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Biotechnology Advances 27 (2009) 4052

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Biotechnology Advances
j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / b i o t e c h a d v

Research review paper

A holistic approach to managing palm oil mill efuent (POME): Biotechnological


advances in the sustainable reuse of POME
Ta Yeong Wu, Abdul Wahab Mohammad , Jamaliah Md. Jahim, Nurina Anuar
Scale-up and Downstream Processing Research Group, Department of Chemical and Process Engineering, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor Darul Ehsan,
Malaysia

a r t i c l e

i n f o

Article history:
Received 24 December 2007
Received in revised form 19 August 2008
Accepted 21 August 2008
Available online 27 August 2008
Keywords:
Cleaner production
Palm oil mill efuent (POME)
Waste reusability
Fermentation substrate
Fertilizer
Animal feeds

a b s t r a c t
During the last century, a great deal of research and development as well as applications has been devoted to
waste. These include waste minimization and treatment, the environmental assessment of waste,
minimization of environmental impact, life cycle assessment and others. The major reason for such huge
efforts is that waste generation constitutes one of the major environmental problems where production
industries are concerned. Until now, an increasing pressure has been put on nding methods of reusing
waste, for instance through cleaner production, thus mirroring rapid changes in environmental policies. The
palm oil industry is one of the leading industries in Malaysia with a yearly production of more than
13 million tons of crude palm oil and plantations covering 11% of the Malaysian land area. However, the
production of such amounts of crude palm oil result in even larger amounts of palm oil mill efuent (POME),
estimated at nearly three times the quantity of crude palm oil. Normally, POME is treated using end-of-pipe
processes, but it is worth considering the potential value of POME prior to its treatment through introduction
of a cleaner production. It is envisaged that POME can be sustainably reused as a fermentation substrate in
the production of various metabolites, fertilizers and animal feeds through biotechnological advances. The
present paper thus discusses various technically feasible and economically benecial means of transforming
the POME into low or preferably high value added products.
2008 Elsevier Inc. All rights reserved.

Contents
1.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1.1.
A brief glance at palm oil mill efuent (POME) . . . . . . . . . . .
1.2.
Cleaner production as a sustainable strategy for POME management
2.
POME as a reusable product . . . . . . . . . . . . . . . . . . . . . . .
3.
Biotechnological advances in the sustainable reuse of POME. . . . . . . .
3.1.
Sustainable reuse of POME as fermentation media . . . . . . . . .
3.1.1.
Antibiotics . . . . . . . . . . . . . . . . . . . . . . . .
3.1.2.
Bioinsecticides . . . . . . . . . . . . . . . . . . . . . .
3.1.3.
Solvents (acetonebutanolethanol: ABE) . . . . . . . . .
3.1.4.
Polyhydroxyalkanoates (PHA) . . . . . . . . . . . . . . .
3.1.5.
Organic acids . . . . . . . . . . . . . . . . . . . . . .
3.1.6.
Enzymes . . . . . . . . . . . . . . . . . . . . . . . .
3.1.7.
Hydrogen . . . . . . . . . . . . . . . . . . . . . . . .
3.2.
Sustainable reuse of POME as fertilizer . . . . . . . . . . . . . .
3.3.
Sustainable reuse of POME as live food for animals and aquacultural
4.
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Corresponding author.
E-mail addresses: tayeong@hotmail.com (T.Y. Wu), wahabm@vlsi.eng.ukm.my, wahabm@yahoo.com (A.W. Mohammad), jamal@eng.ukm.my (J.M. Jahim), drnurina@eng.ukm.my
(N. Anuar).
0734-9750/$ see front matter 2008 Elsevier Inc. All rights reserved.
doi:10.1016/j.biotechadv.2008.08.005

T.Y. Wu et al. / Biotechnology Advances 27 (2009) 4052

41

1. Introduction
1.1. A brief glance at palm oil mill efuent (POME)
The Malaysian palm oil industry has grown rapidly over the years
and Malaysia has become the world's largest producer and exporter of
palm oil and its products. In 2003, more than 3.79 million hectares of
land were under oil palm cultivation, occupying more than one-third
of the total cultivated area in Malaysia and 11% of the total land area
(Yusoff and Hansen, 2007). In total, the palm oil industry contributes
signicantly towards the country's foreign exchange earnings and the
increased standard living among Malaysians.
In general, the palm oil milling process can be categorized into a dry
and a wet (standard) process. The wet process of palm oil milling is the
most common and typical way of extracting palm oil, especially in
Malaysia. It is estimated that for each ton of crude palm oil that is
produced, 57.5 t of water are required, and more than 50% of this water
ends up as palm oil mill efuent (POME) (Ahmad et al., 2003). Raw POME
is a colloidal suspension containing 9596% water, 0.60.7% oil and 45%
total solids. Included in the total solids are 24% suspended solids, which
are mainly constituted of debris from palm fruit mesocarp generated
from three main sources, i.e. sterilizer condensate, separator sludge and
hydrocyclone wastewater (Borja and Banks, 1994; Khalid and Wan
Mustafa, 1992; Ma, 2000). If the untreated efuent is discharged into
watercourses, it is certain to cause considerable environmental
problems (Davis and Reilly, 1980) due to its high biochemical oxygen
demand (25,000 mg/l), chemical oxygen demand (53,630 mg/l), oil and
grease (8370 mg/l), total solids (43,635 mg/l) and suspended solids
(19,020 mg/l) (Ma, 1995). The palm oil mill industry in Malaysia has thus
been identied as the one discharging the largest pollution load into the
rivers throughout the country (Hwang et al., 1978).
Ponding system is the most conventional method for treating POME
(Ma and Ong, 1985; Khalid and Wan Mustafa, 1992) but other processes
such as aerobic and anaerobic digestions, physicochemical treatments
and membrane ltration may also provide the palm oil industries with a
possible insight into the improvement of current POME treatment
process. However, the treatment that is based mainly on biological
treatments of anaerobic and aerobic systems, is quite inefcient to treat
POME, which unfortunately leads to environmental pollution issues
(Ahmad et al., 2005). This is because the high BOD loading and low pH of
POME, together with the colloidal nature of the suspended solids, render

Fig. 1. The 5 R policy (Olgun et al., 2004).

treatments by conventional methods difcult (Olie and Tjeng, 1972;


Stanton, 1974). A detailed cost calculation for Indonesia has also shown
that the conventional system of POME treatment, such as the ponding
system, is not only the system with the highest environmental pollution
and the lowest utilization of renewable resources, but also the system
giving rise to the lowest prot (Schuchardt et al., 2005).
1.2. Cleaner production as a sustainable strategy for POME management
Currently, end-of-pipe standards imposed through command and
control regulations are the basis of environmental legislation (Olgun
et al., 2004). However, an international trend promoting pollution
prevention through cleaner production, which is based on the 5 R
policy (Fig. 1); namely reduction, replacement, reuse, recovery and
recycling, is emerging. Within this context, it is proposed herewith
that a wastewater management based on the promotion of cleaner
production and environmentally sound biotechnologies could be

Table 1
The approximate composition (%) of major constituents, amino acids, fatty acids and minerals in raw POME (adapted from Habib et al., 1997)
Major constituents

Composition (%)

Amino acids

Composition (%)

Fatty acids

Composition (%)

Minerals

Composition (g/g dry weight)

Moisture
Crude protein
Crude lipid
Ash
Carbohydrate
Nitrogen-free extract
Total carotene
Total

6.99
12.75
10.21
14.88
29.55
26.39
0.019
100.789

Aspartic acid
Glutamic acid
Serine
Glycine
Histidine
Arginine
Threonine
Alanine
Proline
Tyrosine
Phenylalanine
Valine
Methionine
Cystine
Isoleucine
Leucine
Lysine
Tryptophan
Total

9.66
10.88
6.86
9.43
1.43
4.25
2.58
7.70
4.57
3.16
3.20
3.56
6.88
3.37
4.53
4.86
2.66
1.26
90.84

Caprylic acid (8:0)


Capric acid (10:0)
Lauric acid (12:0)
Myristic acid (14:0)
Pentadecanoic acid (15:0)
Palmitic acid (16:0)
Heptadecanoic acid (17:0)
10-Heptadecanoic acid (17:1)
Stearic acid (18:0)
Oleic acid (18:1n 9)
Linoleic acid (18:2n6)
Linolenic acid (18:3n3)
-linolenic acid (18:3n6)
Arachidic acid (20:0)
Eicosatrienoic acid (20:3n6)
Eicosatetraenoic acid (20:4n6)
Eicosapentaenoic acid (20:5n3)
Total

2.37
4.29
3.22
12.66
2.21
22.45
1.39
1.12
10.41
14.54
9.53
4.72
0
3.56
2.04
1.12
0.36
95.99

Fe
Zn
P
Na
Mg
Mn
K
Ca
Co
Cr
Cu
Ni
S
Se
Si
Sn
Al
B
Mo
As
V
Pb
Cd

11.08
17.58
14377.38
94.57
911.95
38.81
8951.55
1650.09
2.40
4.02
10.76
1.31
13.32
12.32
10.50
2.30
16.60
7.60
6.45
9.09
0.12
5.15
0.44

42

T.Y. Wu et al. / Biotechnology Advances 27 (2009) 4052

included as a part of the POME management in Malaysia in order to


attain a sustainable development. Such a strategy could take
advantage of the current international interest in promoting cleaner
production as the driving force of a new and sustainable industrial
development style. This review paper thus describes various technically feasible means of transforming the POME into different addedvalue products through cleaner production and environmentally
sound biotechnologies for enabling the balance between environmental protection and a sustainable reuse of bioresources found in the
POME.
2. POME as a reusable product
The high compositions and concentrations of carbohydrate,
protein, nitrogenous compounds, lipids and minerals in POME
(Hwang et al., 1978; Phang, 1990; Habib et al., 1997) render it possible
to reuse the efuent for biotechnological means (Table 1). Chemical
analysis indicates that the rod-like particle fraction (Fig. 2) available in
the POME corresponds to carbohydrate in nature. After treatment
with phenol/sulfuric acid, the fraction shows a maximum absorption
at approximately 480 nm (Fig. 3), indicating the possible presence of
pentose, a building unit for insoluble carbohydrates (Ho and Tan,
1983). The presence of pentose in POME has been reported previously
(Hwang et al., 1978) and its most likely sources are the cell walls.
Water-soluble carbohydrates, in terms of glucose, reducing sugars and
pectin, are also found to be present in the soluble fraction of POME.
However, the low concentrations of total soluble carbohydrate
(0.390 g/100 ml POME) may restrict the usefulness of the soluble
fraction of POME as a possible feedstock for substrate conversion via
direct single-cell protein production (Ho et al., 1984). Preliminary
investigations on enzymatically hydrolyzed substrates from POME
have indeed demonstrated the possibility of such substrates supporting the growth of Candida tropicalis (Wang et al., 1981). On the other
hand, Barker and Worgan (1981) noted that unhydrolyzed POME

Fig. 3. Absorption curves for the rod-like particles after treatment with phenol/
sulphuric acid and for a number of other simple sugars (Ho and Tan, 1983).

could support good growth of Aspergillus oryzae in the presence of an


added inorganic nitrogen source. Their results also revealed that
celluloses, polyphenols and nitrogenous compounds were the least
biodegradable of the substrate constituents. This lends further
support to the view that a proper hydrolysis step is essential in
obtaining an optimal level of readily biodegradable sugars from the
plant cell materials for a meaningful microbial bioconversion.

Fig. 2. Centrifugal fractionation of POME (Ho and Tan, 1983).

Table 2
Various products or metabolites produced in bioprocesses during the reuse of POME or its derivatives as substrates
Product

Microorganism

Penicillin

Penicillium chrysogenum
FR2284
Penicillin
Penicillium chrysogenum
FR2284
Bioinsecticide Bacillus thuringiensis H-14

Fermentation medium based on POME

Fermentation conditions

Fermentation timea
(h)

Maximum production

Reference

50% (v/v) concentrated POME + KH2PO4 +


(NH4)2SO4
50% (v/v) concentrated POME + KH2PO4 +
(NH4)2SO4 + NH4 lactate
Raw POME

300 rpm, 30 C, 2% (v/v) inoculum, ask


fermentation
300 rpm, 30 C, 2% (v/v) inoculum,
ask fermentation
150 rpm, 30 C, initial pH = 6.9, ask
fermentation
150 rpm, 30 C, initial pH = 6.9, ask
fermentation
30 C, 10% (v/v) inoculum, initial pH = 5.8, ask
fermentation
30 C, 10% (v/v) inoculum, initial pH = 5.8, ask
fermentation
200 rpm, 37 C, 10% (v/v) inoculum, pH was
switched from 6.2 to 5.5 at 9 h, 2 g/l/h glucose
feeding started at 10 h, bioreactor fermentation
35 C, 10% (v/v) inoculum, initial pH = 5.8, ask
fermentation
Not clearly stated

72

602 U/ml

Suwandi (1991)

72

715 U/ml

Suwandi (1991)

ABE
ABE

ABE

2.0 10 spores/ml

Suwandi (1991)

Not clearly stated

A = 0.45 g/l, B = 2.47 g/l,


E = 0.49 g/l
A = 0.33 g/l, B = 2.30 g/l,
E = 0.43 g/l
A = 5.78 g/l, B = 6.78 g/l

Mun et al. (1995)

36 (for ABE)

A = 1.97 g/l, B = 1.74 g/l,


E = 0.3 g/l
ABE = 3.8 g/l

Kalil et al. (2003),


Pang et al. (2004)
Kalil et al. (2003)

ABE

35 C, 10% (v/v) inoculum, initial pH = 6, ask


fermentation
Oscillated at 0.45 Hz, 35 C, 10% (v/v) inoculum,
initial pH = 6, oscillatory ow bioreactor
fermentation
Oscillated at 0.78 Hz, 35 C, 10% (v/v)
inoculum, initial pH = 5.8, oscillatory ow
bioreactor fermentation
250 rpm, 35 C, 10% (v/v) inoculum,
initial pH = 5.8, stirred tank bioreactor
fermentation
30 C, pH was controlled at 7, photobioreactor
fermentation

30 (for A) 24 (for
E)
42 (for A) 30 (for
E)

A = 1.2 g/l, B = 0 g/l,


E = 0.5 g/l
A = 0.7 g/l, B = 0 g/l,
E = 0.6 g/l

Takriff et al. (2005)

ABE

48 (for ABE)

A = 0.05 g/l, B = 1.54 g/l,


E = 0 g/l

Masngut et al.
(2006, 2007)

60 (for ABE)

A = 0.13 g/l, B = 0.50 g/l,


E = 0.24 g/l

Masngut et al. (2007)

200

4 g/l

Hassan et al. (1996)

30 C, pH was controlled at 7, photobioreactor


fermentation
400 rpm with an aeration rate of 0.75 l/min,
Standard medium with feeding of
30 C, pH was controlled at 7, stirred tank
acetic acid obtained from
bioreactor fermentation
anaerobically digested POME
Concentrated organic acids from the anaerobically digested 400 rpm with an aeration rate of 0.75 l/min,
POME (100 g/l of total acids with acetic:propionic = 3:1)
30 C, pH was controlled at 7, bioreactor
fermentation
1,000 rpm with an aeration rate of 1.5 l/min,
High concentration of POME with
30 C, pH was controlled at 7, sequencing batch
490 COD/N ratio (g COD/g N) and
reactor
160 COD/P ratio (g COD/g P)
fermentation
POME + palm oil sludge
30 C, pH was controlled at 7, bioreactor
fermentation
POME + palm oil sludge in the ratio of 1:1
300 rpm, 30 C, pH was controlled at 5,
stirred tank bioreactor fermentation
1% (w/w) POME + 2% (w/w) wheat our
150 rpm, 2730 C, initial pH = 3, inoculum size
of 2% (106 spores/ml), ask fermentation
150 rpm, 32 C, initial pH = 5, inoculum size of
2% (w/w) POME + 4% (w/w)
2% (106 spores/ml),
wheat our + 4% (w/w) glucose with no
ask fermentation
added ammonium nitrate (optimized medium)
Retentate of POME
300 rpm, 35 C, 5% (v/v) inoculum, ask
fermentation

Dilution rate = 0.024


d 1
17

N2 g/l

Hassan et al. (1997b)

1.8 g/l

Hassan et al. (1997c)

65

6.25 g/l

Hassan et al. (2002)

Not clearly stated

24.24 g/l

Md Din et al. (2006b)

24

7.8 g/l

Hassan et al. (1996)

84

1014 g/l

Yee et al. (2003)

48

0.28 g/l

Jamal et al. (2005)

168

5.2 g/l

Alam et al. (2008)

120

0.079 g/l

Wu et al. (2005)

90% (v/v) particulate fraction of raw


POME
Raw POME

Particulate fraction of raw POME


Particulate fraction of raw POME

ABE

Clostridium acetobutylicum
NCIMB 13357

Particulate fraction of raw POME

ABE

Clostridium acetobutylicum
NCIMB 13357

Particulate fraction of raw POME

PHA

Rhodobacter sphaeroides
IFO 12203

PHA

Rhodobacter sphaeroides
IFO 12203
Alcaligenes eutrophus H16
(ATCC 17699)

Synthetic waste based on organic


acids proles obtained during POME
treatment
Anaerobically digested POME

PHA

PHA

Ralstonia eutropha
ATCC 17699

PHA

Mixed cultures

Organic acids

Mixed cultures

Organic acids

Mixed cultures

Citric acid

Aspergillus (A103)

Citric acid

Aspergillus niger (A103)

Itaconic acid

Aspergillus terreus IMI 282743

Not clearly stated


35 (for A) 45 (for
B)
48 (for ABE)

Mun et al. (1995)


Somrutai et al.
(1996)

Takriff et al. (2005)

T.Y. Wu et al. / Biotechnology Advances 27 (2009) 4052

ABE

1% (w/v) concentrated POME in powder


form
Clostridium saccharoperbutylacetonicum Separator sludge
N1-4 (ATCC 13564)
Clostridium saccharoperbutylacetonicum Sterilized condensate
N1-4 (ATCC 13564)
Model medium for raw POME
Clostridium aurantibutyricum
ATCC 17777

Clostridium acetobutylicum
NCIMB 13357
Immobilized Clostridium
saccharoperbutylacetonicum
N1-4
Clostridium acetobutylicum
NCIMB 13357
Clostridium acetobutylicum
NCIMB 13357

Suwandi (1991)

7.0 10 spores/ml

72

Bioinsecticide Bacillus thuringiensis H-14


ABE

72

43
(continued on next page)

44

Table 2 (continued)
Product

Microorganism

Fermentation medium based on POME

Fermentation conditions

Fermentation timea
(h)

Maximum production

Reference

Cellulase
(CMCase)

Aspergillus niger ATCC 6275

POME with added nutrients +


0.6 g/l NH4NO3

72

1.09 U/ml

Prasertsan et al.
(1997)

Cellulase
(CMCase)
Cellulase
(CMCase)
Cellulase
(CMCase)
Cellulase
(CMCase)

Aspergillus niger

50% (v/v) raw POME

51

1.040 U/ml

Trichoderma harzianum

50% (v/v) raw POME

45

1.227 U/ml

Mixed culture (1:1) of Aspergillus


niger and Trichoderma harzianum
Myceliophthora thermophila

50% (v/v) raw POME

45

0.656 U/ml

24

3.495 U/ml

Mashitah
(2002)
Mashitah
(2002)
Mashitah
(2002)
Mashitah
(2002)

Trichoderma harzianum

2% (w/v) particulate fraction of


POME + 3% (w/v) wheat our
1% (w/w) POME sludge

200 rpm, room temperature, inoculum size was


7.5 105
spores/ml, ask fermentation
300 rpm with an aeration rate of 4 l/min, 30 C,
10% (v/v) inoculum, bioreactor fermentation
300 rpm with an aeration rate of 4 l/min, 30 C,
10% (v/v) inoculum, bioreactor fermentation
300 rpm with an aeration rate of 4 l/min, 30 C,
10% (v/v) inoculum, bioreactor fermentation
300 rpm with an aeration rate of 4 l/min, 45 C,
10% (v/v) inoculum, initial pH 5.5 was
uncontrolled until 6.0, bioreactor
fermentation
250 rpm, 30 C, 3% (v/v) inoculum,
initial pH = 4, ask fermentation
Not clearly stated

96

13.44 U/ml

Alam et al. (2006a)

144

33 U/ml

10% (v/v) supernatant of POME + another


nine different types of supporting nutrients
2% particulate fraction of POME + 1%
wheat our
1% (w/w) POME sludge

200 rpm, 55 C, 5% (v/v) inoculum,


initial pH = 7, ask fermentation
250 rpm, 40 C, 1% (v/v) inoculum,
initial pH = 6, ask fermentation
Not clearly stated

48

12.11 U/ml

96

3.373 U/ml

Chowdhury et al.
(2006)
Laohaprapanon et al.
(2007)
Alam et al. (2006b)

144

5.038 U/ml

200 rpm, 37 C, 10% (v/v) inoculum, constant


pH at 6.8,
bioreactor fermentation
200 rpm, room temperature, inoculum size
was 7.5 x 105
spores/ml, ask fermentation
Aeration rate of 2.5 l/min, 30 C, 10% (v/v)
inoculum, bioreactor fermentation
200 rpm, 55 C, 5% (v/v) inoculum,
initial pH = 7, ask fermentation

20

0.4 U/ml

96

22.77 U/ml

Prasertsan et al.
(1997)

96

0.448 U/ml

Cheng (2006)

96

50.98 U/ml

Laohaprapanon et al.
(2007)

96

129 U/ml

Wu et al. (2006a)

Not clearly stated

23.82 mmol H2/


(1-medium)

Morimoto et al.
(2004)

38

4,708 ml H2/(l-medium)

Atif et al. (2005)

168

Vijayaraghavan
and Ahmad (2006)

At steady state
(during day 2228)

0.42 l biogas/g
CODdestroyed
with 57% hydrogen
content
4.4 l H2/(1-medium)
per day

At steady state
(during day 2228)

6.1 l H2/(1-medium)
per day

O-Thong et al. (2007)

48

6.33 H2/(1-medium)

O-Thong et al.
(2008a)

Penicillium (P1-EFB)
Isolate SO1

Lignin
peroxidase
Lignin
peroxidase
Lipase

Phanerochaete chrysosporium
Penicillium (P1-EFB)
Clostridium aurantibutyricum
ATCC 17777

Model medium for raw POME

Xylanase

Aspergillus niger ATCC 6275

POME with added nutrients +


0.6 g/l NH4NO3

Xylanase

Aspergillus terreus SUK-1

Raw POME

Xylanase

Isolate SO1

Protease

Aspergillus terreus IMI 282743

10% (v/v) supernatant of POME +


another nine different types of supporting
nutrients
75% (v/v) retentate of POME

Hydrogen

Mixed culture from POME sludge

Hydrogen

Mixed culture from POME sludge

Hydrogen

Mixed culture
(isolated from cow dung)

Raw POME

Hydrogen

Thermophilic microora

Raw POME

Hydrogen

Thermophilic microora

Raw POME + Fe2+ + peptone + Na2


HPO42H2O

Hydrogen

Thermoanaerobacterium-rich
sludge

Raw POME + 257 mg Fe2+/l + a


C/N ratio of 74 + a
C/P ratio of 559 + 0.3 g NaHCO3
(optimized medium)

1% glucose + 0.2% yeast extract + 0.018%


magnesium chloride hexahydrate + 0.5%
(w/v) POME sludge
Raw POME + 2.5% (w/v) POME sludge

A = Acetone, B = Butanol, E = Ethanol.


PHA = Polyhydroxyalkanoates.
a
The fermentation time is the time required to reach a maximum product concentration.

250 rpm, 37 C, 5% (v/v) inoculum, ask


fermentation
60 C, pH was uncontrolled, bioreactor
fermentation
200 rpm, 60 C, pH was controlled at 5.5,
bioreactor fermentation
pH was controlled at 5, anaerobic contact
lter fermentation

200 rpm, 60 C, pH was controlled at 5.5,


anaerobic sequencing batch reactor
fermentation
200 rpm, 60 C, pH was controlled at 5.5,
anaerobic sequencing batch reactor
fermentation
60 C, initial pH = 5.5, 10 ml seed sludge
inoculum, serum bottle fermentation

et al.
et al.
et al.

Chowdhury et al.
(2006)
Somrutai et al.
(1996)

O-Thong et al. (2007)

T.Y. Wu et al. / Biotechnology Advances 27 (2009) 4052

Cellulase
(FPase)
Cellulase
(FPase)
Cellulase

50% (v/v) raw POME

et al.

T.Y. Wu et al. / Biotechnology Advances 27 (2009) 4052

Nitrogen is originally present in POME in the form of organic (protein)


nitrogen and as time progresses the organic nitrogen is gradually
converted to ammoniacal nitrogen with a molecular weight of 1735 kg/
kmol (Chow, 1991). According to Ho and Tan (1988), the nutrient balance
in terms of the average ratio of BOD:N:P for raw POME is 100:4:0.3.
Muhrizal et al. (2006) reported that POME is characterized by a low C:N
ratio (C:NPOME = 6.54) as compared to sawdust (C:Nsawdust = 185.74),
purun (C:Npurun =88.32) and peat (C:Npeat = 50.31). The amino acids of
POME and their approximate compositions (%) are shown in Table 1. The
major portion of proteins in POME is tightly associated with its insoluble
part (Ho et al.,1984). This may perhaps account for the low digestibility of
proteins in POME found by Devendra et al. (1981).
Only N, P, K, Mg and Ca are consistently present in relatively large
amounts in the POME (Ho et al., 1984; Habib et al., 1997; Muhrizal et al.,
2006) (Table 1). Muhrizal et al. (2006) also reported that POME has a
high content of Al as compared to chicken manure and composted
sawdust. It would thus seem that the probable usefulness of POME as
fertilizer or animal feed substitute, in terms of providing sufcient
mineral requirements, depends mainly on the soluble fraction of
POME. Toxic metals, such as Pb, can also be found in POME (Habib et al.,
1997) but their concentrations are usually below sublethal levels
(N17.5 g/g) (James et al., 1996). POME is thus not toxic for plants and
animals. Pb is found in POME due to contamination from plastic and
metal pipes, tanks and containers where Pb is widely employed in
paints and glazing materials (James et al., 1996).
The reusability of POME especially as animal feed is arguable
because another important factor that needs to be taken into
consideration is its lignin content. Lignin is a recalcitrant, waterinsoluble organic chemical (Palm and Rowland, 1997). A high content
of lignin in organic materials is known to slow down their decomposition (Klepper et al., 1990; Tian et al., 1992). High lignin contents
(0.412 g/100 ml POME) also present major barriers with regard to
digestion of roughage by-product feeds from eld and tree crops by
both ruminants and non-ruminants (Ho et al., 1984). Lignin is known to
be highly resistant to chemical degradation thus giving rise to its low
digestibility. This has been clearly illustrated by the work of Devendra
et al. (1981) on the use of POME, in both raw and dehydrated forms, as
animal feed. Therefore, to allow the POME to be reused effectively as
animal feed, Webb et al. (1975) have suggested that efuent products
can be nutritionally improved by reducing the ash and ber content as
well as increasing the protein content on par with imported feed meal.
The composition of raw POME with regard to saturated and
unsaturated fatty acids other than polyunsaturated fatty acids is
shown in Table 1. Here, myristic acid, palmitic acid, stearic acid and
oleic acid are present in compositions higher than other saturated
fatty acids. The 20 carbon chained polyunsaturated fatty acids such as
eicosatrienoic acid (20:3n6), eicosatetraenoic acid (20:4n6) and
eicosapentaenoic acid (20:5n3), which are available in raw POME, are
essential for the proper development of marine sh, shrimp larvae and
fry (Oka et al., 1982). According to Habib et al. (1997), these substances
have been accumulated and synthesized in higher amounts for
chironomid larvae grown in POME than those grown in algal culture.

45

3.1. Sustainable reuse of POME as fermentation media


The possibility of reusing POME as fermentation media is largely
due to the fact that POME contains high concentrations of carbohydrate, protein, nitrogenous compounds, lipids and minerals (Hwang
et al., 1978; Phang, 1990; Habib et al., 1997). Suwandi, (1991) and Wu
et al., (2006b) pointed out the possibility of recovering and concentrating the available bioresources in POME by an ultraltration
process in order for the concentrated bioresources to be reused more
effectively as fermentation media. According to Wu et al. (2007),
POME and its derivatives have been exploited as fermentation media
to produce various products/metabolites such as antibiotics, bioinsecticides, solvents, polyhydroxyalkanoates, organic acids as well as
enzymes to varying degrees of success. The hydrogen production from
POME during anaerobic treatment has also been intensively studied
(Atif et al., 2005; Vijayaraghavan and Ahmad, 2006) since the
generated hydrogen and its combustion products do not count as
green house gases (Koroneos et al., 2004). However, it has been reported that POME also contains certain powerful water-soluble
antioxidants, phenolic acids and avonoids (Wattanapenpaiboon
and Wahlqvist, 2003) that may inhibit the growth development in
microorganisms (Lin et al., 2005; Uzel et al., 2005).
Table 2 displays the various products or metabolites produced in
bioprocesses by reusing POME or its derivatives as substrates.
3.1.1. Antibiotics
Studies on ultraltered POME concentrates or retentates as growth
media for Penicillium chrysogenum in the production of antibiotics have
been conducted some time ago (Suwandi and Mohammad, 1984;
Suwandi, 1991). It was found that a supplementary nitrogen source was
required in the ratio C:N = 20:1 to produce a maximum mass of
P. chrysogenum (Suwandi and Mohammad, 1984). However, no attempts
were made to assay the penicillin produced during the process of
incubation. Suwandi (1991) later determined the effect of the POME
concentration and the addition of chemicals on the production of
penicillin in cultured broths for periods of 4 days. He found that smaller
amounts of penicillin were produced in POME as compared to in Deo
and Gaucher's (1984) standard medium. Suwandi (1991) argued that the
low production of penicillin was due to the lower concentration of
carbohydrates (23 g/l) in POME as compared to in the standard medium,
which contained 35 g/l carbohydrates. The addition of ammonium
lactate to POME stimulated the production of penicillin.

3. Biotechnological advances in the sustainable reuse of POME

3.1.2. Bioinsecticides
Nor and Mahadi (1986) as well as Suwandi (1991) embarked on a
research topic related to the use of ultraltered POME concentrate or
retentate as a medium for Bacillus thuringiensis to produce bioinsecticide for mosquito control. Suwandi (1991) observed that a medium
containing 1% (w/v) retentate in powder form was as good as the
standard medium of glucose yeast extract salts in terms of spore
production by B. thuringiensis. The ability of the retentate to support
and stimulate the growth of B. thuringiensis could be attributed to the
proper ratio of carbon and nitrogen as well as to sufcient levels of
ions (such as Mg, Ca, Mn, etc.) in the POME.

Chemical analyses of POME with respect to its proximate composition have been carried out (Wood, 1977; Hwang et al., 1978; Ho et al.,
1984; Habib et al.,1997), and these analyses are of vital importance in the
understanding of the properties of POME in relation to formulating
waste-utilization programs and efcient wastewater management
processes. This is particularly true in view of the increasing emphasis
placed on the zero discharge concept and innovative technology for
sustainable development. An important case is the production of biogas
and other metabolites by fermentation processes. Of no less importance
is the possibility of recovering bioresources from POME, or its conversion
into useful substitutes for animal feed and fertilizer.

3.1.3. Solvents (acetonebutanolethanol: ABE)


Separator sludge and sterilized condensate from POME have been
tested for their suitability to be reused as fermentation media for ABE
production by Clostridium saccharoperbutylacetonicum N1-4 (ATCC
13564) (Mun et al., 1995). Separator sludge was found to be the better
medium between the two for supporting the production of ABE as no
mineral supplements were required. The enzymes produced by
C. saccharoperbutylacetonicum N1-4 (ATCC 13564) were sufcient to
hydrolyze the mixed carbohydrates and celluloses found in the
separator sludge. Hipolito et al. (2007) later reconrmed that enzymatic
hydrolysates of separator sludge could be used as media for inoculum

46

T.Y. Wu et al. / Biotechnology Advances 27 (2009) 4052

development since the cultures inoculated with C. saccharoperbutylacetonicum N1-4 (ATCC 13564) using the sludge hydrolysate produced the
same concentration of butanol as compared to in a potato glucose
medium, whereas the corresponding ethanol production was increased
by over 100%. The authors concluded that the enzymatic hydrolysates of
separator sludge could serve as growth and ABE fermentation media as
well as a source of nitrogen and trace elements.
Somrutai et al. (1996) investigated the possibility of acetonebutanol
fermentation by C. aurantibutyricum ATCC 17777 in a model medium for
raw POME. They found that by decreasing the pH from 6.2 to 5.5 at 9 h
and starting an hourly glucose feeding (2 g/l) at 10 h, it was possible to
obtain 30% of the oil hydrolysis as well as a production of 5.78 g/l acetone
and 6.78 g/l butanol. Kalil et al. (2003) studied the direct use of raw
POME as a fermentation medium for ABE production by
C. acetobutylicum NCIMB 13357 and immobilized C. saccharoperbutylacetonicum N1-4 in a batch culture system. It was found that
C. acetobutylicum NCIMB 13357 produced the highest total ABE in 90%
(v/v) particulate fraction of raw POME after 48 h of fermentation at an
initial pH of 5.8 while immobilized cells of C. saccharoperbutylacetonicum
N1-4 could be reused for at least 5 times in 100% (v/v) particulate
fraction of raw POME without losing their performance (Kalil et al.,
2003). Similar results were also obtained by Pang et al. (2004) with the
addition of hydrogen production up to 28.5 ml.
An oscillatory ow bioreactor was used to enhance the production
of ABE in the raw POME (Takriff et al., 2005; Masngut et al., 2006,
2007), and initial results showed that by using a particulate fraction of
raw POME as the fermentation medium, C. acetobutylicum NCIMB
13357 could produce 31% higher concentrations of ABE, especially
acetone, in ask as compared to an oscillatory ow bioreactor (Takriff
et al., 2005). On the other hand, Masngut et al. (2006, 2007) found that
C. acetobutylicum NCIMB 13357 could only produce higher amounts of
butanol in shorter periods of time when particulate fractions of raw
POME were used in an oscillatory ow bioreactor as opposed to with a
reinforced clostridial medium in a stirred tank bioreactor. Pang et al.
(2004) also claimed that the concentration of ABE produced by
C. acetobutylicum NCIMB 13357 in a particulate fraction of raw POME
was 20-fold that obtained in the reinforced clostridial medium.
3.1.4. Polyhydroxyalkanoates (PHA)
Over 40% of the total polyhydroxyalkanoates (PHA) production
cost is estimated to account for the raw materials of the overall
process and more than 70% of this cost is attributed to the carbon
source (Lee et al., 1999). POME can be considered as an alternative, nocost reusable substrate for PHA production. According to Hassan et al.,
(1997a), with a content of 50% PHA in the dried cells and 2% dissolved
in the chloroform, the calculated minimum cost for obtaining PHA
from POME is below 2 US$/kg. By increasing the PHA content in the
cell from 50% to 80%, the unit cost of PHA could be slightly reduced;
whereas an increase in the amount of PHA dissolved in chloroform
from 2% to 5% would result in a remarkable reduction of the PHA cost
to less than 1 US$/kg (Hassan et al., 1997a).
Nevertheless, POME is usually presented in complicated forms that
cannot be directly reused by PHA-producing species such as Ralstonia
eutropha, a representative bacterium for PHA synthesis (Salim et al.,
2006). It was proposed that an anaerobic treatment of POME could be
coupled with PHA production using photosynthetic bacteria to reduce
PHA production costs (Hassan et al., 1996, 1997b). According to Hassan
et al. (1996), it was critical to maintain the pH at 7 in the anaerobic
treatment of POME by sludge in the rst stage of the process, in order
for only acetic and propionic acid to be produced and not formic acid
and biogas. With increasing concentrations of formic acid (for a pH
maintained below 4), the PHA yield and content in Rhodobacter
sphaeroides IFO 12203 dropped from 0.50 g/g and 67% to 0.21 g/g and
18%, respectively. Hassan et al. (1997b) later found that the presence of
sludge in the anaerobically treated POME inhibited PHA accumulation
by R. sphaeroides IFO 12203. This was attributed to the PHA being

produced in a POME without sludge as opposed to a treated POME


with sludge. A low concentration of ammonium would accelerate the
PHA production in a synthetic waste with an organic acid prole,
which was observed during POME treatment (Hassan et al., 1996).
However, Hassan et al. (1997b) found that addition of ammonium and
phosphate to anaerobically treated POME was required to maintain
the cell activity and production of PHA since neither ammonium nor
phosphate was present in the anaerobically treated POME. In total, the
organic acid concentrations obtained from anaerobically treated
POME were too low (Hassan et al., 1996) for it to be reused as raw
material in the production of PHA on an industrial scale. The
underlying reason was that this would require a production reactor
with a much larger size than that of a reactor for normal bioplastic
production.
Therefore, Hassan et al. (1997c) used an anion exchange resin to
separate and concentrate the acetic acid from the anaerobically treated
POME so that the concentrated acetic acid could be reused as a substrate
in the fed-batch production of PHA by Alcaligenes eutrophus H16 (ATCC
17699). They found that the PHA content was comparable to that of the
batch and fed-batch PHA production by Alcaligenes (around 18% to 76%),
but the overall PHA productivity obtained was less than the 0.53 g
PHAs/l h obtained by other researchers (Suzuki et al., 1986; Ishizaki and
Tanaka, 1991; Lee et al., 1993; Yamane et al., 1996). This might be due to
the low cell concentration when concentrated acetic acid separated from
POME was incorporated into the standard medium.
Hassan et al. (2002) showed that organic acids in the anaerobically
digested POME could be concentrated by evaporation for use as
substrates in the fed-batch non-sterile PHA fermentation system
using R. eutropha ATCC 17699. Although the proposed overall zero
emission system appeared to be practical, major drawbacks were
found, including the rather low yield and productivity of PHA by R.
eutropha when the concentrated organic acids from POME were used
as compared to synthetic organic acids. This could be due to the high
presence of ammonium (1.5 g/l) or other compounds in the
anaerobically digested POME concentrate (Hassan et al., 2002).
According to Md Din et al. (2006a,b), it was possible to use mixed
cultures to produce PHA in POME since most prokaryotes are capable of
PHA production (Chua et al., 2003). Md Din et al. (2006a) noted that by
using mixed cultures and POME, different types of PHA-constituents
could be obtained. The harvesting of these PHA-constituents was more
reliable for use as biodegradable plastics materials as opposed to a single
PHA-constituent. Md Din et al. (2006b) maintained a type of mixed
culture in a sequencing batch reactor, and a high concentration of POME
was proposed for this system in order to generate autotrophic rather
than heterotrophic bacteria in the production of PHA. However, the
average PHA production by using POME could only reach 44% of the
cells' dry weight, indicating that an optimization of the PHA sludge
content must be carried out by varying the oxygen rate, feeding regime
or transient conditions.
3.1.5. Organic acids
It is a well-known fact that a variety of organic acids are produced
as intermediates during the anaerobic treatment of biological wastes
(Kotz et al., 1969; Zeikus, 1980; Archer, 1983). As mentioned earlier,
POME could be put to sustainable use for organic acid production,
whereby the latter could be utilized as raw material for PHA
production (Hassan et al., 1996, 1997b,c, 2002). According to Hassan
et al. (1996), the conversion to organic acids from the BOD sources in
POME by R. sphaeroides IFO 12203 was more than 70%, and acetic acid
and formic acid were the predominant substances at higher and lower
pH, respectively. Yee et al. (2003) showed that by incorporating a
sludge recycling system with the freezingthawing method in the
anaerobic treatment of POME, the retention time could be lowered to
3.5 days without affecting the organic acid production. Moreover, Yee
et al. (2003) found that the effect of freezing and thawing produced
concentrated viable and ruptured cells in recycled sludge with a total

T.Y. Wu et al. / Biotechnology Advances 27 (2009) 4052

nitrogen source of 45 g/l as a result of the ruptured cells releasing the


nitrogen sources that were required to support the growth of higher
cell densities.
Some organic acids, such as citric acid (Jamal et al., 2005; Alam
et al., 2008) and itaconic acid (Wu et al., 2005), could be produced
under aerobic conditions using POME as the substrate. Jamal et al.
(2005) screened potential microorganisms for citric acid production
and found that Aspergillus (A103) produced the highest concentration
of citric acid after 2 days of fermentation by using POME and wheat
our as medium. Alam et al. (2008) later found that higher production
of citric acid could be obtained with longer time of fermentation (up to
7 days of fermentation) and addition of co-substrates (glucose and
wheat our) into POME. Wu et al. (2005) employed raw POME and its
derivatives to produce itaconic acid by using Aspergillus terreus IMI
282743. However, only little itaconic acid could be obtained. It was
postulated that this low production was mainly due to the wild and
unsuitable strain of A. terreus IMI 282743.
3.1.6. Enzymes
The particulates in the POME, comprised mainly of plant cell debris
and fragments, are entirely organic in nature as indicated by the very
low ash contents (Ho et al., 1984). The availability of such particulates
may provide a potential substrate for production of cellulase
(Prasertsan et al., 1997; Mashitah et al., 2002; Alam et al., 2006a;
Chowdhury et al., 2006; Laohaprapanon et al., 2007), xylanase
(Prasertsan et al., 1997; Cheng, 2006; Laohaprapanon et al., 2007)
and lignin peroxidase (Alam et al., 2006b; Chowdhury et al., 2006) in
POME. The optimization of cellulase (CMCase) and xylanase productions from Aspergillus niger ATCC 6275 was investigated under both
submerged and solid state fermentation (Prasertsan et al., 1997).
Prasertsan et al. (1997) found that the addition of 0.6 g/l NH4NO3 into
the POME during submerged fermentation increased the maximum
production of xylanase and CMCase with up to 156% and 43%,
respectively.
Prasertsan et al. (1997) also revealed that the enzyme production
was lower in POME when the fermentation process was conducted in
a fermenter, which might be due to the destruction of mycelium by
shearing forces, thus causing the cessation of enzyme synthesis and
the induction of enzyme inhibition (Wase et al., 1985). Contrarily,
Cheng (2006) reported on 107% higher activity of xylanase obtained
by A. terreus SUK-1 in the fermenter as compared to the shake ask
when raw POME was used as the substrate. However, Cheng (2006)
also found a 31% lower activity of xylanase with the raw POME as
opposed to the Mandels medium (Mandels, 1974).
Mashitah et al. (2002) used axenic and mixed cultures of
mesophilic and thermophilic fungi to produce cellulase in the
POME, in which case they found that the axenic culture of Trichoderma harzianum was superior to the mixed culture of A. niger and T.
harzianum in terms of CMCase and exoglucanase production. This low
production of cellulase in the mixed culture was believed to be due to
the competition of nutrient consumptions between the fungi in the
POME. Moreover, the genus Aspergillus is known to release other
metabolites such as endotoxins (Debeaupuis and Lafont, 1978) and
proteases (Aunstrup, 1974), which may inhibit the activity of cellulase.
Mashitah et al. (2002) also noted that the thermophilic fungi, namely
Myceliophthora thermophila grew well and produced a higher amount
of cellulase in POME as compared to the mesophilic fungus. Alam et al.
(2006a) utilized a combination of POME and wheat our as the
substrate in the optimization process for maximizing cellulase
production by T. harzianum. They found that the linear effect of
agitation was not highly signicant for cellulase production but this
parameter should not be totally overruled because of its interactive
effect with wheat our.
Six out of twenty strains of Penicillium were isolated from four
different sources of POME sludge and selected for the production of
cellulase and lignin peroxidase in the POME (Chowdhury et al., 2006).

47

The results revealed Penicillium (P1-EFB), which was isolated from


empty fruit bunches, displayed the best potential strain for biodegradation in liquid state bioconversion of POME at pH 7.3. The whiterot fungus Phanerochaete chrysosporium was used for lignin peroxidase production with a combination of POME and wheat our as the
substrate (Alam et al., 2006b). It was observed that, although wheat
our could be used as an additional carbon source to enhance the
initial growth of P. chrysosporium, more than 2% wheat our was
expected to further decrease the enzyme activity of the lignin
peroxidase. Laohaprapanon et al. (2007) found that the isolate SO1,
which was isolated from a soil near to the rst anaerobic pond of palm
oil mill, produced the highest activity of cellulase and xylanase in
comparison with other isolate of microorganisms. Isolate SO1 was an
aerobic, Gram-positive, rod-shaped and thermo-tolerant microorganism, which was able to reduce the oil content in the sediment of POME
up to 85.32%.
In view of the fact that POME contains considerable amounts of oil
and grease, it is possible to reuse POME as a substrate in lipase
production and isolate oil-degrading microorganisms from efuent
treatment ponds of POME. Somrutai et al. (1996) found that Clostridium aurantibutyricum ATCC 17777 was able to produce lipase in the
model medium for POME in which high rate of oil hydrolysis (46.0%)
was observed at pH of 6.8. Razak et al. (1997) were able to isolate
thermophilic fungi, namely Rhizopus oryzae and Rhizopus rhizopodiformis, from POME. They found that the fungi could produce
remarkable amounts of extracellular lipases in the dened medium.
Furthermore, the isolated R. oryzae from POME could produce
membrane-bound lipases that were active in both acidic and alkaline
conditions as opposed to extracellular lipases from the same fungi
(Razak et al., 1999). Apart from thermophilic fungi, thermophilic
bacteria such as Geobacillus sp. strain T1 (Leow et al., 2004; Rahman
et al., 2007) and Bacillus sp. strain 42 (Eltaweel et al., 2005), which
were isolated from POME, were found to be lipase producers too.
The concentrated bioresources from POME or its retentate (Wu
et al., 2006b, 2007) could be reused as effective substrates to produce
protease (Wu et al., 2006a,b). According to Wu et al. (2006a), a wildtype strain of A. terreus IMI 282743 produced a maximum protease
activity in the medium containing 75% (v/v) POME retentate as the
sole carbon and nitrogen source without addition of extra nutrients or
adjustment of the initial pH. However, using pure retentate, i.e.
without slightly diluting it, was not recommended since it was
presumed that an increase in the retentate concentration would bring
about a decrease in the free water level in the medium and
consequently reduce the solubility and availability of nutrients to
the culture (Wu et al., 2006a).
3.1.7. Hydrogen
According to Morimoto et al. (2004), it was possible to use natural
anaerobic microora from POME sludge, instead of pure culture of
isolated strain, to produce signicant amounts of hydrogen under
anaerobic fermentation in a batch culture. The anaerobic microora in
the POME sludge was found to produce hydrogen whereas no
methane gas was observed in the evolved gas (Morimoto et al.,
2004; Atif et al., 2005). Thus, anaerobic microora found in the POME
sludge might be useful for the production of hydrogen from POME
biomass resources without sterilization. Vijayaraghavan and Ahmad
(2006) tested a new source of microora from cow dung for its
hydrogen-generating capability in POME. They pointed out that the
highest biogas generation and hydrogen content occurred at pH 5. OThong et al. (2007) highlighted that a raw POME supplemented with
nutrients (N, P and Fe) gave a 20% increase in hydrogen production
yields as well as 5861% higher hydrogen contents as compared to raw
POME. The hydrogen production rate could be increased by 60% if raw
POME was adjusted to an optimized iron concentration of 257 mg/l, a
C/N ratio of 74 and a C/P ratio of 559 (O-Thong et al., 2008a). The
nutrient supplementation strategy was found to increase the bacterial

48

T.Y. Wu et al. / Biotechnology Advances 27 (2009) 4052

diversity in the anaerobic sequencing batch reactor and promote the


growth of hydrogen-producing bacteria, namely Thermoanaerobacterium thermosaccharolyticum (O-Thong et al., 2007). Later, O-Thong
et al. (2008b) were able to isolate T. thermosaccharolyticum PSU-2
from a sequencing batch reactor, which was used to digest POME for
continuous hydrogen production. They found that the isolated strain
of PSU-2 produced higher amounts of hydrogen, up to 68%, in organic
nitrogen amended medium as compared to inorganic nitrogen
amended medium.

Table 4
The application of POME (m3/acre/year) as fertilizer for palm oil plantations (Onyia
et al., 2001)

3.2. Sustainable reuse of POME as fertilizer

of aluminum in the soil would eventually help prevent toxicity and


growth hindrance for plants in acid soils (Matsumoto, 2000; Guo et al.,
2007). Nevertheless, variations in POME quality among the mills and
the rate of application as well as other details need to be determined
in relation to local situations (Agamuthu et al., 1992). Moreover, the
use of POME as fertilizer must be carried out with caution because of
imbalances in the nutrient composition. A prolonged improper
utilization may cause an accumulation of magnesium and thereby
inhibit the availability of potassium (Onyia et al., 2001). Table 4 shows
the nutrient requirements for the various growth stages of plants as
well as the suitable amount of POME for reuse as fertilizer in order to
avoid soil damage.
According to Chan et al. (1980), the use of POME has been shown to
improve soil productivity and increase the yield of crops as well as
contribute to better root health by improving the soil structure. An
increase in crop yield on the order of 10 to 24% has been reported (Tam
et al., 1982; Lim et al., 1984). Teoh and Chew (1983) have further
shown that mixtures of soil and POME in a ratio of 1:5 resulted in
more vigorous growth of cocoa seedlings and decreased nursery
rotation without the addition of supplementary fertilizers. With the
help of organic matter consisting of peat and the sludge from POME,
Shamshuddin et al. (2004) conrmed that aluminum toxicity towards
the growth of cocoa seedlings on acid sulfate soil could be reduced to a
certain extent. Agamuthu (1994) stated that the application of POME
alone as fertilizer provided the highest yield of Napier grass
(Pennisetum purpureum), up to 3276 kg/ha, as a result of POME
containing almost all the major and minor elements required for its
growth (Agamuthu et al., 1992). Although the application of fresh
dung also gave rise to high yields of Napier grass, up to 2574 kg/ha,
POME was preferred since fresh dung releases an unwanted odor that
might attract ies (Agamuthu, 1994).
Shamshuddin et al. (1998) indicated that the application of POME
together with ground magnesian limestone, which might last for
3 years, was a sound agronomic option to alleviate the soil acidity and
improve the fertility in Ultisol for maize production. They also
revealed that a POME application up to 40 t/ha did not signicantly
change the topsoil pH and exchangeable calcium, magnesium and
aluminum, in which case the calcium and magnesium from the POME
were held by the negative charge present on the exchange complex.
Saltes et al. (2004) conducted a trial on a composting platform in
windrows comprised of shredded empty fruit bunches that were
watered weekly with POME. They found that the resulting compost
had a good agronomic value but that the mineral balance was
considerably affected due to the nutrients provided by POME being
poorly retained by the substrate and partially lost in percolation
following the weekly watering operations.
According to Saltes et al. (2004), a better distribution of POME
applications together with a system for recovering the leaching might
substantially reduce the nutrient losses while maintaining a suitable
humidity for microbial degradation. In a similar case to that of Saltes
et al. (2004), Aisueni and Omoti (2002) also used shredded empty fruit
bunches together with POME in the composting process but with the
addition of poultry droppings as nutrient supplements. They noted
that the use of POME in the composting process was particularly
benecial in signicantly reducing the amount of poultry droppings,
which were required to produce the same amount of nal compost.

The application of raw or digested POME as fertilizer on land was


initially thought to be impractical because of the efuent killing
vegetation and leading to the blocking of percolation and waterlogging, thus resulting in anaerobic conditions. However, Wood et al.
(1979) found that although raw POME would readily cause clogging
and waterlogging of the soil, these problems could be overcome by the
controlled application of small quantities of POME at a time. The
testing of ground waters after 6 to 12 months of trial applications of
raw POME as fertilizer showed no substantial percolation of oxygendemanding or other polluting elements without excessive run-off over
the surface during wet weather (Wood et al., 1979). It was thus
established that the water quality in the applied areas was unaffected
(Dolmat et al., 1987). Oviasogie and Aghimien (2003) later reconrmed that a proper use and safe disposal of POME in the land
environment would lead to improved soil fertility and contribute to
environmental sustainability. Their results showed an enrichment of
the soils with regard to phosphorus, nitrogen, calcium, magnesium,
sodium and potassium following the application of the POME. Copper,
iron and lead were predominant in their organic forms, while zinc was
particularly present in its exchangeable form.
The potential for using POME as a cheap organic fertilizer may offer
an alternative to the excessive application of chemical fertilizers,
especially phosphorus, for which cost is a severe economic constraint.
For example, biologically treated POME has been widely used in the oil
palm plantations for irrigation purposes and can be employed as a
liquid fertilizer. It is estimated that each 15 million tonnes of POME
would have a fertilizer value of RM 95.41 million (Table 3). According
to Wood et al. (1979), an application of POME at 4.5 106 l per applied
hectare was estimated to represent a fertilizer application of about
30 kg ammonium sulfate, 7 kg rock phosphate, 52 kg potash and 18 kg
kieserite per palm per year. The nutrient composition of the fertilizers
is shown in Table 3.
An incorporation of POME may help to increase the organic matter
in the soil, which may turn into humus after decomposition and
become an active soil component. Thus, POME application would
result in changes in the chemical properties of the soil. According to
Ferreira and Araujo (2002), average contents of calcium, magnesium,
potassium and phosphorus were found to increase in the soil with an
increase in POME dosage, especially at a depth of 020 cm but an
application of 120 m3/ha of POME to the soil reduced the aluminum
content to zero at a depth of 20 cm after 12 months. Such a reduction

Table 3
Estimated fertilizer values from POME, which is based on 15 million tonnes of POME
Fertilizer

Tonnes
(1000)

December 2002 price


(RM/ton)

Fertilizer value
(RM million)

Ammonium
sulphate
Rock phosphate
Muriate of potash
Kieserite
Total

75.5

580

43.79

19.5
68.6
59.6

545
250
400

10.63
17.15
23.84
95.41

Crops

Mg

Young palms
Adults palms
Old palms

2570
90128
162

27.532
52.5
52

5.110
1018.5
18

1.210
15
20

T.Y. Wu et al. / Biotechnology Advances 27 (2009) 4052


Table 5
Chemical attributes of humic substances derived from POME (adapted from Siva et al,
2000)
Chemical attribute
Percent yield
Percent loss on ignition
Elemental make-up (%)
C
H
N
O
O:H
C:N
C:H
Functional groups (meq/g)
Quinonoid (C=O)
Carboxylic (COOH)
Phenolic (OH)
Total acidity (carboxylic + phenolic)
Optical density (E4:E6 ratio)

Humic acid
Claried POME

Decomposed POME

3.47
97.5

1.82
99.5

57.87
8.26
2.91
30.96
3.75
19.89
7.01

48.94
5.76
8.05
37.25
6.47
6.08
8.50

2.52
2.22
3.34
5.56
4.22

2.85
2.08
3.27
5.35
6.09

The slow release of the total N and P after the rst 12 weeks could
also become a limiting factor if these nutrients were to be made
available for plant growth (Palaniappan et al., 1983). Therefore, Azizah
Chulan (1991) suggested that if POME were to be reused as fertilizer,
the soil should be inoculated with vesiculararbuscular mycorrhizal
(VAM) fungus Scutellospora calospora because the combination
between POME and VAM will form mycorrhizae that may enhance
the breakdown of certain soluble phosphates and insoluble organic
phosphate such as phytate by roots (Gianinazzi-Pearson, 1985). Onyia
et al. (2001) stated that the application of organic nitrogen from raw
POME has been associated with lower yields due to ammonia being
liberated during the mineralization of organic matter. Onyia et al.
(2001) therefore suggested that nitrication of POME was necessary
since a nitried POME would be more easily absorbed by most plants
than a raw POME with a high organics content, especially in the
tropics where nitrate leaching does not present a major problem.
Numerous studies have identied ammonia volatilization as the
major cause of low N efciencies in urea (Mikkelsen et al., 1978; Fillery
et al., 1984), in which case up to 80% of the applied urea-N may be lost
within 23 weeks of application (Hargrove and Kissel, 1979; Torello
et al., 1983). Siva et al. (2000) reported that POME is rich in organic
matter and varying amounts of humic substances across their
respective organic matrices (Table 5). Seeing as humic substances
have been reported to interact with ammonia compounds (Banerjee
and Basak, 1978; Thorn and Mikita, 1992) and urea (Patti et al., 1992),
Siva et al. (1999, 2000) investigated the effects of POME-derived
humic substances on ammonia volatilization from urea. Initial studies
by Aminuddin (1994) showed that POME could introduce a preferred
environment within the ureasoil reaction zone (microsite) and
successfully reduce ammonia volatilization to 8% of the applied N. Siva
et al. (1999) displayed that this reduction in ammonia volatilization
was accompanied by a corresponding increase in ammonium recovery
and a decrease in pH, particularly at the microsite. The performance of
humic fractions from POME also indicated an interplay of several
mechanisms that could possibly include urease inhibition, urea
absorption and ammonia xation (Siva et al., 2000). These results
have implications to the reduction of N loss by ammonia volatilization
from urea applied to the soil during crop production.
According to Muhrizal et al (2006), the incorporation of organic
material into iron-poor acid sulfate soil might enhance the benecial
effects of reducible Fe(III) oxides or S in the soil and eventually promote
an increase in pH under ooded conditions. However, not all organic
materials are able to alleviate acid sulfate soil infertility with equal
efcacy (Muhrizal et al., 2003). Although POME contains considerable
amounts of organic materials, Muhrizal et al. (2006) revealed that

49

POME did not signicantly affect the pH and redox potential in the
iron-poor acid sulfate soil during submergence. They also claimed that
POME contains high concentrations of lignin that presumably decomposes slowly under anaerobic condition. Thus, these materials could
not become active electron donors in the reduction process.
3.3. Sustainable reuse of POME as live food for animals and aquacultural
organisms
The reuse of POME as a dietary substitute for pigs, poultry and small
ruminants as well as aquacultural organisms is gaining importance.
Apart from oil palm fronds, palm press ber and palm kernel cake,
Devendra (2004) pointed out that POME was especially important for
feeding ruminants. Using POME as animal feeds, however, could only
be considered as a co-management of the efuent because, according
to Agamuthu (1995), a 40-ton-per-hour mill would require around
44,000 pigs or 43,000 cattle for the entire efuent to be utilized.
Hutagalung et al. (1977) investigated the use of POME as animal
feed for growingnishing pigs, in which case two types of meals
known as censor tk8 (35% palm oil sludge, 32.5% cassava root meal,
32.5% palm kernel cake) and tkg (32% palm oil sludge, 34% cassava root
meal, 17% palm kernel cake, 17% grass meal) were used. They found
that it was economical to replace 50% maize (the regular diet
constituent) with a POME-based animal feed, thus saving up to RM
0.02 per pig per day. In Colombia, POME has been fed with good
results directly to pig (1012 l/head/day) together with palm oil and
other ingredients (Devendra, 2004).
POME could also be used as supplementary food in poultry farming.
According to Ho (1976), animal feed production from palm oil wastes
can replace at least half of the amount of imported maize for poultry
diets and up to 100% for pig diets. Yeong et al. (1980) investigated the
nutritive values of a POME product known as Prolima (Table 6) as the
protein source in broiler chicken diets. It was observed that the amino
acid content of palm kernel cake and palm oil sludge were somewhat
close to cereal by-products and that of Prolima was between soybean
meal and peanut meal, in which case the overall percentage of amino
acid availability for palm kernel cake, palm oil sludge and Prolima
were 74.4%, 24.8% and 71.0%, respectively. Therefore, the concentrations of Prolima up to 30% could be included in broiler diets as a
replacement for soybean meal without causing any adverse effect on
the growth performance of the chickens (Yeong et al., 1980). Later,
Yeong and Azizah (1987) reported the optimum levels of using 1015%
of dried POME in chicken feed for the growth and egg production.
Pasha (2007) also reported that the optimum levels of POME in the diet
for broilers and layers are 15% and 10%, respectively.
The Malaysian Agricultural Research Development (MARDI) proved
that wastes from the palm oil industry (such as oil palm sludge and palm
press ber) alone or in combination, dried to moisture contents of 7%,

Table 6
The chemical composition of Prolima as compared to palm oil sludge (Agamuthu,
1995)
Composition

Prolima

Palm oil sludge

Moisture, %
Crude protein (N 6.25), %
Crude ber, %
Ether extract, %
Ash, %
Nitrogen-free extract, %
Calcium, %
Phosphorus, %
Magnesium, %
Iron, mg/l
Copper, mg/l
Manganese, mg/l
Zinc, mg/l
Gross energy, MJ/kg

5.1
43.3
7.6
12.0
4.1
27.9
0.19
0.52
0.17
365
42
56
145
18.5

6.9
12.4
15.2
24.1
11.2
46.7
0.28
0.18
0.25
1757
36
62
1075
19.6

50

T.Y. Wu et al. / Biotechnology Advances 27 (2009) 4052

could be used as supplementary food for sheep (Devendra and


Muthurajah, 1976). Vadiveloo (1988) fed Katjang and Katjang German
Fawn crossbred goats with Napier grass and Leucaena leucocephala,
which were supplemented with dried POME. He found that supplementing with POME at all levels did not signicantly depress forage
intake but rather increased the total intake. Vadiveloo (1989b) further
conrmed that L. leucocephala, which was supplemented with dehydrated POME, allowed mature regrowths of the crop (increased with
regard to both dry matter and neutral detergent ber digestibility) to be
fed to goats. Agamuthu et al. (1996) also found that goats and sheep
digested POME-treated Napier grass signicantly faster than Napier
grass alone. Feeding studies with goats have also shown that rice straw,
which was properly supplemented with dehydrated POME, could
promote satisfactory performance levels (Phang and Vadiveloo, 1991).
According to Vadiveloo (1989a), NaOH treatment of rice straw together
with dehydrated POME and Leucaena promoted an even higher straw
intake among the goats. The increased intake and dry matter
digestibility with the NaOH treatment might be due to an enhanced
edibility and digestible energy of the roughage (Kellaway and Leibholz,
1983). It was concluded by Vadiveloo (1989a) that diets comprising 25%
NaOH-treated straw, 50% dehydrated POME and 25% Leucaena
permitted dietary nutrients to be reused efciently and maximized
the inclusion of agro by-products. According to Devendra (2004), 10% of
POME in diets for sheep gave the best result in terms of digestibility
because crude ber digestibility dropped signicantly from 80.6% in a
10% POME diet to 27.0% in a 60% POME diet. Ether extract digestibility
decreased progressively with increasing dietary POME.
It should be stressed that the utilization of POME as animal feeds
could be enhanced further by addition of molasses and palm press
ber or other oil palm by-products. According to Devendra (2004), the
maximum suitable level of inclusion of molasses appeared to be one
part molasses for every 1.2 parts of palm press ber + POME. It was
found that combining palm kernel cake and oil palm fronds with
POME could create a low-cost and excellent feeding system. According
to Pasha (2007), 50% palm kernel cake, 30% oil palm fronds and 20%
POME can produce a reasonably good diet for moderate growth rate
and acceptable meat quality in beef cattle.
Two agricultural waste products, namely YM20 (a mixture of pea
and corn) and POME, were evaluated in a closed recirculation system
for their suitability to replace a costly diet of live algae in the culture of
the Sudanese fairy shrimp, Streptocephalus proboscideus (Jawahar Ali
and Brendonck, 1995). They found that the results in terms of growth
(increase in length), cyst production and mortality were more
successful when S. proboscideus were supplied with high densities of
YM20 as compared to POME and algae. Habib et al. (1997) pointed out
that POME could also be reused as a food source by aquatic organisms
such as chironomid larvae known as bloodworms. They reported that
the production of chironomid larvae was signicantly higher in POME
(580 g/20 l POME) than in algal cultures (35 g/20 l algal culture). These
chironomid larvae, in turn, present valuable live food for sh or
cultured invertebrates (Shaw and Mark, 1980; Yusoff et al., 1996). Babu
et al. (2001) studied the use of POME for the culturing of four species of
sh, i.e. silver carp, catla, rohu and mrigal. The sh were harvested after
9 months and the maximum individual growths of silver carp, rohu
and mrigal were 700, 550 and 600 g, respectively whereas the average
growth of catla was 35.3 g. Vairappan and Yen (in press) showed that
Isochrysis sp., which was grown in a modied medium of aerobically
digested POME, was suitable to be reused as a supplement to further
enrich and improve the rotifer cultures. These rotifer cultures, in turn,
play their role as food organisms for sh larvae (Lubzens et al., 2001).
4. Conclusions
On the whole, it is an undeniable fact that POME has its own potential
for sustainable reuse through biotechnological advances. Moreover, it is
understood that a cleaner production is, in the long run, a better option

for managing POME as opposed to end-of-pipe processes. However,


although the emphasis on a cleaner production for POME management is
well-intentioned, it may sometimes raise false expectations. The limits
imposed by the economic and social frameworks present obvious
limitations to sustainable practices that could be applied in the industries
(Fricker, 2003), especially in most developing countries such as Malaysia.
Consequently, there is usually no economic incentive to develop wastefree processes. A cleaner production is therefore limited unless it is
subsidized, externalities are factored in, products are successfully
designed for commercial reuse and, most importantly, the government
takes the initiative in legislating for a sustainable industrial development.
Since the economic framework depends on growth, production and
consumption, the initiatives to promote a cleaner production for POME
management can only come from the palm oil industries themselves
since their subtle actions could accelerate the research and development
for an enhanced POME management. In short, we need to become
responsible citizens rather than mere consumers.
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