Journal of Hazardous Materials 167 (2009) 866872

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Journal of Hazardous Materials

journal homepage: www.elsevier.com/locate/jhazmat

Potential for land application of contaminated sewage sludge treated

with fermented liquid from pineapple wastes
Dominica Del Mundo Dacera a , Sandhya Babel a, , Preeda Parkpian b
a
Environmental Technology Program, School of Bio-Chemical Engineering and Technology, Sirindhorn International Institute of Technology (SIIT),
Thammasat University, P.O. Box 22, Pathumthani 12121, Thailand
b
School of Environment, Resources and Development, Asian Institute of Technology, P.O. Box 4, Klong Luang, Pathumthani 12120, Thailand

a r t i c l e i n f o a b s t r a c t

Article history: The suitability for land application of anaerobically digested sewage sludge treated with naturally fer-
Received 2 October 2008 mented and Aspergillus niger (A. niger) fermented raw liquid from pineapple wastes, in terms of changes
Received in revised form 16 January 2009 in the forms and amount of heavy metals and nutrient and pathogen content, were investigated in this
Accepted 16 January 2009
study. Leaching studies for fermented liquid at optimum conditions (pH and contact time with best metal
Available online 18 February 2009
removal efciencies) were carried out for the removal of Cd, Cr, Cu, Pb, Ni and Zn from sewage sludge,
with citric acid as a reference. Using the same sludge before and after leaching, sequential fractionation
Keywords:
studies were done to observe the effect of treatment on the forms of metals in sludge and their mobil-
Chemical extraction
Heavy metals
ity and bioavailability. Results of laboratory scale studies revealed that leaching with all extractants at
Land application selected optimum conditions resulted in a decrease in heavy metals and pathogen content of the treated
Sequential fractionation sludge, presence of sufcient amount of nutrients (nitrogen and phosphorous) and dominance of residual
Sewage sludge fractions in most metals, with sludge treated with A. niger, having the best quality. The results, therefore,
indicate the high potential of the treated sludge for land application, with no harm from heavy metals
released and no toxicity to the soil and groundwater.
2009 Elsevier B.V. All rights reserved.

1. Introduction Sewage sludge treatment processes are intended to reduce the

Land application of treated sewage sludge (biosolids) for soil
amendment and land reclamation purposes has increased over the
past decade as an alternative to other disposal options such as
land-lling or incineration, and as a result of the ban on ocean
dumping of wastewater residuals. This practice, besides solving
the nal disposal problem of sewage sludge, favors plant growth.
Sludge is a valuable source of nutrients and trace elements impor-
tant for plant growth, and can improve the chemical and physical
properties of soils. Although these benets have a great practical
meaning, it must be taken into account that sludge may contain
organic, inorganic, and biological pollutants from the wastewaters
of households, commercial establishments, and industrial facili-
ties and compounds added or formed during various wastewater
treatment processes. Such pollutants include inorganic contami-
nants (e.g., metals and trace elements), organic contaminants (e.g.,
polychlorinated biphenyls [PCBs], dioxins, pharmaceuticals and
surfactants), and pathogens (e.g., bacteria, viruses and parasites).
Hence, indiscriminate use of sludge in agriculture is considered as
a potential health risk [1].
Corresponding author. Tel.: +66 2 986 9009x2307; fax: +66 2 986 9009x2301.
E-mail address: sandhya@siit.tu.ac.th (S. Babel).
volume and organic and inorganic content of biosolids, as well
as reduce the presence of pathogens, while retaining benecial
properties for soil amendment and land-reclamation purposes.
Studies have shown however, that sludge from treatment pro-
cesses still contains harmful substances especially heavy metals
which can accumulate in the environment for long periods of time
[24]. Numerous studies have indicated that metal-contaminated
sewage sludges applied to agricultural land resulted in harmful
effects on crop quality which demonstrated the occurrence of phy-
totoxic effects of the metals on crops. Lester [5] conrmed that
if highly contaminated sludges are disposed of to the land at
excessive rates of application, the possibility of phytotoxic effects
exists.
To remove these concerned heavy metals from sludge, various
technologies such as chemical extraction, have been developed. The
chemical extraction process involves solubilization of heavy met-
als in sludge via acidication, followed by separation of solids from
the liquid through the dewatering step of the sludge handling pro-
cess. Extracting agents used were inorganic acids (HCl, H2 SO4 and
HNO3 ), organic acids (citric and oxalic acids), inorganic chelating
agents (EDTA and NTA) and inorganic chemicals (FeCl3 ) [2]. After
extraction, removal of heavy metals from the extracting agents can
be accomplished by chemical sulphide precipitation and selective
ion-exchange [6].

0304-3894/$ see front matter 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.jhazmat.2009.01.064
 D. Del Mundo Dacera et al. / Journal of Hazardous Materials 167 (2009) 866872
Among the extracting agents used in the chemical extraction
process, citric acid has been found to be promising, since extraction
can be performed at relatively mild acidic condition (pH 34) with
relatively high efciency of metal removal. Moreover, citric acid,
being organic, is readily degradable under aerobic and anaerobic
conditions [68]. Citric acid is a 6-carbon containing tricarboxylic
acid and exists as an intermediate in the citric acid cycle when car-
bohydrates are oxidized to carbon dioxide. The acidic nature of citric
acid results from the three carboxy groups COOH which can lose
a proton in solution forming the citrate ion. Citrates can chelate
metal ions and therefore have been used as chelating and seques-
tering agents [9,10]. Citric acid is currently produced commercially
by fermentation of sucrose using mutant strains of Aspergillus niger
(A. niger), and chemical synthesis. Carbohydrates and wastes that
have been considered experimentally to produce citric acid by A.
niger include date fruit syrup, soya whey, cheese whey, pineapple
wastes, corncobs and cane molasses.
The presence of citric acid in pineapple wastes became the basis
for recent studies by Del Mundo Dacera and Babel [7,11,12] in the
use of fermented liquid (natural fermentation and fermentation
by A. niger) from pineapple wastes to extract heavy metals (Cd,
Cr, Cu, Pb, Ni and Zn) from sludge. Using citric acid as a refer-
ence, leaching studies were done to determine the pH and contact
times (optimum conditions) which resulted in the best heavy metal
extraction efciencies. Results revealed that for leaching with cit-
ric acid and naturally fermented liquid from pineapple wastes, best
heavy metal removal efciencies were attained at pH of 3.04 and
3.67, respectively at contact time of 1 day. When leaching with A.
niger fermented liquid, the best removal efciencies were attained
at pH 3.73 and 3.88 at 5 days contact time. The study determined
only the amount of heavy metals retained in the sludge after treat-
ment not the forms. Moreover, in the previous studies, although
metal forms were identied in the sewage sludge before treat-
ment, study was not done on the change in metal forms as well as
changes in other properties of sludge after treatment in assessing
the suitability of the treated sludge for land application.
This study investigated the effect of treatment with naturally
fermented, A. niger fermented liquid, and commercial citric acid on
the characteristics of anaerobically digested sewage sludge, and its
suitability for land application. At optimum pH and leaching time
obtained from previous studies, a laboratory scale study was con-
ducted to observe the effect of treatment with various extractants
on the quality of the sewage sludge especially on the amount and
forms of heavy metals (Cd, Cr, Cu, Pb, Ni and Zn) as well as the nutri-
ent and pathogen content in the sludge. To determine the form of
heavy metals in the sludge and its mobility after land application,
chemical speciation studies by sequential fractionation, was done
before and after treatment of sludge.
2. Materials and methods
2.1. Sludge characterization
The sludge sample was collected from the sludge treatment
facility at Nongkhaem, in Bangkok, Thailand, which receives dewa-
tered sludges mainly from ve central wastewater treatment
facilities under the Bangkok Metropolitan Administration (BMA).
The central wastewater treatment plants treat mostly domestic
wastewater and a small amount of industrial wastewater. Sludge
sent to the treatment facility in Nongkhaem undergoes anaer-
obic digestion at 19 days retention time, and dewatering using
lter press prior to disposal mostly by landll. The sludge sam-
ple collected was analyzed in terms of its physical and chemical
characteristics, including heavy metals content according to the
Standard Methods for the Examination of Water and Wastewa-
ter [13]. Heavy metals were analyzed in duplicate using ame
867
atomic absorption spectrophotometer (AAS Hitachi Z-8230) after
microwave digestion (Analytical Microwave System operated by
WinWave application software) with nitric acid (HNO3 ), hydrou-
oric acid (HF), hydrochloric acid (HCl) and boric acid (H3 BO3 ) [13].
Sludge analysis was also done after treatment with various extrac-
tants (citric acid and fermented liquid from pineapple wastes).
2.2. Chemical speciation studies
Chemical speciation studies were done for both the untreated
and treated sludge using the sequential chemical extraction (SCE)
procedure employed by Del Mundo Dacera and Babel [7]. The
sequential extraction was carried out in 2 g of air dried sludge sam-
ples in 250 mL erlenmeyer asks using MgCl2 (exchangeable phase),
sodium acetate (bound to carbonates phase), NH2 OHHCl (bound
to Fe and Mn oxides), Na2 EDTA (bound to organic and inorganic
matter) and HNO3 , HCl and HF (residual phase). Between each of
the successive extractions, separation was done by centrifuging at
4000 rpm for 30 min where the supernatant was removed and ana-
lyzed for trace metals by ame AAS and the residue washed with
40 mL deionized water. Analyses for all metal forms were done in
duplicate.
2.3. Raw liquid extraction and analysis
Pineapple waste samples, consisting of the core, peel, and top
and bottom cuts were collected from a local fruit processing facil-
ity. The wastes were then crushed, ground and squeezed manually
to separate the pulp from the raw liquid. The raw liquid was ana-
lyzed for total sugar using high performance liquid chromatography
(HPLC-Agilent Technologies 1100) and total acidity as citric acid
using the Glass electrode method following the AOAC Ofcial Meth-
ods of Analysis [14]. Infrared spectroscopy (Brucker Vector 22) was
used to conrm the presence of citric acid as carboxylic acid in the
raw liquid. The pulp, which is known to contain a high percentage
of protein [15], can be used as animal feed.
2.4. Natural fermentation of raw liquid by shake ask studies
Raw liquid fermentation from pineapple wastes with A. niger at
optimum conditions by Sun [15], were adopted in this study. The
raw liquid extracted from pineapple wastes was allowed to undergo
aerobic fermentation in natural conditions (i.e. without A. niger)
by shaking at 150 rpm for 144 h (6 days) at 30 C. Samples taken
from fermentation (fermented mash) were ltered to separate the
solids from the ltrate. The ltrate was then used for leaching the
BMA sludge samples. Total sugar and acidity analyses of the l-
trate were done immediately in order to avoid decomposition by
methods stated in Section 2.3 using Glass electrode method and IR
spectroscopy studies. Analyses were done in duplicate.
2.5. Raw liquid fermentation with A. niger
2.5.1. A. niger inoculum preparation
The individual strain of A. niger obtained from BIOTEC Central
Research Unit, Pathumthani, Thailand, was inoculated on potato
dextrose agar slant (PDA) at 30 C for 7 days. Spore suspension
was prepared by cultivating the strain in asks containing 2930 g
rice grain, with 6 mL sterilized medium (yeast, peptone, glucose or
YPG) for 7 days at 30 C. The YPG contained the following: yeast
extract (5 g/L); peptone (10 g/L) and glucose (20 g/L). The resulting
spores were harvested in 0.1% Tween 80 (Polyoxyethylene-sorbitan
monooleate) solution and used to inoculate the raw liquid at
109 1010 spores/L [16]. The prepared A. niger inoculums, if properly
stored, can be used several times for fermentation of the raw liquid.
868 D. Del Mundo Dacera et al. / Journal of Hazardous Materials 167 (2009) 866872

2.5.2. Raw liquid fermentation with A. niger by shake ask studies
Optimum conditions for raw liquid fermentation from pineapple
wastes using A. niger by Sun [15], were also adopted in this study.
Prior to fermentation, the raw liquid (250 mL) was dispensed into
1000 mL erlenmeyer asks. Since the initial pH of the raw liquid
was 3.7, no pH adjustment was made to meet the pH requirement
for citric acid fermentation, which is 34. Phosphorus in the form of
potassium dihydrogen phosphate (KH2 PO4 ) was added at the rate
of 0.51.0 g/L. The asks were autoclaved at 103.42 kPa (15 lbf /in.2 )
at 121 C for 15 min prior to use. Each ask was inoculated with
2 mL spore suspension and was shaken at 150 rpm for 144 h (6
days) at 30 C. Samples taken from fermentation (fermented mash)
were ltered to separate the mycelium from the liquid phase. The
mycelium, which is high in protein [15], can be used as animal feed.
The yield of mycelial dry weight was 28.2 g/L. The ltrate was then
used for leaching the BMA sludge samples and analyzed for total
sugar and citric acid immediately, in order to avoid decomposition.
Three types of analyses were done to determine the presence and
amount of citric acid in the ltrate: (i) total acidity, to determine the
presence of citric acid and all other organic acids, using the Glass
electrode method following the AOAC Ofcial Methods of Analysis
[14]; (ii) infrared spectroscopy (Brucker Vector 22) studies to con-
rm the presence of citric acid as carboxylic acid; and (iii) high per-
formance liquid chromatography (HPLC) studies to determine the
amount of citric acid present in the ltrate. The HPLC was used with
an Aminex HPX-87H column (Bio-Rad, Hercules, CA, USA) at 60 C,
using 5 mM H2 SO4 as a mobile phase at a ow rate of 0.6 mL/min.
Citrate was detected refractometrically (Waters 410 Differential
Refractometer Detector, Millipore Corp., Milford, MA, USA).
2.6. Leaching Procedure for commercial citric acid, naturally
fermented and A. niger fermented liquid at optimum conditions
Optimum conditions for leaching with citric acid [7], naturally
fermented raw liquid [11] and A. niger fermented liquid [12], were
used for this study. Optimum conditions were selected based on
the pH and contact time which gave the best removal efciency for
all extractants (pH of 3.04 at 1 day contact time for citric acid; pH
of 3.67 at 1 day contact time for naturally fermented liquid; and
pH of 3.73 and 3.88 at 5 days contact time for A. niger fermented
liquid). The following acid leaching procedure modied from Ali
[17], Marchioretto et al. [8] and Veeken and Hamelers [6], was used.
Samples containing 7 g of air dried sludge were transferred to
reactors and lled with 140 mL deionized water. Varying amounts
of the extractants were then added to the sludge samples to obtain
the desired pH of 3.04 (1.4 101 g/g), for 0.1 M commercial citric
acid; pH of 3.67 (46.6 g/g), for naturally fermented liquid; and pH of
3.73 (42.0 g/g) and 3.88 (9.0 g/g), for A. niger fermented liquid. The
pH measurements were done using Oakton pH 10 series (Model No.
35614-70). In order to ensure accuracy across the entire range of the
meter, a two-point calibration was done before each pH measure-
ment. A rotary shaker (Panapolytech Sseriker II) was used to mix the
reactors continuously at 150 rpm at room temperature for 1 day for
sludge treated with citric acid and naturally fermented raw liquid;
and 5 days for sludge treated with A. niger fermented raw liquid
from pineapple wastes. After leaching, the samples were collected
and centrifuged (Nuve NF 800) at 4000 rpm for 30 min and then
ltered using a 47 mm glass microbre lter (1.2 m GF/C). The l-
trate was then analyzed for heavy metals (Cd, Cr, Cu, Pb, Ni and Zn)
using ame AAS. All analyses were done in duplicate.
3. Results and discussion
3.1. Sludge characterization
Table 1 shows the characteristics of the sludge sample before and
after treatment at optimum conditions with the following extrac-
tants: commercial citric acid (CA), naturally fermented raw liquid
from pineapple wastes (NF), A. niger fermented raw liquid at pH
3.73 (AF1) and A. niger fermented raw liquid at pH 3.88 (AF2).
As shown, there is an observed increase in the organic matter
content of treated sludges compared to the untreated sludge which
may be due to the organic nature of the extractants added to the
sludge during treatment. For total nitrogen, there seemed to be

Table 1
General characteristics of untreated and treated BMA sewage sludge at optimum conditions.

Parameters Untreated CA treated NF treated AF1 treated AF2 treated Proposed BMA Compost
anaerobic sludgea sludgeb sludgec sludged guidelinesf /USEPA standards
sludge standardsg

pH (sludge:water ratio = 1:2) 6.5 3.0 3.7 3.7 3.9 5.58.5h

Total solids (%) 23.1 17.0 17.6 10.7 13.8 65
Total volatile solids (TVS) 44.7 96.4 85.7 81.6 95.7
Total nitrogen (%) 2.5 2.1 3.0 1.7 1.5 0.21
Total phosphate (%) 3.4 3.2 3.4 3.7 3.6 0.21
Organic matter (%) 44.7 96.4 85.7 81.6 95.7 1560
Faecal coliform (MPN/g) 1.6 104 9.2 103 490 <2 <2 /1 103 2 106

Heavy metals (mg/kg)

Cd 4.8 2.3 2.3 1.7 2.9 20/39 19i
Cr 264 202 264 43.8 107 1000/1200
Cu 3043 2739 2833 3043 2897 900/1500 725
Pb 175.2 122 175 166 175 1000/300 565
Fe 34,190 NAe 9776 10,054 10,361
Mn 2011 NA 860 374 300
Ni 298 243 194 52.6 155 400/420
Zn 1908 1166 985 43.9 47.7 3000/2800 1000
a
CA citric acid.
b
NF naturally fermented raw liquid from pineapple wastes.
c
AF1 A. niger fermented raw liquid from pineapple wastes (pH 3.73).
d
AF2 A. niger fermented raw liquid from pineapple wastes (pH 3.88).
e
NA not analyzed.
f
Proposed BMA guidelines [19].
g
USEPA standards [20].
h
Thai compost standard [21].
i
US compost standard [22].
 D. Del Mundo Dacera et al. / Journal of Hazardous Materials 167 (2009) 866872 869

Table 2
Characteristics of raw and fermented liquid from pineapple wastes.

Parameters Raw liquid Naturally fermented liquid A. niger fermented liquid

Density (kg/L) 1.051.25 1.051.25 1.051.25

pH 3.94.09 3.43.64 3.673.70
Total sugar (%): 5.1712.42 4.43 2.435.59
Fructose 0.72.2 2.0 2.49
Glucose 2.79 2.43 2.433.10
Sucrose 4.477.43 ND ND
Maltose ND ND ND
Lactose ND ND ND
Acidity as citric acid (g/100 g) 0.50.97 0.62 4.54
Citric acid content (g/L) NA NA 5.346.36

Heavy metals (mg/L)

Cd 0.01 0.01 ND
Cr 2.5 ND ND
Cu 0.06 ND ND
Pb 0.3 0.3 ND
Ni 0.18 0.06 0.2
Zn 2.33.3 2.32.9 1.9
Fe 3.2 0.85 1.65
Mn 14.7 NA 12.3

ND, not detected; NA, not analyzed.

an observed decrease for sludge treated with A. niger fermented
liquid which might be attributed to the use of nitrogen by A. niger
as a nutrient in the fermentation process [10]. The phosphorous
content of the A. niger treated sludge seemed to be unaffected since
a phosphate source in the form of potassium dihydrogen phos-
phate (KH2 PO4 ) has been added as a nutrient in the fermentation
process. In terms of coliform removal, an almost complete removal
of faecal coliform was observed for the sludge treated with A. niger
fermented raw liquid as compared to the sludge treated with other
extractants. This may be due to the secretion of secondary metabo-
lites by the fungus, such as antibiotics, which had disinfecting
effect on the sludge [18]. In terms of remaining metals, the sludge
treated with A. niger fermented liquid seemed to contain the least
amount of most metals, indicating a higher metal removal attained
for the extractant. However, the remaining copper metal for sludge
treated with all four extractants is still high and so cannot comply
with the proposed BMA guidelines. It can also be noticed that a
high amount of Fe (removal at 71.4% for naturally fermented liquid
while 70.6% and 69.7% for A. niger fermented liquid at pH 3.73
and 3.78, respectively) and Mn (removal at 57.2% for naturally
fermented liquid while 81.4% and 85.1% for A. niger fermented
liquid at pH 3.73 and 3.78, respectively) was also removed in the
process, indicating that Fe and Mn may have been utilized in the
fermentation process and may have also acted as competing metals
in the extraction process. With the exception of Cu, all the other
parameters including the nitrogen and phosphorous content of the
sludge seem to indicate the potential of the treated sludge for land
application. However, due to the high organic content of the treated
sludge, further treatment such as air drying, may be necessary
before nal disposal, to increase the total solids and decrease
the organic content of the treated sludge, which do not meet the
compost standards. Moreover, since the pH of the treated sludge is
below the compost standard, liming may be necessary to adjust the
pH to 5.5 or greater, and to further stabilize the sludge before land
application.
3.2. Characteristics of raw and fermented liquid from pineapple
wastes
glucose and sucrose) seemed to be present in the raw liquid which
is favorable in the production of citric acid. According to Yigi-
toglu [10], the usual carbon sources for fermentation by the fungus
A. niger to produce high yield of citric acid are glucose, fruc-
tose, or sucrose. Yigitoglu [10] also noted that not only the type
but also the concentration of the carbon source is important in
the citric acid fermentation, with maximal citric acid production
rate achieved at 1422% of sugar in the medium. The absence
of sucrose in both the naturally fermented raw liquid and the A.
niger fermented raw liquid indicated that sucrose fermentation
has taken place, although the process may not have been com-
pleted as indicated by the increased production of fructose and
glucose in the A. niger fermented liquid. According to Batista et al.
[23], it is generally accepted that sucrose fermentation proceeds
through extracellular hydrolysis of the sugar producing glucose and
fructose.
The total acidity of a solution is a measure of all the hydro-
gen ions of both the xed and volatile acids present. The acidity
then indicates the presence of citric acid and all other acids such
as malic and ascorbic acids [24] in the raw liquid. An increase in
total acidity was observed after fermentation of raw liquid indicat-
ing the increase in the amount of citric acid and other acids present.
Results of HPLC measurements of duplicate samples of A. niger fer-
mented liquid revealed a citric acid content of 5.346.36 g/L. The
result seemed to be consistent with the ndings of Sun [15] who
was able to obtain 5.013.6 g/L of citric acid from A. niger fermented
liquid from pineapple wastes, depending on the sugar content of the
raw liquid. However, since the sugar content in the raw liquid was
found to vary according to seasons [15], citric acid content of the
liquid would be expected to be low during rainy season due to low
sugar content of the liquid.
Infrared (IR) spectroscopy studies were also done on the raw
liquid, naturally fermented liquid and A. niger fermented liquid to
determine the functional groups present in the samples. Results of
the analysis showed the presence of the carboxy groups (COOH)
indicating the presence of citric acid, and other carboxylic acids.
Carboxylic acid dimers display very broad, intense OH stretching
absorption in the region of 33002500 cm1 [25].

The physical characteristics and metal content of the unfer- 3.3. Chemical speciation studies
mented and fermented raw liquid are summarized in Table 2.
As shown, some heavy metals are contained in the raw liq- 3.3.1. Untreated sludge
uid which may come from the peeling operations or cutting and Results of the chemical speciation studies for the untreated
grinding of pineapple peels. Only three types of sugar (fructose, sludge sample are shown in Fig. 1(a).
870 D. Del Mundo Dacera et al. / Journal of Hazardous Materials 167 (2009) 866872

Fig. 1. Metal fractionation prole of (a) untreated BMA sewage sludge; (b) citric acid-treated sludge, (c) naturally fermented liquid-treated sludge. (d) A. niger fermented
liquid-treated sludge at pH 3.73 and (e) A. niger fermented liquid-treated sludge at pH 3.88.

As shown, Cd seemed to predominate in the bound to Fe and Mn
form (36.1%) and least predominant in residual form. Chromium
and Cu seem to be predominantly in the residual form (92% and
89.6% respectively), although for Cu, a very minimal exchangeable
form (0.51%) was detected which is not present in Cr. Lead predom-
inates in bound to organic matter (53.4%) with a relatively high
residual portion at 26.5%. Nickel contains an almost equal amount
of residual (at 32.4%) and bound to Fe and Mn form (at 31.1%) and a
relatively high exchangeable form (7.45%). Zinc on the other hand
has a lesser amount of residual form (at 9.6%) and is predominantly
in the bound to Fe and Mn form (at 43.8%). All forms of Zn metal
were detected.
Furthermore, it was observed that the sum of ve metal frac-
tions obtained from sequential extraction procedure was higher
than the total metal contents in the sludge following acid digestion.
This may be due to the slow but increasingly stronger attack by the
various reagents used in the sequential extraction procedure which
removed specic forms of metals in the process, whereas, after acid
digestion, not all forms of metals may have been removed. This dif-
ference was particularly pronounced for Cd, Cr and Cu. A similar
observation was recorded by Par et al. [26] and Staelens et al. [27].
3.3.2. Sludge treated with commercial citric acid (CA treated)
Fig. 1(b) shows the results of the sequential chemical extraction
studies for sludge treated with commercial citric acid. For Cd, com-
pared with the untreated sludge, the portion which is bound to Fe
and Mn and the residual forms seemed to increase to 41.3% and 7.9%,
respectively, while the exchangeable form of the metal seemed to
be unchanged. For Cr, the residual form seemed to predominate
completely while it is less in the untreated sludge. Copper seemed
to predominate in residual form at 89.6%, with most metal forms
at a lesser proportion with no bound to Fe and Mn forms. For Pb,
the presence of bound to Fe and Mn form (at 24%) seemed to be
noticeable where as it is absent in the untreated sludge. A decrease
in residual form for Pb to 12.5% in the CA treated sludge was also
observed. The forms of Ni were almost the same although there is an
observed decrease in proportion, except for the exchangeable form
where an increase in proportion to 12.1% was observed. For Zn, all
forms of the metal were detected although at a lesser proportion.
The increase in the proportion of exchangeable form to 17.1% was
also noticeable.
The results revealed the potential of the CA treated sludge
for land application since most metals were in residual fractions.
 D. Del Mundo Dacera et al. / Journal of Hazardous Materials 167 (2009) 866872
However, the high percentage of exchangeable forms of metals
such as in Cd, Ni and Zn, could affect the mobility of these metals
in the environment. Metals in the exchangeable phase are easily
exchangeable with the soil solution and hence comparatively
mobile and bioavailable [28], while residual fractions are tightly
bound to the sludge and therefore less mobile.
3.3.3. Sludge treated with naturally fermented raw liquid (NF
treated)
The results of the SCE studies for sludge treated with natu-
rally fermented raw liquid from pineapple wastes are shown in
Fig. 1(c). As shown, for Cd, the portion which is bound to Fe and
Mn seemed to have decreased to 23.8% while the residual form
has increased to 14.8%, compared to the untreated sludge. More-
over, a slight decrease in the exchangeable form of the metal to
19% has been observed, as well as in bound to carbonate form. For
Cr, the residual form of the metal seemed to predominate com-
pletely while this form is less in the untreated sludge. Copper still
predominates in residual form at a lesser proportion of 76.4% but
with an observed increase in the exchangeable form to 4.1%. For Pb,
the absence of bound to carbonate form is noticeable while this is
present in the untreated sludge. A decrease for Pb in the bound to
organic matter form and residual form to 44.3% and 17.5%, respec-
tively in the CA treated sludge was also observed. The forms of Ni
metal observed were of lesser proportion although an increase of
exchangeable form to 11% was observed in the CA treated sludge.
For Zn, all forms of the metal were detected although at a lesser
proportion. The increase in the proportion of exchangeable form to
19.5% was also noticeable.
The results revealed that the naturally fermented treated sludge
contains metals mostly high in residual fractions, hence its potential
for land application. However, the high percentage of exchange-
able forms of metals such as in Cd, Ni and Zn, could affect the
mobility of these metals in the environment. Metals associated
with the exchangeable and oxidizable (bound to organic matter)
phases are easily mobilized by the ion exchange reaction and also
by the decomposition and transformation of organic matters and
can therefore easily be leached out with the acids [28,29]. Moreover,
metals in the acid extractable phase (or carbonate bound) which are
very sensitive to pH changes are also readily leached when the pH of
the environment is decreased [27] and, hence, are easily extractable
from the sludge solution at favorable pH. The residual fraction on
the other hand is strongly bound to the sludge matrix.
3.3.4. Sludge treated with A. niger fermented raw liquid at pH
3.73 (AF1 treated)
Fig. 1(d) shows the results of the SCE studies for sludge treated
with A. niger fermented raw liquid at pH 3.73. For Cd, compared
with the untreated sludge, equal amounts of only two forms of the
metal (exchangeable and bound to carbonate forms) were detected
at lower proportions. For Cr, the residual form of the metal seemed
to predominate completely at a much lower proportion (26%). Cop-
per still predominates in residual form at a lower proportion of
34.7% but with an observed increase in the exchangeable form
to 7.1%. Lead metal seemed to be present only in exchangeable
form in contrast with the untreated sludge where it is present in
three forms (bound to organic matter, residual and bound to car-
bonate) and not in exchangeable form. Only one form (residual)
of Ni at a lower proportion (16.8%) was observed in the sludge
treated with A. niger fermented liquid at pH 3.73, in contrast to the
untreated sludge where almost all forms of metals were present.
For Zn, all forms of the metal were also detected with the pre-
dominance of the exchangeable form at 11.7% in contrast to the
untreated sludge where the predominant form is bound to Fe and
Mn. Other forms of metals were observed to be at a much lower
proportion.
871
Results revealed that for this treated sludge, Cr, Cu and Ni do not
seem to pose a problem of mobility once disposed to land because
of their relatively high proportion of residual forms. However, Cd
and Pb which seem to predominate in exchangeable and carbonate
forms may affect the mobility of these metals to the environment.
3.3.5. Sludge treated with A. niger fermented raw liquid at pH
3.88 (AF2 treated)
Results of the SCE studies for sludge treated with A. niger fer-
mented raw liquid at pH 3.88 is depicted in Fig. 1(e). As shown
for Cd, compared with the untreated sludge, only the exchange-
able form of the metal was detected at lower proportion. For Cr,
the residual form of the metal seemed to predominate completely
at a much lower proportion (19.9%). Copper still predominates in
residual form at a lower proportion of 26.4% but with an observed
increase in the exchangeable form to 3.7%. Lead metal seemed to be
present only in exchangeable form in contrast with the untreated
sludge where it is present in three forms (bound to organic matter,
residual and bound to carbonate) and not in exchangeable form.
Only two forms (residual and exchangeable) of Ni at a lower pro-
portion (18.9% and 1% respectively) were observed in the sludge
treated with A. niger fermented liquid at pH 3.88, in contrast to the
untreated sludge where almost all forms of metals were present.
For Zn, not all forms of the metal were detected. The exchangeable
form of the metal (at 7.14%) predominates while all the other forms
are of much lower proportion.
For sludge treated with A. niger fermented liquid at pH 3.88, a
similar observation is made at pH 3.73, as to the mobility of the met-
als present in the treated sludge once disposed to land. Chromium,
Cu and Ni do not seem to pose a problem of mobility because of their
relatively high proportion of residual forms. However, Cd, Pb and
Zn which seem to predominate in exchangeable form, may affect
their mobility to the environment.
3.4. Leaching with various extractants at optimum conditions
Fig. 2 presents the results of leaching at optimum conditions
with the following extractants: commercial citric acid (CA), natu-
rally fermented raw liquid (NF), A. niger fermented raw liquid at pH
3.73 (AF1), and A. niger fermented raw liquid at pH 3.88 (AF2).
For Cd, the highest removal of 64.6% was attained using A niger
fermented liquid at pH 3.73 at 5 days contact time, followed by
citric acid at 52.5% and naturally fermented liquid at 51.6%. The
least removal of 39.3% was obtained using A. niger fermented liquid
at pH 3.88 and optimum leaching time of 5 days.
The highest removal attained for Cr metal was 83.4% using A.
niger fermented raw liquid at pH 3.73, followed by the same extrac-
tant at pH 3.88 (59.3% removal), both at 5 days contact time; and
citric acid at 23.4%. No removal was detected using naturally fer-
mented raw liquid.
Fig. 2. Metal Removal of various extractants at optimum conditions.
872 D. Del Mundo Dacera et al. / Journal of Hazardous Materials 167 (2009) 866872
Copper removal was very minimal using all extractants, with
citric acid attaining the highest removal of only 10%. No removal
was detected using A. niger fermented liquid.
Lead removal was highest at 30.2% using citric acid as an extrac-
tant at optimum conditions. Using A. niger fermented liquid at pH
3.73, a very minimal removal of 5.3% was attained. No removal was
detected for other extractants.
For Ni, the highest removal of 82.4% was attained using A. niger
fermented liquid at pH 3.73 as an extractant, followed by the same
extractant at pH 3.88, attaining about 48.1% removal, and naturally
fermented raw liquid at 34.9% removal. The least removal of 18.6%
was attained using citric acid as an extractant.
For Zn, metal removal was attained using all extractants at opti-
mum conditions, with almost all metals being removed using A.
niger fermented liquid at pH 3.73 and 3.88. A removal of 48.4% was
attained using naturally fermented raw liquid, and the least removal
of 38.9% was attained using commercial citric acid.
4. Conclusions
At selected optimum conditions, treatment of BMA sewage
sludge with A. niger fermented raw liquid from pineapple wastes,
seemed to yield the best quality of treated sludge with the least
amount of remaining metals, most metals being dominant in resid-
ual fractions, as well as negligible amount of pathogen left and
sufcient amount of nutrients. Highest percentages of removal for
Cd (64.6%), Cr (83.4%), Ni (82.4%) and Zn (97.7%) were attained at pH
3.73. Moreover, A. niger fermented liquid seemed to exhibit effec-
tiveness in the removal of bound to Fe and Mn form of Cd, residual
and bound to organic matter form of Cr, and most metal forms
including the residual form of Ni and Zn. The superiority of the A.
niger fermented liquid over the other extractants for metal removal,
seemed to be due to the presence of a relatively high amount of cit-
ric acid as conrmed by the infrared (IR) spectroscopy studies and
HPLC analyses.
In general, the sludge treated with various extractants seemed
to exhibit a high potential for land application due to the presence
of a sufcient amount of nutrients (nitrogen and phosphorous) and
improvement in treated sludge characteristics, especially in terms
of decreases in pathogen and heavy metals content which were
low enough to comply with regulatory standards for land applica-
tion; and dominance of residual fractions in most metals (Cr, Cu
and Ni) present in the treated sludge. However, the high organic
matter content of the treated sludge might pose an odor problem
once disposed to land and hence may need to undergo further treat-
ment or stabilization, such as air drying, for several days before nal
disposal.
The main drawback of the process seemed to be its inefciency in
the extraction of the Cu metal. It was observed that even after treat-
ment with A. niger fermented liquid, Cu concentration (2025 mg/kg
DM) in the sludge still exceeded the recommended BMA guideline
of 900 mg/kg DM. However, this may not seem to pose a serious
problem since after treatment, Cu metal still predominates in resid-
ual form and, hence, is comparatively immobile.
Acknowledgments
Thanks are due to BIOTEC Central Research Unit, Thailand, for
providing the fungus A. niger used in the study; and the Department
of Drainage and Sewerage, Bangkok Metropolitan Administration
(BMA), for providing the sludge samples used.
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