incorporated
into microorganisms.
Adenuga et al. (1992) investigated the biodegradation of pyrene
(13 mg kg1 ) using in-vessel composting technology at the laboratory scale.
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They amended a spiked soil with composted sewage sludge (40 g mixture),
in quantities ranging from 0 to 50% dry weight basis, and the moisture was
adjusted to 40%. The mixture was placed in amber flasks connected to an
airflow system, in a water bath. Then the temperature was raised from 20 C
by 5 C day1 to 60 C over a period of 21 days, probably trying to stimulate the mesophilic and thermophilic microbiological stages characteristic of
composting. The results from their preliminary studies showed that pyrene
could be degraded in the composting of soil/sludge mixture, although the
rate and extent were not fully described in their study.
Crawford et al. (1993) reported a pilot study to asses the feasibility of
treating two- to four-ring PAH-contaminated soils by composting leaves. The
study used small windrows (about 19 m3 each) of varied ratios of soils from
a former industrial site contaminated with low levels of two- to four-ring
PAHs (about 100 mg kg1 ) and other semivolatile compounds (less than
10 mg kg1 ). During their study, it was observed that temperature, moisture
contents, and ratio of carbon to nitrogen were deficient for optimal composting operation, which indicated the need for larger windrows and increased
process control. Complete removal of these PAHs due to mesophilic degradation, abiotic breakdown, volatilization, or a combination of them, occurred
within 150 days, with most losses during the first 63 days. Crawford et al.
found that the amendment ratio did not affect the extent of degradation of
the PAHs, and appeared to only slightly decrease the rate of degradation of
semivolatile compounds with increasing soil content.
After the completion of these preliminary studies, it was observed that
removal of PAHs from contaminated waste was feasible using composting approaches, although its optimization required adequate oxygen supply, sufficient nutrients, and suitable pH, temperature, and moisture for the microbial
activity. The ratio of PAH-contaminated waste in the composting mixture
needed to be optimized as well to avoid toxicity effects. Attempts to study
the fate of the target PAHs were already observed, with special emphasis on
the entrapment of PAHs in the solid matrix or incorporation into the microbial
biomass.
Civilini (1994) described a laboratory-scale in-vessel composting process
(2 kg mixture) operated at a constant temperature of 45 C during 15 days
following the Finstein approach (Finstein et al., 1996). Civilini (1994) used
municipal solid wastes and fertilizer to clean up PAHs present in creosotecontaminated soil, using an optimal ratio of starting material to creosote
[80% compost, 5% fresh organic matter, 5% fresh organic mater mixed with
fertilizer (NPK 20:50:5), 8% creosote-contaminated soil, 2% fertilizer (NPK
20:50:5), 0.2% creosote] to avoid toxicity effects. Water moisture and airflow were continuously controlled, and samples were taken at days 0, 5,
10, and 15. Civilini investigated the fate of 2- to 4-ring PAHs (naphthalene,
acenaphthene, fluorene, phenanthrene, anthracene, fluoranthene, pyrene,
benzo[a]anthracene, and chrysene). He reported a PAH removal between
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81.63% (benzo[a]anthracene) and 98.63% (fluorene) after 15 days of treatment, although the initial PAH concentration was not given. The author accounted for volatilization in this study, where it was found to be less than
10% of total losses for all the PAHs with the exception of acenaphthene,
where it was found to be approximately 54%. The lack of thermophilic
phase must be considered in this study, since it allows the development
of important degraders of PAHs. Civilini (1994) observed a selection of microorganisms during days 5 to 10, in which only sporogenic aerobic and/or
facultative gram-positive bacteria increased and all other groups decreased,
maybe caused by the reduction of water-soluble PAHs. During days 10 to 15,
a pathogenic problem was identified (Escherichia coli), which confirmed the
unsatisfactory sanitization activity of the process at 45 C (Haug, 1993).
So far, there was not any report on the bioremediation of PAHcontaminated wastes using composting approaches where the mixture was
inoculated. By the mid-1990s, research on biodegradation had shown that
special groups of microorganisms (i.e., white-rot fungi) have a remarkable
potential to degrade PAHs. This fungi naturally degrade lignin to obtain the
cellulose that is inside wood fiber, but the nonspecific mechanisms, which
enable them to degrade lignin, also allow them to degrade a wide range of
pollutants.
McFarland and coworkers (Qiu and McFarland, 1991; McFarland et al.,
1992; McFarland and Qiu, 1995) investigated the removal of PAH in a contaminated soil using fungi. They investigated the fate of benzo[a]pyrene in a silt
loam soil at laboratory scale under an in-vessel-composting regime (reactor
volume, 125 ml) in the presence and absence of Phanerochaete chrysosporium (McFarland and Qiu, 1995). The soil spiked with benzo[a]pyrene
(150 mg kg1 ) was amended with corncobs (primary growth substrate) using
a soil to amendment ratio of 2:1 (dry weight), and the reactor head space was
periodically purged with humidified oxygen to keep aerobic conditions and
water moisture. PAHs were also monitored in HgCl2 (4%)-treated systems to
compare the impact of biotic and abiotic processes. Information on the temperature profile during composting was not given. Samples were taken after
1, 7, 14, 21, 28, 35, 84, 91, and 95 days. This study showed that although the
benzo[a]pyrene appeared to be removed, there was not appreciable difference between the uninoculated and inoculated systems with 65.6 and 62.8%
removal, respectively, after 95 days, although initial rates of removal were
faster in the inoculated incubations (Table 6). During poison test conditions,
removal of benzo[a]pyrene was observed, which suggested the possibility of
irreversible adsorption of benzo[a]pyrene to compost materials. A substantial
concentration of P. chrysosporium (>1 104 CFU g1 ) was found in both
the inoculated and uninoculated compost systems at the end of the treatment period, which explained the similarity in removal in both systems. This
suggests that amending soils with suitable fungal substrates may be sufficient
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TABLE 6. Removal of Benzo[a]pyrene (150 mg kg1 ) in a Silt Loam Soil During 95-Day
Composting Process
Composting,
days
1
7
14
21
28
35
84
91
95
Poisoned control,a
%PAH removal (%SD)
13.6
34.6
41.9
43.0
42.7
47.2
46.8
46.7
49.3
(3.2)
(1.6)
(1.1)
(2.7)
(0.9)
(3.0)
(0.1)
(0.6)
(1.5)
Uninoculated,
%PAH removal (%SD)
21.9
32.3
42.3
49.3
43.5
44.7
61.8
74.3
65.6
(0.1)
(1.9)
(4.5)
(4.6)
(0.7)
(3.5)
(18.1)
(9.1)
(1.2)
Fungal inoculated,b
%PAH removal (%SD)
32.5
44.1
44.6
51.6
60.7
49.5
60.8
58.9
62.8
(0.5)
(13.0)
(0.5)
(6.2)
(3.5)
(0.8)
(8.4)
(3.5)
(5.9)
Note. Adapted from McFarland and Qiu (1995).

ml of 4% mercury chloride.
b Phanerochaete chrysosporium BKMF-1767, from the Utah State University Biotechnology Center.
Inoculated at 39 C.
a3
to encourage the growth of P. chrysosporium populations already present in

soil. Other studies have found that autochthonous microflora, with no introduction of foreign microorganisms, offers the greatest potential for PAH
degradation in contaminated soils when an organic substrate is added (Eggen
and Sasek, 2002; Canet et al., 2001; Eggen and Sveum, 1999).
McFarland and Qiu (1995) reported the loss of benzo[a]pyrene by
first-order kinetics during composting with rate constants of 0.003 day1 ,
0.08 day1 , and 0.06 day1 for poisoned control, fungal unamended, and
fungal amended treatments, respectively. Analysis of gaseous traps indicated
that there was no loss through volatilization or mineralization and that nearly
100% of the benzo[a]pyrene removed was attributable to bound residues as
the parent compound (60%) or as chemical intermediates. Furthermore,
this study highlighted that the presence of the fungi increased the rate of
bound residue formation in the first 30 days of the composting study, where
the rate increased from 0.73 mg kg1 day1 in the absence of the fungi to
1.58 mg kg1 day1 in the presence of the fungi. The authors concluded
that the bioaugmentation of a soil-composting system with P. chrysosporium
was ineffective in degrading benzo[a]pyrene during 95 days of incubation.
However, in terms of locking up the PAH within the compost matrix, this
technique proved very successful, although the long-term implications for
the fate of benzo[a]pyrene are unknown. In addition, when bioaugmentation is practiced the rates of nutrient uptake may increase due to a higher
metabolism of the target contaminant, which might result in nutrient-limiting
conditions resulting in a reduction in microbial activity during long-term soil
treatment.
Similarly, Joyce et al. (1998) investigated the fate of a mixture of
three- and four-ring PAHs (fluorene, anthracene, phenanthrene, pyrene,
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benzo[a]anthracene) under laboratory-scale in-vessel composting conditions

of spiked simulated solid municipal waste, monitored over a 60-day period
(30 days of active composting followed by 30 days of compost maturation).
PAHs were also monitored in HgCl2 (2%)-treated systems to compare the impact of biotic and abiotic processes. The moisture of the compost was kept to
5060% during the first 30 days and to 30% during the last 30 days. The reactors were aerated and/or stirred periodically to maintain aerobic conditions;
temperature was kept at 50 C during the first 30 days and nutrients (0.8%
ammonia nitrogen, 2.3% nitrate, 32.9% urea) were added only during the first
30 days. The results of this study showed that the loss processes occurred during the active phase of composting (first 30 days), when all investigated PAHs
showed some abiotic losses in addition to their biological removal from the
compost. Anthracene, phenanthrene, and pyrene were removed during the
composting process by a combination of biotic and abiotic mechanisms, but
biotic processes were predominant. However, fluorene was readily lost with
abiotic processes accounting for approximately 75% of the removal of this
PAH. Benzo[a]anthracene was resistant to biodegradation throughout composting, but 4050% was lost abiotically. These results suggest that the PAHs
present in the contaminated soil should be carefully screened, considering
the potential for volatilization losses to prevent the process from becoming
an air-stripping process.
Kirchmann and Ewnetu (1998) investigated the biodegradation of
petroleum-based oil wastes in 280-L aerated composting bins using horse
manure as amendment. PAH concentrations in oil sludge and petroleum
residue was 16,800 and 78,500 mg kg1 dry matter respectively. They studied 4 treatments, using 1.8% oil sludge (5400 mg PAH kg1 dry matter), 2.1%
petroleum residues (6100 mg PAH kg1 dry matter), 7.1% petroleum residues
(1000 mg PAH kg1 dry matter) and 7.0% paraffin oil (5300 mg PAH kg1
dry matter). During all the treatments, the temperature increased from 15
to 30 C during the first 1217 days and then decreased to 2225 C. In the
treatment using 7.1% petroleum residues, additions of horse manure were
applied repeatedly, which resulted in repeated increases in the temperature
following each addition. At the start of the composting period, the dominant PAH was naphthalene, which accounted for more than 50% of the
measured PAHs. After 135 days of treatment, Kirchmann and Ewnetu (1998)
reported that the majority of the PAHs were removed with measurable quantities close to or below the detection limit of 0.1 mg kg1 dry matter, but
pyrene, chrysene, and dibenzo[a,h]anthracene were only partially removed
(10%) and thus still present at concentrations of 0.20.8 mg kg1 dry matter.
Thus, Kirchmann and Ewnetu (1998) proved that composting PAH-oil wastes
with horse manure was a suitable environmental approach. Horse manure is
high in lignocellulosic residues, and at the temperatures cited considerable
impact would have expected from the natural mycoflora including members
of the Basidiomycotina.
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Loser et al. (1999) investigated the removal of PAHs during composting of wood containing PAHs with liquid pig manure. They compared the
removal of PAHs in artificially contaminated pine wood (1000 mg phenanthrene kg1 and 1000 mg pyrene kg1 aged by autoclaving) and in real PAHpolluted waste wood (5485 mg PAH kg1 ) in a pilot-scale percolator system.
They inoculated both kinds of wood with 50 g decomposed wood kg1 , and
mixed with 26 L liquid pig manure each. After 31 days of composting treatment, the PAH concentration of the real polluted waste wood was higher
than the concentration of the artificially contaminated pine wood (1470 mg
kg1 to 170 mg kg1 ), which was probably due to the lower bioavailability
of PAHs in the naturally polluted waste and thus slower biodegradation as
compared to the artificially contaminated wood. In addition, in pine wood
93% of phenanthrene and 90% of pyrene were removed, but in naturally
polluted waste wood 86% and 32% of phenanthrene and pyrene, respectively,
were degraded. Another possible reason for the higher residual hydrocarbon
ratio in the naturally polluted soil could be the presence of higher molecular weight PAHs. In the naturally polluted soil two- and three-ring PAHs
were decreased by 75 to 98% and four-ring PAHs by 40 to 45%, but fiveand six-ring PAHs were reduced only by 15%. Loser et al. (1999) concluded
that remediation of PAH-polluted waste wood by means of microorganisms
is possible. Despite using a different PAH-contaminated waste to enhance
composting, Loser et al. (1999) corroborated the suitability of composting
approaches to bioremediate highly PAH-contaminated wastes.
Potter et al. (1999) investigated the degradation of 19 PAHs from a Reilly
soil (creosote manufacturing and wood preserving) during in-vessel composting at the laboratory scale. Each of the test conditions in their experiments
utilized a 70% soil and 30% corncob mixture on a dry weight basis, amended
with cow manure, a modified OECD fertilizer, or activated sludge to adjust
the nutrient content (CNP 100:5:1). Moisture content in each 208-L compost
reactor was adjusted to 3035%, and aerobic conditions were facilitated by
a continuous vertical air flow. Samples for analyses were taken after 7, 14,
28, 56, and 84 days of treatment. Temperatures in all reactors increased to
the upper mesophilic and lower thermophilic ranges (4153 C) during the
first 15 days of treatment and subsequently decreased to ambient temperature, which confirmed aerobic conditions. Compost reactors amended with
sludge sustained higher biomass concentrations than those amended with
cow manure during the first 28 days. In addition, the greatest amount of
biomass appeared between the 15 days of composting corresponding to the
highest temperatures, and thus greatest aerobic activity. Following 56 days
of composting, all compost reactors contained similar amounts of biomass.
Starting concentrations of total PAHs ranged from 1606 to 4,445 mg kg1 , and
final concentrations ranged from 888 to 1556 mg kg1 in the reactors. They
reported that two- to three-ring PAH (small) were removed by an average of
87% in all composters after 84 days of treatment, and four-ring PAH (medium)
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TABLE 7. Small, Medium, and Large PAH Concentrations at the Beginning and
Week 12 of Compost Treatments
Day 0 (mg PAH kg1 ash)
and number of rings
Experimental
conditions
Treatment 1a
Treatment 2b
Treatment 3c
Treatment 4d
Treatment 5e
Average percent
removal
Day 84 (mg PAH kg1 ash)

and number of rings
2+3
(small)
4
(medium)
5+6
(large)
2+3
(small)
4
(medium)
5+6
(large)
1604
2628
1633
962
1524
1093
1245
1110
945
1122
385
444
402
328
497
290
217
303
121
178
86.7%
487
468
406
332
442
61.3%
534
457
483
448
432
14.5%
Note. Adapted from Potter et al. (1999). Values represent the average of duplicate reactors
rounded to the nearest whole number.
a Std nutr + 1% cow manure.
b Modified OECD + 1% cow manure.
c Std nutr + 1% activated sludge.
d Std nutr + 5% activated sludge.
e Std nutr + 5% autoclaved sludge.
were reduced by an average of 61%; however, none of the amendment conditions appeared effective in degrading five- to six-ring PAHs (large) (Table 7).
Most of the concentration reduction occurred within the first 28 days of treatment, with a plateau forming by 56 days, suggesting first-order kinetics. Potter
et al. (1999) reported removal rates of small PAHs ranging from 0.012 day1
(5% activated sludge) to 0.081 day1 (OECD corncobs +1% cow manure),
and removal rates of medium PAHs ranging from 0.004 day1 (5% autoclaved
sludge) to 0.033 day1 (1% cow manure) during the first 28 days. Potter et al.
(1999) results showed a general similarity of final PAH concentrations across
all treatments, which might reflect the recalcitrance of PAHs during the composting bioremediation process, whereby different types of amendments did
not significantly alter the final results.
Guerin (2000) investigated the removal of PAHs during bioremediation
comparing the use of mesophilic composting of soil with conventional land
treatment or land farming, both of them at field scale. This study was of
special importance because it was amongst the first to quantitatively compare the treatment of a highly PAH-polluted soil using a composting approach with a different bioremediation technology. The treated contaminated soil (4.36915 mg kg1 total PAH) had a silty clay texture, visually
contaminated with tar residues, and it was initially blended with commercially based slow-release nutrients. A ratio of green tree waste to manure to
soil of 15:5:80 was used, where green tree waste was fresh (<5 days old)
Eucalyptus spp. leaf and stem waste. The initial concentration of naphthalene was 180300 mg kg1 , phenanthrene was present at 70230 mg kg1 ,
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and benzo[a]pyrene was present at 5871 mg kg1 . The soil compost mixture (130 m3 ) was placed in a windrow 4 m (wide) 24 m (long) 1.5 m
(high) and regularly mixed during 224 days. The moisture was maintained
at 6080% of the water-holding capacity of the treatment soils during the
course of the field program. Soil composting temperature reached maximum
temperature (42 C) after 35 days, while there was no self-heating of the soil
observed in the land treatment. The soil composting process conditions reduced the total PAH concentrations to below the target level given by the
regulatory body (500 mg kg1 ) after 224 days and resulted in a final concentration of 120 mg kg1 , which was lower than that obtained by land treatment. Losses of the low-molecular-weight PAH from volatilization throughout
the treatment period, as determined by a portable flame ionization detector, were not detected. After 224 days of composting treatment, there was
complete removal of the lower molecular weight PAH, 90% degradation of
medium PAHs and 70% degradation of large PAHs. Indeno[1,2,3-cd]pyrene
and benzo[g,h,i]perylene were most resistant to degradation, but approximately 50% of each was lost. Guerin (2000) also investigated changes in
microbial populations during 224 days of composting. Total heterotrophic
populations remained in the range 107 109 per gram soil, showing slightly
higher values in the composting treatment than in the land treatment. Microorganisms capable of utilizing naphthalene (Pseudomonas sp.) remained
in the range of 107 108 /g soil in the first 35 days; however, after 224 days
they considerably decreased as expected due to the reduction in PAH concentration, and in particular naphthalene concentration. In this study, composting proved to be a suitable field-scale environmental technology for
PAH-contaminated soil treatment. Operational parameters such as appropriate amendment and ratio of amendment to soil, oxygen supply, and moisture were critical factors in achieving effective soil composting. Contaminated
soils can vary greatly in distribution of contaminants; thus, special attention
should be given to the appropriate soil preparation previous to composting
treatment.
Ahtiainen et al. (2002) constructed two pilot compost piles (5 m3 )
with soil from a sawmill area heavily contaminated with creosote oil
(23,600 mgPAHs kg1 fresh weight soil) and metals (As, Cr, Cu), and they
added spruce bark chips (mixture rate not available) as a bulking agent. One
pile was inoculated with Mycobacterium, and the other pile was left uninoculated. At the start of composting, most of the PAHs (about 78%) were small
PAHs and hence rather quickly biodegradable. However, the total amount
of PAHs was high enough to cause potential inhibition of biological activity.
From their results, it was observed that soil native microbes were able to
degrade PAHs under composting conditions (Table 8). Furthermore, inoculation of the compost with known PAH degraders did not speed up the process
markedly, as some years before McFarland and Qiu (1995) reported using
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TABLE 8. Concentration and Reduction of PAHs after 17 Months of Composting Treatment in a

Control Pile Compared to Mycobacterium-Inoculated Piles with and without Soil Pretreatment
with Hydrogen Peroxide
Concentration, mg kg1 (%PAH removal)
Compost
Inoculated pile
Mycobacterium
small scale
Control pile
small scale
Soil pretreated with

hydrogen peroxide,
then inoculated pile
Mycobacterium
large scale
PAHs
Initial
After 5 months
After 17 months
2 + 3 rings
4 rings
5 + 6 rings
PAHs
Percent removal
2 + 3 rings
4 rings
5 + 6 rings
PAHs
Percent removal
2 + 3 rings
4 rings
5 + 6 rings
PAHs
Percent removal
18,400
4500
680
23,600
21,020
10,500
440 (35%)
31,960
4750 (74%)
5130
240 (65%)
10,120
57%
169 (96%)
1763 (55%)
517 (58%)
2449
75%
2070 (89%)
3120 (31%)
310 (54%)
5500
77%
1150 (94%)
3100 (31%)
290 (57%)
4540
81%
18,400
4500
680
23,600
4652
3908
1230
9789
Note. Adapted from Ahtiainen et al. (2002).
P. chrysosporium as the inoculate. The increase in certain PAHs was probably

due to the heterogeneous nature of the compost. These results support the
recommendations given by Guerin (2000) regarding the importance of soil
homogenization previous to composting treatment.
Ahtiainen et al. (2002) also investigated the removal of PAHs during
composting on a larger scale, constructing one compost pile (100 m3 ) with
soil from an old wood-preserving facility heavily contaminated with creosote
oil (10,960 mg PAHs kg1 fresh weight soil) and metals (As, Cr2 , Cu). The
soil was pretreated with 50% hydrogen peroxide to speed up the breakdown
of the recalcitrant medium and large PAHs. After the hydrogen peroxide was
completely degraded, a microbial inoculum of PAH degraders, nutrients, and
spruce bark chips were added. The concentration of PAHs is summarized in
Table 8. The results of the Ahtiainen et al. (2002) investigation showed that
by pretreating the soil with hydrogen peroxide, they could achieve similar
removal rates in shorter periods of time of about 96% of small PAHs, and
57% of medium and large PAHs.
B. Treatment of PAHs-Contaminated Wastes With Compost

Compost can also be added to contaminated waste after its maturation for
bioremediation purposes. The composts sustain populations of microorganisms with the potential to degrade a variety of organic contaminants (Mahro
et al., 1994), and they can improve the contaminated soil environment for
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TABLE 9. Degree of Compost Maturity
Degree of
maturity
I
II
III
IV
V
Maximum
temperature ( C)
O2 consumption
(mg g1 )
>60
6050.1
5040.1
4030.1
30
>80
8050
5030
3020
20
Material status
Raw material
Fresh compost
Fresh compost
Mature compost
Mature compost
indigenous or introduced microorganisms by changing the soil pH, nutrient

status, aeration, and moisture retention characteristics.
The maturity of compost, distinguishing mainly among fresh and mature
compost, is important for application purposes (Korner et al., 2003). Usually,
the degree of compost maturity is calculated by the maximum self-heating
temperature in an isolated vessel (suitable for large-scale composting) or respiration activity in the respirometer over a period of 4 days (suitable for labscale composting). Table 9 summarizes the relationship between the degree
of maturity, temperature, and oxygen consumption. In general, both methods are comparable for mature compost, although during early and middle
stages of composting the degree of maturity may vary and a classification
with regard to the material status could be inaccurate.
One major concern of using compost as a bioremediation approach is
the problem of mixing noncontaminated material with contaminated soil, resulting in a greater quantity of contaminated material if the treatment does
not succeed. In fact, dilution has frequently been practiced as a simple means
of getting contaminated sites within regulatory limits. Research in using compost as a bioremediation approach is limited and most of it has been done
on the laboratory scale. A review of investigations on treatment of PAHcontaminated wastes with composts is presented chronologically.
Martens (1982) investigated the changes in concentration of four- to sixring PAHs in fresh compost and in mature compost, which had been allowed
to mature for 90365 days in stacks. Information on the compost technology
and scale was not reported. Martens (1982) found a higher removal of fourto six-ring PAHs in the mature compost than in the fresh compost. Additionally, when these composts were inoculated with 14 C-labeled anthracene,
benzo[a]anthracene, benzo[a]pyrene, and dibenzo[a,h]anthracene, higher levels of mineralization to 14 CO2 in the mature composts were found. Maximal
removal for the four-ring 14 C-labeled PAHs in fresh and mature compost
were 19% and 62% for anthracene, 8% and 58% for benzo[a]anthracene, 0.5%
and 19% for benzo[a]pyrene, and 1.4% and 21% for dibenzo[a,h]anthracene,
respectively, over a 70-day incubation period. From this early study, it
seems that mature compost may be more efficient during treatment of PAHcontaminated wastes.
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Mahro and Kastner (1993) investigated the fate of pyrene in soil and
soilcompost mixtures over a period of 100 days, finding that the degradation of pyrene was enhanced significantly with the addition of mature
compost with >80% pyrene removal after 20 days in the presence and <5%
pyrene removed in the absence of the compost. Further, Kastner et al. (1995)
investigated the impact of mature compost addition on the fate of 14 C-labeled
anthracene in soil at laboratory scale. They used 3-L closed compost reactors
incubated at 21 2 C, continuously aerated with humidified air to keep 60%
moisture. In soilcompost incubations, 23% of the 14 C-labeled anthracene
was mineralized to 14 CO2 and 42% was irreversibly sequestered/bound to
the soilcompost matrix after 103 days (they suggested biogenic binding).
However, in soil-only incubations, approximately 88% of the PAH was recoverable by solvent extraction, with the formation of bound residues being
less significant.
Following this investigation, investigations showed an interest in the understanding of the interaction between the PAHs and the soilcompost matrix on biodegradation and binding mechanisms. Thus, Kastner and Mahro
(1996) continued this work by investigating the degradation of naphthalene
(500 mg kg1 ), phenanthrene (100 mg kg1 ), anthracene (100 mg kg1 ), fluoranthene (100 mg kg1 ), and pyrene (100 mg kg1 ) in soil (Ah horizon of
a para brown soil at a noncontaminated, rural area) and soilcompost (soil
to compost weight ratio 3:1) incubations (25 C, 60% of the water-holding
capacity) at laboratory scale during 100 days. The authors found that the
presence of the compost enhanced the removal of the PAHs and that the
presence of the organic matrix of the compost was essential for enhanced
degradation. In contrast to the pure soil, naphthalene, phenanthrene, and
anthracene were degraded after 20 days in the soilcompost mixture. Fluoranthene and pyrene showed lag phases of 10 days, and then complete
degradation occurred after 35 days. The authors suggested that the stimulating effect on the PAH degradation was a function of the organic matrix of
the compost (humic substances) and the ecological niches of the compost,
which have to be colonized by the respective microorganisms. Kastner and
Mahro (1996) suggested that the addition of compost to contaminated soils
may enhance the biodegradation and bioavailability of PAHs, retain certain
volatile PAHs, and reduce the sorptive effects in soils, which prevents the
compounds from being analytically detected.
Kastner et al. (1999) investigated the fate of [14 C]anthracene
(100 mg kg1 ) in soil (particle size <2 mm) and in soilcompost mixtures
(particle size <4 mm) in a continuously aerated bioreactor at laboratory scale
during 176 days. Soil and compost were mixed at a ratio of 4:1 (dry weight),
with a moisture content adjusted to 60%. They reported complete transformation of the parent compound (anthracene). Although the amount of organic
carbon, which might act as an additional binding substrate, was larger in
the soilcompost mixture (12.7%) than in the native soil (1%), Kastner et al.
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(1999) reported less formation of bound residues from [14 C]anthracene and a
higher mineralization in the soil-compost mixture (67.2% mineralized, 20.7%
transformed into bound residues) than in the native soil (43.8% mineralized,
45.4% transformed into bound residues).
Haderlein et al. (1999) also investigated the impact of humic matter
present in the compost on the mineralization of PAH-contaminated wastes.
They prepared mixtures of 640 g of a silty soil contaminated with aliphatic
hydrocarbons (total petroleum hydrocarbons (TPH) = 40,000 mg kg1 ) and
PAH (630 mg kg1 ), 250 g maple leaves, 750 g alfalfa, and 80 g (w/w) CaCO3
with a moisture content about 50% (w/w), incubated at 55 C, 50% moisture, and aerated either continuously or intermittently during 35 days and
left to mature for 90 days at ambient temperature. This mature composted
PAH-contaminated soil had a pyrene concentration of about 16 mg kg1 .
Then Haderlein et al. (2001) mixed this resulting mature compost with PAHcontaminated soil (80% soil, 20% compost) and left the mixtures for further
composting during 100 days. Abiotic controls contained 0.4% NaN3 . Pyrene
was rapidly mineralized (>50% mineralization after 15 days), whereas mineralization in unamended soil was limited to <3% during the same period.
Abiotic controls had a maximum total mineralization of 0.7% of the initially
added pyrene. Handerlein et al. (2001) focused their efforts to elucidate the
link between PAH mineralization and humic matter based on their preliminary studies, where they found that pyrene mineralization potential during
the composting of contaminated soil increases with time, as does humification. The addition of humic acid (previously extracted from the mature compost) to the soilcompost mixture enhanced pyrene mineralization, reaching
an increase of 18 14% mineralization values at the end of the experiment.
However, the addition of fulvic acid (previously extracted from the mature
compost) inhibited pyrene mineralization, probably due to the high content
on mineral salts remaining in the fulvic acid after extraction and high pH (8
10). From this study, it was corroborated that although humic acid content is
likely not to be the sole reason why the addition of compost stimulates PAH
mineralization, it is a major reason. This is probable due to the increased
bioavailability of contaminants sorbed to mineralhumic acid complexes as
suggested by Laor et al. (1999) and that the sorption of the microorganisms and the PAHs to the colloidal surfaces of humic matter stimulates PAH
biodegradation.
Wischmann and Steinhart (1997) investigated the removal of PAH/N-PAH
in soilcompost mixtures (415 g mixture) as compared to unamended soil
(Ah/Al horizon soil material; 400 g) in a 1-L bioreactor at laboratory scale
for 180 days. Soil and soilcompost mixtures were spiked with a PAH/NPAH standard solution in dichloromethane, resulting in concentrations from
28 to 181 mg kg1 dry weight. The moisture of the mixture was kept to
50% during the length of the treatment. The compost used in this investigation had a degree of maturity V. Abiotic removal of PAH/N-PAH was
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investigated in poisoned controls (soil autoclaved 35 min at 130 C, 1.7 bar,

1 g kg1 HgCl2 ). Samples were taken after 1, 3, 8, 14, 21, 28, 42, 54, 77,
105, and 180 days. In unamended soils, only PAHs up to three-ring PAH
were degraded over 105 days. In the soilcompost mixture there was a lag
phase of 8 days, and then two-ring PAHs were depleted within the following 49 days. Three-ring PAHs were eliminated to <3% during 105 days. Of
the PAHs with more than three-rings, only fluoranthene and pyrene were
almost completely transformed within 105 days. The residual concentration
of benzo[a]anthracene, chrysene and benzo[a]pyrene decreased to 2, 3, and
27% compared to the initial estimated amounts within 180 days of treatment. PAH removal in the poisoned soil showed similar elimination rates to
those in the unamended soil, which suggested abiotic losses predominated
in the unamended soil. Microbiological analyses indicated nonsterile conditions in the poisoned soilcompost mixture, which suggested potential biotic
losses, although they occurred to a lesser extent as compared to the soil
compost mixtures. Longer treatment times were required in the investigation
by Wischmann and Steinhart (1997) than in the investigation by Kastner and
Mahro (1996) for complete removal of two- and three-ring PAHs, although
both investigations used mature compost and not aged soils. These different
results might be explained by the use of different operational parameters and
different origins of soil and compost.
Carlstrom and Tuovinen (2003) investigated the mineralization of
phenanthrene in yard-waste compost in biometers to assess the impact of
the origin of the compost on the mineralization of PAHs. The compost was
collected in four different sampling events from the interior thermophilic
zone and from the exterior mesophilic zone of compost piles between 3 and
6 months old. Replicates of 5 g compost were spiked with phenanthrene
(100 mg kg1 ) and incubated in the dark at 22 2 or 60 2 C during
90 days. Carlstrom and Tuovinen (2003) reported a dominant effect due to
the heterogeneity of the yard-waste samples, which obscured the possible effect of surfactant addition, particle size, and moisture content. Nevertheless,
they reported an effect of the origin of the compost on the mineralization
of phenanthrene. Yard-waste compost samples collected from the 5060 C
thermophilic interior zone and incubated at 60 2 C yielded 12% mineralization, whereas their incubation at 22 2 C resulted in 17% average
mineralization of phenanthrene. These results suggested that phenanthrenemineralizing microorganisms present in the biometer were not thermophiles,
but were able to survive in the thermophilic zone of the compost, probably spore formers. Carlstrom and Tuovinen (2003) were probably the first
to report thermophilic biomineralization of PAHs. Samples collected from an
outer 3040 C mesophilic zone and incubated at 60 2 C showed negligible mineralization, while parallel subsamples incubated at 22 2 C yielded
about 8% mineralization. The removal of phenanthrene was attributed to microbial activity because sterile samples showed negligible 14 CO2 evolution
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(<1%). The rate constants were in the range of 0.0830.033 day1 for the
mineralizable fraction of phenanthrene.
Sasek et al. (2003b) investigated the bioremediation of an MGP site soil
contaminated with PAHs by amending with mushroom compost in mid-phase
I (consisting of wheat straw, chicken manure), and gypsum during 54 days
in a thermally insulated composting chamber (1000 kg mixture) followed
by a further 100 days of maturation in windrows. The total concentration of
12 U.S. EPA PAHs in the soil was 610 mg PAH kg1 dry mass of soil. The
mixture comprised 64% soil and 36% compost on a dry weight basis, and
the mixture moisture was maintained at 64%. Changes in the temperature
of compost were monitored, showing an initial increase of temperature up
to 70 C, and after 12 days of composting the temperature progressively decreased, indicating the different stages of composting. The degradation of
individual PAHs was in the range of 2060% at the end of 54 days of composting, followed by further PAH removal (3780% maximum) after another
100 days of maturation (Table 10). During composting, the outgoing air was
passed through a filter and the filter was analyzed for possible volatilization
losses of PAHs. The amount of PAHs retained in the filter was below detection limits, indicating that the removal of PAHs during composting was
due to either compost microflora metabolism or irreversible sorption to the
compost matrix.
Sasek and coworkers investigated the same composting/compost approach in the treatment of a soil collected from an area of a former tarproducing plant with a total concentration of 16 PAH listed by the U.S. EPA
TABLE 10. Concentration of PAHs in Manufactured Gas Plant Soil (610 mg kg1 )
before and after Composting and after Maturation
mg PAH kg1 dry soil (SD) (%PAH removal)
PAHs
Soilcompost
mixture 0 days
After composting
54 days
Phenanthrene
Anthracene
Fluoranthene
Pyrene
Benzo[a]anthracene
Chrysene
Benzo[a]pyrene
Dibenzo[a,h]anthracene
Indeno[123-cd]pyrene
PAHs
168.9 (14.2)
37.1 (4.6)
87.6 (8.5)
131.7 (3.4)
38.3 (1.3)
32.1 (4.2)
28.5 (6.5)
12.0 (2.2)
38.2 (1.9)
15.1 (1.4)
17.2 (1.1)
23.1 (7.2)
610
49.4
17.7
74.4
88.3
24.2
22.1
14.6
8.6
29.9
11.1
14.2
18.4
Note. Adapted from S asek et al. (2003b).
(2.5)
(1.4)
(6.3)
(4.7)
(2.8)
(2.4)
(2.0)
(1.8)
(3.6)
(4.6)
(1.8)
(1.7)
373
(71%)
(52%)
(15%)
(33%)
(37%)
(31%)
(49%)
(28%)
(22%)
(26%)
(17%)
(20%)
After maturation
54 + 100 days
24.6
1.1
24.8
67.4
11.3
9.5
9.8
4.1
12.6
8.4
12.4
10.8
(2.1)
(0.6)
(1.8)
(2.6)
(2.2)
(1.2)
(1.3)
(3.2)
(3.1)
(2.1)
(3.9)
(2.6)
197
(85%)
(97%)
(72%)
(49%)
(70%)
(70%)
(66%)
(66%)
(67%)
(44%)
(28%)
(53%)
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279

TABLE 11. Concentration of PAHs in Manufactured Gas Plant Soil (2832 mg kg1 )
before and after Composting and after Maturation
mg PAH kg1 dry soil (SD) (%PAH removal)
PAHs
Phenanthrene
Anthracene
Fluoranthene
Pyrene
Benzo[a]anthracene
Chrysene
Benzo[a]pyrene
Benzo[a]perylene
Indeno[123-cd]pyrene
PAHs
Soilcompost
mixture 0 days
187 (21.8)
64 (8.1)
505 (66.9)
356 (42.6)
111 (13.1)
102 (12.2)
146 (16.9)
66.3 (7.5)
125 (14.6)
64.4 (9.0)
81.4 (9.3)
2832
After composting
42 days
68.5
37.2
238
159
68.4
53.3
62.4
31.1
58.2
35.2
39.9
(19.6) (63%)
(20.2) (42%)
(57.0) (53%)
(31.9) (55%)
(19.0) (38%)
(14.2) (48%)
(12.1) (57%)
(7.1) (53%)
(13.1) (53%)
(9.2) (45%)
(8.9) (51%)
851.2
After maturation
42 + 100 days
38.7
12.1
157
114
56.9
43.8
63.0
28.8
59.3
32.0
40.1
(21.4) (79%)
(9.5) (81%)
(85.0) (69%)
(58.6) (68%)
(28.1) (49%)
(21.2) (57%)
(30.4) (57%)
(14.3) (57%)
(27.8) (53%)
(15.6) (50%)
(20.2) (51%)
645.7
Note. Adapted from Cajthaml et al. (2003b).
at a higher concentration of 2832 mg kg1 (Cajthaml et al., 2003). The mixture comprised approximately 47% soil and 53% compost on a dry weight
basis, and the mixture moisture was maintained at 64%. Their results showed
4268% removal of three- to four-ring PAHs, and 3557% removal of five- to
six-ring PAHs after 42 days of composting. However, an additional 100 days
of compost maturation in open air did not result in a further decrease of PAH
concentrations (Table 11).
Lau et al. (2003) investigated the effect of temperature on the biodegradation of naphthalene, phenanthrene, benzo[a]pyrene, and benzo[g,h,i]perylene, using a compost approach in the laboratory. One gram of sterilized garden soil was spiked with 1 ml acetone containing the PAHs and
mixed with straw spent mushroom compost (Pleurotus pulmonarius), which
is a combination of wheat straw, dried blood, horse manure, and and ground
chalk composted together. The moisture content of the mixture was adjusted
to 60%, and the sample was incubated at 4 to 80 C at 200 rpm. Removal
of the PAH under investigation occurred due to biodegradation and sorption mechanisms. Under the experimental conditions of 1% spent mushroom
compost treating 100 mg PAH L1 at room temperature, the removal of PAHs
varied between 82% naphthalene and 59% phenanthrene. The highest sorption removal (46%) was with phenanthrene. Lau et al. (2003) reported an
increase in PAH removal as temperature was increased. At 50 C, three PAHs
but not phenanthrene were completely removed. At 80 C, 5% of the spent
mushroom compost completely degraded the four PAHs at 200 mg kg1 soil.
Thus, this mechanistic study indicates that increasing the temperature during
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bioremediation of PAH-contaminated waste using compost enhance the removal of PAHs, reporting an optimal removal at 80 C.
IV. DISCUSSION AND CONCLUDING REMARKS

Most investigations of the bioremediation of PAH-contaminated waste using composting approaches conducted to date have been at laboratory or
pilot-plant scale. Furthermore, efforts have focused on operational considerations rather the fundamental physical, chemical, and biological mechanisms
that underpin bioremediation-composting technologies. Results from these
investigations were difficult to compare due to the use of different experimental conditions(1) temperature, (2) moisture, (3) soil/waste to amendment/compost ratio, (4) aeration, (5) inoculation versus noninoculation
and to different composting technologies, with windrows versus in-vessel
approach, and different scales of operation: laboratory versus pilot versus
field. Treatment of wastes/soils of different origin with different total PAHs
concentration, distribution of PAHs, bioavailability of PAHs, homogenization,
variations in sources, and types of organic wastes were further complications.
Most of the reviewed investigations, regardless of the composting/
compost approach, technology, or scale used, agreed on the importance of
optimizing the operations conditions during the application of the bioremediation technology. Emphasis is given to temperature, moisture, and
maintenance of aerobic conditions, but particularly to the ratio of waste
to amendment used. The majority of the laboratory-scale investigations on
the use of composting/compost of PAH-contaminated wastes were kept in
the mesophilic or lower thermophilic ranges (Joyce et al., 1998; Kirchmann
and Ewnetu, 1998; Potter et al., 1999), with a few investigations in the thermophilic phase (Carlstrom and Tuovinen, 2003; Lau et al., 2003). Moisture
differed from one investigation to another, ranging from 40% to 80%, although
the majority of the studies emphasized the importance of keeping the moisture of the mixture constant throughout the treatment. Different technologies require different approaches to aeration, but has commonly achieved
by aerating the mixture with humidified air. By doing so, both moisture and
aerobic conditions are maintained. Although some of the earliest work on
composting/compost bioremediation approaches suggested the importance
of finding a suitable mixture ratio between the contaminated waste and the
amendment/compost (Crawford et al., 1993) there are still few reports where
the optimal mixture ratio has been investigated (Civilini, 1994), and in general it does not exceed 80% soil content on a dry weight basis (Haderlein
et al., 1999; Kastner et al., 1999).
Composting of PAH-contaminated wastes has received more attention
than the treatment of PAH-contaminated wastes with compost. One major
concern of using compost as a bioremediation technology is the problem
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of mixing noncontaminated compost with contaminated waste, resulting in

a greater quantity of contaminated material if the treatment does not succeed. Nevertheless, if using compost as a bioremediation technology proves
to achieve similar removal levels of PAHs as using composting as a bioremediation technology, the application of compost bioremediation technology
may offer important operational advantages (i.e., homogenization) during
the application of the technology at a field scale. Consequently, more mechanistic studies comparing the bioremediation of PAH-contaminated waste using composting and compost approaches applying the same technology and
scale at optimal operational conditions are hitherto necessary. If fresh composts are mixed with the soil, a composting process may occur (Cajthaml
et al., 2003; Sasek et al., 2003b), and then a more appropriate definition
would be composting/compost approach rather than composting or compost approach.
Composting and the use of compost have both been successfully applied
to the bioremediation of PAH-contaminated wastes. The main mechanisms of
PAH removal under both bioremediation regimes were mineralization, binding, and volatilization. Mineralization was the more significant of the mechanisms of removal reported in most studies to date. Mineralization of PAHs
may be enhanced by increasing their availability to microbial attack during
bioremediation processes. In order for the pollutants to become available
to microbial attack, desorption from the wastecompost matrix may have to
take place. In terms of composting, increases in temperature may enhance
the rate of PAH desorption from the matrix and thus transfer to the aqueous
phase (Pignatello and Xing, 1996). In terms of compost, enhanced PAH mineralization of PAHs present in soilcompost mixtures may occur due to the
presence of humic matter in the compost matrix. This is supported by studies where either humic acid and/or fulvic acid has been added to a soil with
very low endogenous humic acids/fulvic acids (Bogan and Sullivan, 2003;
Conte et al., 2001; Haderlein et al., 2001; Laor et al., 1999) and an increase
in the bioavaliable fraction has been observed. Another favorable factor inherent to composting approaches is that normally large amounts of organic
matter, considered a major factor in the locking up of organic pollutants,
are added to the system (Brusseau et al., 1991; McFarland and Qiu, 1995).
Thus, by utilizing composting approaches, the bioavailable fraction will ideally be mineralized and the unavailable fraction will be locked up in the
soilcompost matrix, reducing the overall risk. However, the long-term fate
of the locked up organic contaminants remains uncertain.
While more research on comparisons of composting/compost bioremediation technologies versus conventional technologies remains limited, the
investigations reviewed have proved that composting, regardless of the approach used, is a good environmental technology that may be used to remove PAH from contaminated wastes. These bioremediation technologies
have proved to be beneficial for the amelioration of contaminated wastes by
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reducing the concentration of PAHs, which promotes soil sustainability and

soil reuse in contrast to landfill or incineration approaches. Guerin (2000)
reported a higher PAH removal from contaminated soils using composting
approaches compared to conventional landfarming.
Further study should be focused on the optimization of operational parameters at laboratory and pilot scales using naturally PAH-contaminated
wastes, which will facilitate the highest possible removal of the target PAHs.
Complementary studies will be needed to obtain a better understanding of
the different mechanisms contributing to PAH mineralization during composting, and in particular of the interactions between the different components
in the wastecompost matrix together with a greater understanding of the
microflora involved with particular emphasis on the impact of lignocellulytic
fungal decomposers. Commercial industrial-scale operations will undoubtedly benefit from the results obtained from such studies.
ACKNOWLEDGEMENTS
We are grateful to Cleanaway Ltd and London Remade for providing support
for this study through the Entrust scheme.
REFERENCES
Adenuga, A.O., Johnson, J.H., Jr., Cannon, J.N., and Wan, L. Bioremediation of PAHcontaminated soil via in-vessel composting. Water Sci. Technol. 26, 23312334,
1992.
Ahtiainen, J., Valo, R., Jarvinen, M., and Joutti, A. Microbial toxicity tests and chemical
analysis as monitoring parameters at composting of creosote-contaminated soil.
Ecotoxicol Environ Safety 53, 323329, 2002.
Antizar-Ladislao, B., Lopez-Real, J.M., and Beck, A.J. Laboratory studies of the remediation of polycyclic aromatic hydrocarbon contaminated soil by in-vessel
composting. Waste Manage. (3414CSP), 2004.
Bardos, P., and Lopez-Real, J.M. The composting process and susceptible feedstocks,
temperature, microbiology, sanitisation and decomposition. In Compost processes in waste management. Eds. W. Bidlingmaier and P. LHermite, pp. 179
190. Commission of the European Communities. Directorate General, Science,
Research, and Development, E Guyot SA, Belgium, Commission of the European
Communities, 1989.
Beck, A.J., Johnson, D.L., and Jones, K.C. The form and bioavailability of non-ionic
organic chemicals in sewage sludge-amended agricultural soils. Sci. Total Environ. 185(13), 125149, 1996.
Bewley, R., Ellis, B., Theile, P., Viney, I., and Rees, J. Microbial clean up of contaminated soil. Chem. Ind. 23, 778783, 1989.
P1: FZX/Sanjeev
TJ1023-02
EST.cls
March 24, 2004
9:41
283
Bezalel, L., Hadar, Y., and Cerniglia, C.E. Enzymatic mechanism involved in phenanthrene degradation by the white rot fungus Pleurotus ostreatus. Appl. Environ.
Microbiol. 63, 24952501, 1997.
Bhatt, M., Cajthaml, T., and S asek, V. Mycoremediation of PAH-contaminated soil.
Folia Microbiol. 47(3), 255258, 2002.
Birngstingl, J.G.A. An investigation into the bioremediation of polycyclic aromatic hydrocarbons in a manufactured gas plant soil. PhD thesis, University of Lancaster,
Lancaster, UK, 1997.
Bogan, B.W., Lamar, R.T., Burgos, W.D., and Tien, M. Extent of humification of anthracene, fluoranthene and benzo[a]pyrene by Pleurotus ostreatus during growth
in PAH-contaminated soils. Lett. Appl. Microbiol. 28, 250254, 1999.
Bogan, B.W., and Sullivan, W.R. Physicochemical soil parameters affecting sequestration and mycobacterial biodegradation of polycyclic aromatic hydrocarbons
in soil. Chemosphere 52(10), 17171726, 2003.
Bolta, S.V., Mihelic, R., Lobnik, F., and Lestan, D. Microbial community structure
during composting with and without mass inocula. Compost Sci. Util. 11(1),
615, 2003.
Bostrom, C.E., Gerde, P., Hanberg, A., Jernstrom, B., Johansson, C., Kyrklund, T.,
Rannug, A., Tornqvist, M., Victorin, K., and Westerholm, R. Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the
ambient air. Environ. Health Perspect. 110(suppl. 3), 451488, 2002.
Brandt, C.A., Becker, J.M., and Porta, A. Distribution of polycyclic aromatic hydrocarbons in soils and terrestrial biota after a spill of crude oil in Trecate, Italy.
Environ. Toxicol. Chem. 21(8), 16381643, 2002.
Brenner, R.C., Magar, V.S., Ickes, J.A., Abbott, J.E., Stout, S.A., Crecelius, E.A., and
Bingler, L.S. Characterization and fate of PAH-contaminated sediments at the
Wyckoff/Eagle Harbor superfund site. Environ. Sci. Technol. 36(12), 26052613,
2002.
Brusseau, M.L., Jessup, R.E., and Rao, S.C. Nonequilibrium sorption of organic chemicals: Elucidation of rate-limiting processes. Environ. Sci. Technol. 25, 134142,
1991.
Bumpus, J.A. Biodegradation of polycyclic aromatic hydrocarbons by Phanerochaeta
chrysosporium. Appl. Environ. Microbiol. 55(1), 154158, 1989.
Burnley, S. The impact of the European landfill directive on waste management in
the United Kingdom. Resource Conserv. Recy. 32, 349358, 2001.
Buyuksonmez, F., Rynk, R., Hess, T.F., and Bechinski, E. Occurrence, degradation
and fate of pesticides during composting. Part I: Composting, pesticides and
pesticide degradation. Compost Sci. Util. 7(4), 6682, 1999.
Cajthaml, T., Bhatt, M., S asek, V., and Mateju, V. Bioremediation of PAH-contaminated
soil by composting: A case study. Folia Microbiol. 47(6), 696700, 2002.
Canet, R., Birnstingl, J.G., Malcolm, D.G., Lopez-Real, J.M., and Beck, A.J. Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by native microflora and
combinations of white-rot fungi in a coal-tar contaminated soil. Bioresource
Technol. 76, 113117, 2001.
Canet, R., Lopez-Real, J.M., and Beck, A.J. Overview of polycyclic aromatic hydrocarbon biodegradation by white-rot fungi. Land Contam. Reclam. 7(3), 191197,
1999.
P1: FZX/Sanjeev
TJ1023-02
EST.cls
284
March 24, 2004
9:41
Carlstrom, C.J., and Tuovinen, O.H. Mineralization of phenanthrene and fluoranthene

in yardwaste compost. Environ. Pollution. 124(1), 8191, 2003.
Cavicchioli, R. Extremophiles and the search for extraterrestrial life. Astrobiology 2(3),
281292, 2002.
Cerniglia, C.E. Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation
3, 351368, 1992.
Cerniglia, C.E. Fungal Metabolism of polycyclic aromatic hydrocarbons: Past, present
and future applications in bioremediation. J. Ind. Microbiol. Biotechnol. 19, 324
333, 1997.
CIRIA (Construction Industry Research and Information Association). 2003. Town and
Country Planning (Applications) Regulations 1988 (SI 1988/1812) www.ciria.org
Civilini, M. Fate of creosote compounds during composting. Microbiol. Eur. 2, 1624,
1994.
Conte, P., Zena, A., Pilidis, G., and Piccolo, A. Increased retention of polycyclic
aromatic hydrocarbons in soils induced by soil treatment with humic substances.
Environ. Pollut. 112(1), 2731, 2001.
Cowan, D.A., Russell, N.J., Mamais, A., and Sheppard, D.M. Antarctic Dry Valley mineral soils contain unexpectedly high levels of microbial biomass. Extremophiles
6(5), 431436, 2002.
Crawford, S.L., Johnson, G.E., and Goetz, F.E. The potential for bioremediation of
soils containing PAHs by composting. Compost Sci. Util. 1, 4147, 1993.
Das, K., and Keener, H.M. Numerical model for the dynamic simulation of a large
scale composting system. Trans. ASAE 40(4), 11791189, 1997.
Dean-Ross, D., Moody, J., and Cerniglia, C.E. Utilization of mixtures of polycyclic
aromatic hydrocarbons by bacteria isolated from contaminated sediment. FEMS
Microbiol. Ecol. 41(1), 17, 2002.
Department of the Environment, Transport, and Regions. Waste strategy 2000:
England and Wales. London: The Stationary Office, 2000.
Dyke, P.H., Foan, C., and Fiedler, H. PCB and PAH releases from power stations and
waste incineration processes in the UK. Chemosphere 50(4), 469480, 2003.
Eggen, T., and S asek, V. Use of edible and medicinal oyster mushroom [Pleurotus
ostreatus (Jacq.:Fr.)Kumm.] spent compost in remediation of chemically polluted
soils. Int J. Med. Mushrooms 4, 255261, 2002.
Eggen, T., and Sveum, P. Decontamination of aged creosote polluted soil: The influence of temperature, white rot fungus Pleurotus ostreatus, and pre-treatment.
Int. Biodeter. Biodegr. 43(3), 125133, 1999.
Ellis, B., Harold, P., and Kronberg, H. Bioremediation of a creosote contaminated
site. Environ. Technol. 12, 447459, 1991.
Epstein, E. The science of composting. Lancaster: Technomic, 1997.
Eriksson, M., Sodersten, E., Yu, Z.T., Dalhammar, G., and Mohn, W.W. Degradation of
polycyclic aromatic hydrocarbons at low temperature under aerobic and nitratereducing conditions in enrichment cultures from northern soils. Appl. Environ.
Microbiol. 69(1), 275284, 2003.
European Commission. Council directive on the landfill of waste (1999/31/EC). Off.
J. Eur. Commun. L 182/1, 16 July, 1999.
European Commission. EU animal by-products regulations. 2003/31/EEC. EC
No. 1774/2002, 2003.
P1: FZX/Sanjeev
TJ1023-02
EST.cls
March 24, 2004
9:41
285
Ferguson, S.H., Franzmann, P.D., Snape, I., Revill, A.T., Trefry, M.G., and Zappia, L.R.
Effects of temperature on mineralisation of petroleum in contaminated Antarctic
terrestrial sediments. Chemosphere 52(6), 975987, 2003.
Fernandez, P., Grimalt, J.O., and Vilanova, R.M. Atmospheric gas-particle partitioning of polycyclic aromatic hydrocarbons in high mountain regions of Europe.
Environl. Sci. Technol. 36(6), 11621168, 2002.
Finstein, M.S., Miller, F., and Strom, P.F. Waste treatment composting as a controlled
system. Biotechnology, vol. 8. Eds. H. Rehm and G. Reed. 363398, 1986.
Fraser, B.S., and Lau, A.K. The effects of process control strategies on composting
rate and odor emission. Compost Sci. Util. 8(4), 274292, 2000.
Guerin, T.F. The differential removal of aged polycyclic aromatic hydrocarbons from soil during bioremediation. Environ. Sci. Pollut. Res. 7(1), 1926,
2000.
Gunderson, C.A., Kostuk, J.M., Gibbs, M.H., Napolitano, G.E., Wicker, L.F.,
Richmond, J.E., and Stewart, A.J. Multispecies toxicity assessment of compost
produced in bioremediation of an explosives-contaminated sediment. Environ.
Toxicol. Chem. 16(12), 25292537, 1997.
Haderlein, A., Aly-Hassan, M.C.B., Legros, R., and Ramsay, B.A. The design and use
of aerated microcosms in mineralization studies. Biodegradation 10(6), 437442,
1999.
Haderlein, A., Legros, R., and Rambsay, B. Enhancing pyrene mineralization in contaminated soil by the addition of humic acids or composted contaminated soil.
Appl. Microbiol. Biotechnol. 56, 555559, 2001.
Haeseler, F., Blanchet, D., Druelle, V., Werner, P., and Vandecasteele, J.P. Ecotoxicological assessment of soils of former manufactured gas plant sites: Bioremediation potential and pollutant mobility. Environ. Sci. Technol. 33(24), 43794384,
1999.
Harvey, R.G. Polycyclic aromatic hydrocarbons. New York: Wiley-VCH, 1997.
Haug, R.T. The practical handbook of compost engineering. Boca Raton, FL: Lewis,
CRC Press, 1993.
in der Wiesche, C., Martens, R., and Zadrazil, F. The effect of interaction between white-rot fungi and indigenous microorganisms on degradation of polycyclic aromatic hydrocarbons in soil. Water Air Soil Pollut. Focus 3, 7379,
2003.
Interdepartmental Committee on the Redevelopment of Contaminated Land. Guidance on the assessment and redevelopment of contaminated land. ICRCL
Guidance Note 59/83, 2nd ed. DETR (Department of the Environment Transport
and Regions), Publications Centre, Unit 8, Goldthrop Industrial State, Goldthrop,
Rotherham 5639BL, United Kingdom, 1987.
International Society for Polycyclic Aromatic Compounds. 2003. PAH structure/
properties www.ispac.org
Joner, E.J., and Leyval, C. Rhizosphere gradients of polycyclic aromatic hydrocarbon
(PAH) dissipation in two industrial soils and the impact of arbuscular mycorrhiza.
Environ. Sci. Technol. 37(11), 23712375, 2003.
Jrgensen, K.S., Puustinen, J., and Suortti, A.-M. Bioremediation of petroleum
hydrocarbon-contaminated soil by composting in biopiles. Environ. Poll. 107,
245254, 2000.
P1: FZX/Sanjeev
TJ1023-02
EST.cls
286
March 24, 2004
9:41
Joyce, J.F., Sato, C., Cardenas, R., and Surampalli, R.Y. Composting of polycyclic
aromatic hydrocarbons in simulated municipal solid waste. Water Environ. Res.
70, 356361, 1998.
Juhasz, A.L., and Naidu, R. Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: A review of the microbial degradation of benzo[a]pyrene.
Int. Biodeter. Biodegr. 45, 5788, 2000.
Kanaly, R.A., and Harayama, S. Biodegradation of high-molecular-weight polycyclic
aromatic hydrocarbons by bacteria. J. Bacteriol. 182(8), 20592067, 2000.
Kastner, M., Breuerjammali, M., and Mahro, B. Enumeration and characterization of
the soil microflora from hydrocarbon-contaminated soil sites able to mineralize
polycyclic aromatic-hydrocarbons. Appl. Microbiol. Biotechnol. 41(2), 267273,
1994.
Kastner, M., Lotter, S., Heerenklage, J., Breuer-Jammali, M., Stegmann, R., and Mahro,
B. Fate of 14 C-labeled anthracene and hexadecane in compost-manure soil. Appl.
Microbiol. Biotechnol. 43, 11281135, 1995.
Kastner, M., and Mahro, B. Microbial degradation of polycyclic aromatic hydrocarbons in soils affected by the organic matrix of compost. Appl. Microbiol. Biotechnol. 44, 668675, 1996.
Kastner, M., Streibich, S., Beyrer, M., Richnow, H.H., and Fritsche, W. Formation of
bound residues during microbial degradation of [14 C]anthracene in soil. Appl.
Environ. Microbiol. 65(5), 18341842, 1999.
Kirchmann, H., and Ewnetu, W. Biodegradation of petroleum-based oil waste
through composting. Biodegradation 9, 151156, 1998.
Korner, I., Braukmeier, J., Herrenklage, J., Leikam, K., Ritzkowski, M., Schlegelmilch,
M., and Stegmann, R. Investigation and optimisation of composting processes
Test systems and practical examples. Waste Manage. 23, 1726, 2003.
Laine, M.M., and Jrgensen, K.S. Effective and safe composting of chlorophenolcontaminated soil in pilot scale. Environ. Sci. Technol. 31(2), 371378,
1997.
Laor, Y., Strom, P.F., and Farmer, W.J. Bioavailability of phenanthrene sorbed to
mineral-associated humic acid. Water Res. 33, 17191729, 1999.
Lau, K.L., Tsang, Y.Y., and Chiu, S.W. Use of spent mushroom compost to bioremediate PAH-contaminated samples. Chemosphere 52, 15391546, 2003.
Lei, A.P., Wong, Y.S., and Tam, N.F.Y. Removal of pyrene by different microalgal
species. Water Sci. Technol. 46(1112), 195201, 2002.
Liang, C., Das, K.C., and McClendon, R.W. The influence of temperature and moisture
contents regimes on the aerobic microbial activity of a biosolids composting
blend. Bioresource Technol. 86(2), 131137, 2003.
Loser, C., Ulbricht, H., Hoffmann, P., and Seidel, H. Composting of wood containing polycyclic aromatic hydrocarbons (PAHs). Compost Sci. Util. 7(3), 1632,
1999.
Mahro, B., and Kastner, M. Mechanisms of microbial degradation of polycyclic aromatic hydrocarbons (PAHs) in soil-compost mixtures. In Contaminated soil 93,
vol. 2, Eds. F. Arendt, G.J. Annokkee, R. Bosman, and W.J. van den Brink,
pp. 12491256, Dordrecht, the Netherlands: Kluwer. 1993.
Mahro, B., Schaefer, G., and Kastner, M. Pathways of microbial degradation of polycyclic aromatic hydrocarbons in soil. In Bioremediation of chlorinated and
P1: FZX/Sanjeev
TJ1023-02
EST.cls
March 24, 2004
9:41
287
polycyclic aromatic hydrocarbons, Eds. A.R. Hinchee, E. Leeson, L. Semprini,

and S.K. Ong, pp. 203217, Boca Raton, FL: Lweis, 1994.
Maini, G., Sharman, A.K., Knowles, C.J., Sunderland, G., and Jackman, S.A.
Electrokinetic remediation of metals and organics from historically contaminated
soil. J. Chem. Technol. Biotechnol. 75(8), 657664, 2000.
Martens, R. Concentrations and microbial mineralization of four to six ring polycyclic
aromatic hydrocarbons in composted municipal waste. Chemosphere 11, 761
770, 1982.
McFarland, M.J., and Qiu, X.J. Removal of benzo(a)pyrene in soil composting systems
amended with the white rot fungus Phanerochaete chrysosporium. J. Hazard
Mater. 42, 6170, 1995.
McFarland, M.J., Qiu, X.J., Sims, J.L., Randolph, M.E., and Sims, R.C. Remediation of
petroleum impacted soils in fungal compost bioreactors. Water Sci. Technol. 25,
197206, 1992.
Michel, F.C., Quensen, J., and Reddy, C.A. Bioremediation of a PCB-contaminated
soil via composting. Compost Sci. Util. 9(4), 274284, 2001.
Mougin, C. Bioremediation and phytoremediation of industrial PAH-polluted soils.
Polycyclic Aromatic Compounds. 22(5), 10111043, 2002.
Mueller, J.G., Cerniglia, C.E., and Pritchard, P.H. Bioremediation of environments
contaminated by polycyclic aromatic hydrocarbons. In Bioremediation: Principles and applications, Eds. R.L. Crawford and D.L. Crawford, Biotechnology Research Series 6, pp. 125194. New York: Cambridge University Press,
1996.
Namkoong, W., Hwang, E.-Y., Park, J.-S., and Choi, J.-Y. Bioremediation of dieselcontaminated soil with composting. Environ. Pollut. 119, 2331, 2002.
Phillips, P.A., Pratt, R.M., and Pike, K. An analysis of UK waste minimization clubs:
Key requirements for future cost effective developments. Waste Manage. 21,
389404, 2001.
Picado, A., Nogueira, A., Baeta-Hall, L., Mendonca, E., Rodrigues, M.D., Saagua,
M.D., Martins, A., and Anselmo, A.M. Landfarming in a PAH-contaminated soil.
J. Environ. Sci. Health A 36(9), 15791588, 2001.
Pignatello, J.J., and Xing, B. Mechanisms of slow sorption of organic chemicals to
natural particles. Environ. Sci. Technol. 30, 111, 1996.
Potter, C.L., Glaser, J.A., Chang, L.W., Meier, J.R., Dosany, M.A., and Herrmann, R.F.
Degradation of polynuclear aromatic hydrocarbons under bench-scale compost
conditions. Environ. Sci. Technol. 33, 17171725, 1999.
Qiu, X.J., and McFarland, M.J. Bound residue formation in PAH contaminated soil
composting using Phanerochaete chrysosporium. Hazard Waste Hazard Mater.
8, 115126, 1991.
Racke, K.D., and Frink, C.R. Fate of organic contaminants during sewage-sludge
composting. Bull. Environ. Contam. Toxicol. 42(4), 526533, 1989.
Ro, K.S., Preston, K.T., Seiden, S., and Bergs, M.A. Remediation composting process
principles: Focus on soils contaminated with explosive compounds. Crit. Rev.
Environ. Sci. Technol. 28(3), 253282, 1998.
S asek, V. Why mycoremediations have not yet come into practice. In The utilization
of bioremediation to reduce soil contamination: Problems and solutions, Eds.
V. S asek, J.A. Glaser, and P. Baveye, pp. 247266. Boston: Kluwer, 2003.
P1: FZX/Sanjeev
TJ1023-02
EST.cls
288
March 24, 2004
9:41
S asek, V., Cajthaml, T., and Bhatt, M. Use of fungal technology in soil remediation:
A case study. Water Air Soil. Pollut. 3, 514, 2003a.
S asek, V., Bhatt, M., Cajthaml, T., Malachova, K., and Lednicha, D. Compost-mediated
removal of polycyclic aromatic hydrocarbons from contaminated soil. Arch. Environ. Contam. Toxicol. 44, 336342, 2003b.
Semple, K.T., Reid, B.J., and Fermor, T.R. Impact of composting strategies on the
treatment of soils contaminated with organic pollutants. Environ. Pollut. 112(2),
269283, 2001.
Seymour, R.M., Donahue, D., Bourdon, M., Evans, J.R., and Wentworth, D. Intermittent aeration for in-vessel composting of crab processing waste. Compost Sci.
Util. 9(2), 98106, 2001.
Slater, R., and Frederickson, J. Composting municipal waste in the UK: Some lessons
from Europe. Resource Conserv. Recy. 32, 359374, 2001.
Steffen, K.T., Hatakka, A., and Hofrichter, M. Degradation of benzo[a]pyrene by the
litter-decomposting basidiomycete Stropharia coronilla: Role of manganese peroxidase. Appl. Environ. Microbiol. 69(7), 39573964, 2003.
Thomas, A.O., and Lester, J.N. The microbial remediation of former gasworks sites
A review. Environ. Technol. 14(1), 124, 1993.
United Nations Economic Commission for Europe Persistent Organic Pollutants. 2003.
Pollutant release & transfer registers. www.chem.unep.ch/pops
U.S. Environmental Protection Agency. Cost and performance report: Land treatment at the Burlington Northern Superfund Site, Brainerd/Baxter, Minnesota.
Report contract number 68-W3-0001, 1995a. www.clu-in.org/download/remed/
brown.pdf
U.S. Environmental Protection Agency. Cost and performance report: Slurry phase
bioremediation application at the Southeastern Wood Preserving Superfund
Site, Canton, Mississippi. Report contract number 68-W3-0001, 1995b. www.
clu-in.org/download/remed/brown.pdf
VanBrummelen, T.C., Verweij, R.A., Wedzinga, S.A., and VanGestel, C.A.M. Polycyclic
aromatic hydrocarbons in earthworms and isopods from contaminated forest
soils. Chemosphere 32(2), 315341, 1996.
VanderGheynst, J.S., and Lei, F. Microbial community structure dynamics during aerated and mixed composting. Trans. ASAE 46(2), 577584, 2003.
van Herwijnen, R., Wattiau, P., Bastiaens, L., Daal, L., Jonker, L., Springael, D., Govers, H.A.J., and Parsons, J.R. Elucidation of the metabolic pathway of fluorene and cometabolic pathways of phenanthrene, fluoranthene, anthracene and
dibenzothiophene by Sphingomonas sp LB126. Res. Microbiol. 154(3), 199206,
2003.
Walter, E., Lopez-Real, J.M., and Wharfe, J. Composting of sewage sludge and straw:
Laboratory scale simulation and evaluation of selected temperatures and effect
on composting performance. In International Symposium on Compost Recycling of Wastes, Eds. C. Balis, M. de Bertoldi, G.L. Ferrero, V. Maniow, and E.
Kapetanios. Acta Hort. 302, 113124, 1992.
Williams, R.T., and Keehan, K.R. Hazardous and industrial waste composting. In
Science and engineering of composting: Design, environmental, microbiological and utilization aspects, Eds. H.A.J. Hoitink and H.M. Keener, pp. 363381.
Worthington, OH: Renaissance, 1993.
P1: FZX/Sanjeev
TJ1023-02
EST.cls
March 24, 2004
9:41
289
Wilson, S.C., and Jones, K.C. Bioremediation of soil contaminated with polynuclear aromatic hydrocarbons (PAHs): A review. Environ. Pollut. 81, 229249,
1992.
Wischmann, H., and Steinhart, H. The formation of PAH oxidation products in soils
and soil/compost mixtures. Chemosphere 35, 16811689, 1997.
Yu, H.T. Environmental carcinogenic polycyclic aromatic hydrocarbons: Photochemistry and phototoxicity. J. Environ. Sci. Health C. 20(2), 149183, 2002.
Zeng. Y., Hong, P.K.A., and Wavrek, D.A. Integrated chemical-biological treatment
of benzo[a]pyrene. Environ. Sci. Technol. 34(5), 854862, 2000.

Antizar Et Al. (2004) Bioremediation of Polycyclic Aromatic Hydrocarbon (PAH) - Contaminated Waste Using Composting Approaches

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March 24, 2004

Critical Reviews in Environmental Science and Technology, 34:249289, 2004

Bioremediation of Polycyclic Aromatic

B. ANTIZAR-LADISLAO, J. M. LOPEZ-REAL, and A. J. BECK

Environmental pollution and in particular contaminated waste

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Bioremediation of Polycyclic Aromatic Hydrocarbon

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there is no single source that reviews the success of composting in treatment

II. BIOREMEDIATION OF POLYCYCLIC AROMATIC

Domestic gardens, allotments, play areas

as a marker for coal tar. See CIRIA (1988, Annex 1).

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Bioremediation of Polycyclic Aromatic Hydrocarbon

FIGURE 1. Regulatory considerations for bioremediation of PAH-contaminated soil using

Figure 1 summarizes the regulations to consider at the different stages

B. PAHs in the Environment

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TABLE 3. Examples of PAH Concentrations in Contaminated Soils from Industrial Sites

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concentration of PAHs at MGP sites. In addition, MGP are well known to

C. Physicochemical Properties of PAHs

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Bioremediation of Polycyclic Aromatic Hydrocarbon

conditions. Table 4 outlines some physicochemical properties of the 16 U.S.

Solubility Vapor pressure Henry constant Resonance

279 3.925.07 2.9 102

218 3.004.00 2.4 101

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TABLE 4. Structure and Physico-Chemical Properties of 16 U.S. EPA Regulated PAHs

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Note. From ISPAC (2003).

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TABLE 5. Microorganisms Degrading PAHs

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Bioremediation of Polycyclic Aromatic Hydrocarbon

TABLE 5. Microorganisms Degrading PAHs (Continued)

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Bacteria: Beijerinckia sp., Mycobacterium sp., Pseudomonas

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Bioremediation of Polycyclic Aromatic Hydrocarbon

are cometabolic, where an alternate carbon source is utilized for energy

III. COMPOSTING APPROACHES

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FIGURE 3. Variation of compost core temperature with the windrow system.

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