Renewable and Sustainable Energy Reviews 79 (2017) 308–322

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Renewable and Sustainable Energy Reviews

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

Anaerobic co-digestion of animal manures and lignocellulosic residues as a MARK

potent approach for sustainable biogas production
⁎
Soheil A. Neshata, Maedeh Mohammadia, Ghasem D. Najafpoura, , Pooya Lahijanib,c
a
Biotechnology Research Laboratory, Faculty of Chemical Engineering, Babol Noshirvani University of Technology, Babol, Iran
b
Faculty of New Technologies and Energy Engineering, Shahid Beheshti University, Zirab Campus, Mazandaran, Iran
c
Biomass and Bioenergy Laboratory, School of Mechanical Engineering, Universiti Sains Malaysia, 14300 Nibong Tebal, Pulau Pinang, Malaysia

A R T I C L E I N F O A BS T RAC T

Keywords: Anaerobic digestion is a versatile biotechnology for conversion of organic wastes to valuable biogas. Anaerobic
Anaerobic co-digestion digestion of manure is making the most of it, as the process allows simultaneous bio-energy generation,
Biogas production of nutrient rich soil amendment, reduced emission of greenhouse gases and odor control; it is thus
Lignocellulosic residue in line with climate friendly farming practices. Despite the enumerated advantages, the potential of manure for
Manure
biogas production is not fully utilized due to the low and imbalance carbon to nitrogen (C/N) ratio in animal
manures. To satisfy the anaerobic digestion requirements and to compensate the carbon deficiency of manure,
there should be another carbon-rich substrate to be co-digested with manure to improve its characteristics for
anaerobic digestion; lignocellulosic biomass residues seem promising for this purpose. This work presents a
review on anaerobic co-digestion of animal manure and lignocellulosic feedstock for biogas production. Several
research studies conducted on co-digestion of these organic wastes are described and reviewed. The impact of
numerous parameters including temperature, pH, organic loading rate (OLR), hydraulic retention time (HRT),
C/N ratio, alkalinity and concentration of volatile fatty acids (VFAs) on the performance and stability of the co-
digestion process is extensively discussed. The influence of various pretreatment methods including physical,
chemical and biological pretreatments on providing well-prepared substrate for anaerobic co-digestion and thus
enhancement of biogas production is discussed. An overview of the most significant factors and intermediates
which can inhibit or even cease the process is also presented.

1. Introduction contains beneficial microorganisms which can enhance soil structure

The environmental implications of animal manure disposal have
motivated authorities to seek for strategies which could lead to
“sustainable animal farming”. Towards this transition, solutions that
could help to transform manure into value-added marketable products
sound green and caring. As a biodegradable product, manure should
not be disposed of in landfills as it contains significant levels of
nutrients and pathogens. Any improper management of this valuable
waste can contaminate soil, air and water and also cause harmful
microbial build-up in the environment. Among the best manure
management practices which also contribute to sustainability is
anaerobic digestion through which, simultaneous waste treatment
and bio-energy production could be achieved.
Traditionally, manure has been used as a valuable fertilizer for
virtually all farming operations to provide required nutrient for crop
growth. An ordinary cow manure is likely to contain roughly10 lb
nitrogen, 5 lb phosphate and 10 lb potash per ton [1]. Manure also
and biological activity. Nevertheless, over the past 50 years, use of
manure on many farms has gradually declined due to several reasons
including: i) specialized farms use with increasing separation of
breeding and cultivation (livestock and crop production), ii) cost
considerations of manure transportation and (iii) increased availability
of synthetic fertilizer with desirable compositions and concentrations at
cheaper prices. Today, mass-production of animals in factory farms to
provide food requirements generates staggering amount of manure;
almost 130 times that of human waste produced in the United States
[2]. Understanding how to manage the huge amount of manure daily
produced is challenging and of course a wiser utilization of the manure
on the farm is in demand. The same nutrients that make manure a
valuable commodity also make it a threat to the environment.
Inappropriate handling of manure may lead to destructive run-off,
containing bacteria and nutrients which contaminate local ground
water and threaten public health. Significant nutrient loss during
collection, storage, distribution and utilization of manure is almost

⁎
Corresponding author.
E-mail addresses: najafpour@nit.ac.ir, najafpour8@gmail.com (G.D. Najafpour).

http://dx.doi.org/10.1016/j.rser.2017.05.137
Received 4 July 2016; Received in revised form 15 May 2017; Accepted 19 May 2017
Available online 22 May 2017
1364-0321/ © 2017 Elsevier Ltd. All rights reserved.
S.A. Neshat et al.
inevitable. Manure storage in open air, particularly in humid tropics
with high rain fall, can conclude to 70% nitrogen loss within 24 h which
happens through ammonia (NH3) volatilization and nitrate (NO−3 )
leaching [3]. Leaching of P (P2O5) and K (K2O) also occurs when rain
fall is high. In some countries, manure is first treated in lagoons and
then directly discharged into the surface water; this implies almost
complete loss of organic matter and nutrients from the manure. When
manure is directly discharged into the surface water, decomposition of
easily degradable fractions starts immediately which consume all
dissolved oxygen and creates an anaerobiosis condition in water. The
heavy load of nutrients in the manure will deteriorate the condition by
contributing to water eutrophication and heavy metal toxicity [4]; this
will eventually conclude to the death of water fauna and flora and
reduce the aquatic life of a river to zero. Moreover, the methane and
carbon dioxide produced by anaerobic self-remediation of manure can
largely contribute to the global warming. In manure management
plants, the challenge is thus to find ways to maximize the benefits of
manure while protecting water resources and environment. Anaerobic
digestion of manure has attracted considerable attention in this regard;
it has the potential of tolerating high organic load and biogas
production.
Even though anaerobic digestion can serve as an alternative to
manure disposal in landfill sites, however, the low carbon to nitrogen
(C/N) ratio in animal manures cannot fully satisfy the anaerobic
digestion requirements. Hence to conduct an effective anaerobic
digestion, there should be another carbon-rich substrate to be co-
digested with manure to compensate its carbon deficiency and improve
its characteristics for anaerobic digestion. Anaerobic digestion for
production of biogas is not a novel process; for many years the process
was conducted in Asia; historians claim that the biogas production was
performed in Assyria and Persia years before Christ [5]. It is interesting
to note that in old days even anaerobic co-digestion was conducted
without any knowledge about the effect of addition of carbon-rich
substrates to anaerobic digesters by discharging fruit wastes to
digesters. The characteristics of co-substrate utilized for co-digestion
is important; wastes with high carbon and low nitrogen contents are
favored. Among different feedstocks potent to be used as co-substrate
in anaerobic digestion, lignocellulosic residues seem promising as they
are rich in carbon and abundantly available at low cost. The intricate
composition of lignocellulosic materials, where cellulose fiber is tightly
linked to hemicellulose and lignin, hinders their biodegradability and
thus restricts their use as the sole substrate for anaerobic digestion [6];
however, through co-digestion with manure, they can be converted to
valuable products and contribute to waste to energy plants. A scheme
of anaerobic co-digestion plant in which manure and lignocellulosic
wastes are co-digested to provide energy and fuel is illustrated in Fig. 1.
As any process, anaerobic digestion has its own advantages and
drawbacks. Long retention time for digestion and low heating value of
the produced gas are considered as the main disadvantages associated
with this process. Most studies on anaerobic co-digestion are con-
cerned with enhancement of biogas production while increasing
methane content and shortening the retention time to increase the
treatment capacity of the unit. Nevertheless, for today's demand the old
anaerobic digestion systems with low efficiency are not efficient any-
more. Recent researches have shown that combination of modern
reactors and optimized digestion conditions can reduce the hydraulic
retention time (HRT) and enhance methane and biogas production
yields.
This paper provides a review on co-digestion of animal manures
and lignocellulosic biomass residues for biogas production as an
evolving field of sustainability. It is obvious that the anaerobic
digestion of manure reduces the emission of CH4 from manure,
however, the amount of carbon being mineralized to biogas and utilized
in the plants, instead of being released into the atmosphere depends on
the reaction condition. Here, an outline of the most effective para-
meters on the performance and stability of anaerobic co-digestion
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Renewable and Sustainable Energy Reviews 79 (2017) 308–322
process which include temperature, pH, OLR, HRT, C/N ratio,
alkalinity and concentrations of VFA is presented and different findings
and conclusions from the literature are reviewed. Moreover, different
methods used for the pretreatment of substrates to enhance their
digestibility are discussed. An overview of the most influential inhibi-
tors which can disturb the anaerobic digestion or even cease the
process is presented and at the end the strategies used for upgrading
the produced biogas are reviewed.
2. Anaerobic digestion
Basically, anaerobic digestion is characterized by reaction wherein,
biogas is produced from biodegradable materials under anaerobic
condition. Composition of the produced biogas depends on the utilized
substrate and digestion conditions. Biogas is mostly comprised of
methane and carbon dioxide, with minor amounts of other gases
including nitrogen, hydrogen, hydrogen sulfide, ammonia and water
vapor. The evolution of biogas occurs through the activity of various
microorganisms in three steps; namely, hydrolysis, acidogenesis (also
called fermentation) and methanogenesis [7,8]. Although some refer-
ences describe the progression of anaerobic digestion within four steps
including hydrolysis, acidogenesis, acetogenesis and methnogenesis
[9]. A microbial consortium comprising of different species of hydro-
lytic organisms, acidogens and methanogens are known to be respon-
sible for biogas production. Fig. 2 depicts a scheme of the steps
involved in anaerobic digestion.
In the hydrolysis step, complex materials such as lipids, polysac-
charides, proteins and nucleic acids are converted to soluble com-
pounds including fatty acids, monosaccharides, amino acids, purines
and pyrimidines. In the next step (fermentation), acetate, hydrogen,
carbon dioxide, formate, methanol, methylamines, propionate, buty-
rate, etc. are produced by acidogenesis. At the final stage, methane is
produced by two groups of methanogens; i.e., acetoclastic (acetate
consumer) and hydrogen-utilizing methanogens (H2/CO2 consumer).
Acetoclastic methanogens split acetate into methane and carbon
dioxide, while hydrogen-utilizing methanogens are responsible for
methane production using CO2 and hydrogen as electron acceptor
and donor, respectively. Synthesis of methane from different precur-
sors is summarized in Reactions (1)–(6) [7,10]:
4H2+ CO2 → CH4 + 2H2O (1)
4HCOO- + 4H+ → CH4 + 3CO2 + 2H2O (2)
4CO + 2H2O → CH4 + 3CO2 (3)
4CH3OH → 3CH4 + CO2 + 2H2O (4)
4(CH3)3N + 6H2O → 9CH4 + 3CO2 + 4NH3 (5)
CH3COOH → CH4 + CO2 (6)
The organisms responsible for the hydrolysis and acidogenesis are
facultative and obligate anaerobic bacteria. Isolation of several bacter-
ial genera including Clostridium, Peptococcus, Bifidobacterium,
Desulphovibrio, Corynebacterium, Lactobacillus, Actinomyces,
Staphylococcus and Escherichia coli from anaerobic digesters has been
reported [6,7,11]. As mentioned, methane production is conducted by
two groups of methanogens; the community composition of methano-
gens is similar to microbial consortium of ruminant animal's stomach.
Methanobacterium, Methanobacillus, Methanococcus, Methanothrix
and Methanosarcina are the main microorganisms which serve for
methane production in the anaerobic digestion [7,12]. All of the
methanogens are archaea and strict obligate anaerobes which require
redox potentials below −300 mV for growth [13]. They are very
sensitive to oxygen and grow very well in the presence of H2 and
CO2. Methanosarcina and Methanothrix are among the limited
S.A. Neshat et al. Renewable and Sustainable Energy Reviews 79 (2017) 308–322

Fig. 1. A scheme of anaerobic co-digestion of animal manure and lignocellulosic residues for biogas production along with its potential applications.

number of microorganisms which are able to convert acetate into is discharged from the chamber. The produced biogas is collected
methane and carbon dioxide; the others are hydrogen-utilizing metha- under the roof of the digester and burnt as fuel for heating and
nogens [6,7,12]. electricity production. Solid effluent of these digesters, which is rich in
nitrogen (night black soil), is usually used as fertilizer. The effluent has
less intense odor than influent. These types of reactors still have
3. Anaerobic bioreactors
application in third world countries such as India, African countries,
etc.; China is among leading countries in biogas production [20–26].
As prior mentioned, anaerobic digestion is not a newly emerged
Beside Asian countries, European countries and United states are using
treatment process. The first study on anaerobic digestion was con-
developed technology for anaerobic treatment of wastewaters and
ducted by Alessandro Volta who studied the relationship between
production of biogas as fuel [27].
organic loading and gas production in 1776. Later on, in 1804–1808,
Advances in bioprocess engineering and biotechnology have led to
John Dalton and Humphrey Davy found that the combustible gas
design and operation of new digesters with improved yields and high
generated from decomposition of organic materials is methane [14].
efficiencies compared to the traditional batch ones. Use of modern
Anaerobic digestion has long been used as an energy providing method,
reactors for anaerobic digestion has enabled the treatment of variety of
especially in Asian countries such as China and India. Hence, many
wastes with different characteristics. Now, wastewaters and effluents
diverse configurations of digester basins have been designed, developed
with high solid content can be well treated in continuous stirred tank
and operated for biogas production. Among hundreds of traditional
reactors (CSTR), while for waste streams with a high concentration of
reactors, three of them are most efficient which are floating drum, fixed
soluble materials up flow anaerobic sludge blanket (UASB) reactors,
dome and inflatable tubular (plug flow) digester [15–19]. Schematic
fluidized bed reactors and anaerobic filters are preferred [28]. Recent
representation of these digesters is illustrated in Fig. 3.
researches have shown that use of advanced digesters such as UASB
Conventional anaerobic digesters are built on very simple basis.
reactor can increase methane yield and COD removal efficiency of the
They provide an anaerobic reaction chamber wherein influent is
process. Schematic representation of a UASB digester is illustrated in
retained for a defined HRT and upon completion of the digestion it

Fig. 2. Scheme of the steps involved in anaerobic digestion.

310
S.A. Neshat et al.
Fig. 3. Conventional digesters for biogas production: (a) floating drum digester, (b) fixed dome digester and (c) inflatable tubular digester.
Fig. 4. Schematic representation of (a) UASB and (b) UAFF digesters.
Fig. 4. Rico et al. [29] used a single stage UASB for co-digestion of
cheese whey and liquid fraction of dairy manure and achieved COD
removal efficiency of 95% in their experiments. Zhang et al. [30]
performed anaerobic digestion of sewage and glucose as co-substrate in
a UASB reactor and reported that around 75% of maximum potential
methane production was attained. Use of hybrid bioreactors has gained
interest among researchers in recent years. These hybrid configurations
are combinations of different bioreactors such as UASB and up flow
anaerobic packed bed (UAPB) which is also referred as up flow
anaerobic fixed film (UAFF). Such hybrid bioreactor combines the
advantages of both bioreactors and can work with higher efficiency
compared to UASB or UAPB. In this regard, Tehrani et al. [31]
operated an up flow anaerobic sludge fixed film (UASFF) bioreactor
which was a combination of UASB and UAFF bioreactors in continuous
mode and treated 2.4 L of dairy wastewater (cheese whey) per day; they
reported a COD removal efficiency of 80%. Najafpour et al. [32] used a
UASFF bioreactor for digestion of palm oil mill effluent. They achieved
a COD removal efficiency of 97% and methane production yield of
0.346 L/gCOD removal at HRT of 3 days. It is worth to mention that
although continuous anaerobic digestion operations show a stable
performance, the methane production yield might not be as high as
that of batch operation. Risberg et al. [33] used a 5 L laboratory scale
CSTR as digester for anaerobic treatment of wheat straw and cattle
manure. When similar experiments were carried out in batch bior-
eactor, the methane production was much higher. It was reported that
in continuous operation the degradation efficiency, calculated based on
reduction in volatile solids in relation to total solids, was lower than
batch tests.
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Renewable and Sustainable Energy Reviews 79 (2017) 308–322
4. Co-digestion
The high nitrogen content of animal manures opposes an obstacle
to provide optimum C/N ratio required for anaerobic digestion [34]. To
address this issue, the carbon content of animal manure needs to be
increased before proceeding to the anaerobic digestion. Lignocellulosic
materials including agricultural wastes are potential candidates to
compensate the carbon deficiency of animal manure, as they contain
high carbon content but can hardly be used as the sole substrate for
anaerobic digestion. The anaerobic digestion of lignocellulosic materi-
als is restricted by their slow degradation and consequently low
methane yield. The digestibility rate of lignocellulosic feedstock is
governed by slow hydrolysis of cellulose which is suggested to be the
rate-controlling step of the process [6]. Although biogas production
potential from lignocellulosic materials can be enhanced through the
exploitation of pretreatments such as steam explosion or enzymatic
hydrolysis, however, the economic feasibility of the process might be
disturbed. Co-digestion of lignocellulosic materials and animal man-
ures offers a solution to balance the C/N ratio of feedstock for
anaerobic digestion. The process allows the conversion of organic
waste materials to bio-energy in the form of biogas, while leaving
behind a nutrient rich residue which can be used as fertilizer.
Increasing the buffering capacity, dilution of potential toxic com-
pounds, utilizing the nutrients, bacterial diversity and lowering the
risk of ammonia inhibition are some benefits which come along co-
digestion of lignocellulosic materials and animal manures [35–37].
Moreover, the high water content of animal manures dilutes the
concentrated organic compounds existing in lignocellulosic wastes
which may oppose inhibitory effect on the process. Some anaerobic
digestion processes wherein lignocellulosic residues or other carbon
rich streams were utilized as co-substrate with animal manures are
discussed here.
Wheat straw, as the second abundant agricultural waste in the
world [33], is an interesting material for biogas production. High
lignocellulose content of wheat straw causes slow biodegradability and
low efficiency of anaerobic digestion which eventually results in low
methane production rate. The C/N ratio of wheat straw is about 100
which is too high for anaerobic digestion. The low level of trace
elements in wheat straw is also a limiting factor for anaerobic digestion
[38,39]. In a study conducted by Wang et al. [38] co-digestion of cattle
and chicken manures and wheat straw was investigated. They reported
that the co-digestion enhanced the performance of the process. They
believed that synergic effect of these materials was responsible for
improvement of anaerobic digestion. Han et al. [40] and Wang et al.
[38] reported that addition of 4.6 kg wheat straw per ton of cattle
manure improved the biogas yield by 10%. However, a different result
was reported by Risberg et al. [33] who compared the digestion of
cattle manure and wheat straw. They obtained same yield for both
substrates, 0.15 N L CH4/g VS (volatile solid) for wheat straw and
S.A. Neshat et al.
0.17 N L CH4/g VS for manure, and reported that co-digestion of
manure and wheat straw did not improve the methane production
yield. Li et al. [41] also reported that methane production yield in co-
digestion of cow manure and rice straw was slightly higher than that of
mono-digestion of cow manure.
The byproduct of oil extraction process from palm fruit is called
palm pressed fiber. Palm pressed fiber is commonly burnt as fuel to run
electricity generators in palm farms. Combustion of this byproduct is a
source of air pollution in Southeast Asia [42]; whereas, palm pressed
fiber can be co-digested, due to its high carbon content [43,44], to
produce biogas. Bah et al. [45] conducted a study on co-digestion of
palm pressed fiber with cattle manure and found that co-digestion
shortened the lag phase of the system and improved the COD removal
at lower HRTs. They also reported an improvement in hydrolysis of
substrates which resulted in higher accessibility of microorganisms to
substrates.
Whole stillage is the residue of ethanol fermentation whose main
application is for animal feeding. Whole stillage has high protein
content which turns it into a suitable material for biogas production.
Nevertheless, the high protein content of whole stillage can lead to
ammonia inhibition in anaerobic digestion. There is also another
disadvantage associated with the use of sulfuric acid in ethanol
fermentation plants. A common pretreatment in ethanol production
industry is use of sulfuric acid for degradation of complex compounds
and pH control. Addition of sulfuric acid to whole stillage can activate
sulfate reducing bacteria which compete with methanogenic bacteria
for substrate. Activation of sulfate reducing bacteria results in lower
level of methane and higher level of hydrogen sulfide production.
Westerholm et al. [46] digested whole stillage as the sole substrate in
an anaerobic CSTR digester. They observed some signs of instability
(after 120 days) in the system. To solve this issue, they added cattle
manure to the system and compared the results to those obtained from
co-digestion of whole stillage and cattle manure. According to their
report, the highest methane production for whole stillage digestion and
whole stillage co-digested with cattle manure was 0.51 and 0.31 N L
CH4/g VS, respectively. The lower methane production achieved in co-
digestion was reasonable due to low energy content and high fiber
fraction of cattle manure. Although co-digestion process resulted in
lower methane yield, the stability of the system increased and the
concentration of VFAs reduced which made it a favorable process. In
fact, the alkalinity of cattle manure helped the system to neutralize the
accumulated fatty acids and improved the system condition signifi-
cantly.
Kitchen wastes include residues of foods from households, restau-
rants, hotels, etc. According to the reports [47,48], 37–55% of
municipal solid wastes are comprised of kitchen wastes and treatment
of these solid wastes is one of major concern for governments. The
carbon content of these materials is high and hence can be used as
appropriate substrates for co-digestion with animal manures. To this
end, Li et al. [47] co-digested kitchen waste with cattle manure in a
laboratory scale batch reactor and found that methane production
increased by 44% as compared to the sole digestion of kitchen waste.
Corn stover which is the leftover after harvest of maize is also a
potential substrate for anaerobic co-digestion with manure. Li et al.
[49] carried out an investigation in this regard; their findings con-
firmed that co-digestion of cattle manure and corn stover enhanced
biogas production (4.9–7.4% increase in methane content) and pro-
vided more stable condition due to synergic effect of co-digestion
compared to digestion of corn stover as the sole substrate.
Cotton stalk contains a lignin content of about 21.6%; it is poorly
degradable in anaerobic digestion. When Cheng and Zhong [50] co-
digested it with swine manure in a laboratory scale batch reactor, they
observed an enhancement of about 1.9 and 1.8 times in biogas
production yield and rate, respectively, as compared to the condition
where cotton stalk was solely digested.
The high rate of harvest of maize has turned maize silage into a
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Renewable and Sustainable Energy Reviews 79 (2017) 308–322
favorable agricultural byproduct in most European countries. Its high
carbon content has made it a suitable substrate for co-digestion.
According to the reports [51], 80% of Germany's biogas production
plants use maize silage as co-substrate. Kalamaras and Kotsopoulos
[52] conducted a set of experiments to compare the methane produc-
tion yield from co-digestion of several crops including silages of maize,
cardoon, milk thistle and sorghum with cattle manure. Results showed
the predominant performance of cardoon silage co-digested with cattle
manure over other biomass residues for methane production.
Salix, also known as willow, has high carbon content and is also
adaptable to extreme soil conditions. It is very productive and can
produce 35000 kg of stem per hectare per year, hence it is sometimes
called energy crop. The high lignocellulose content could be considered
as a disadvantage of this substrate for anaerobic digestion. Proper
pretreatment can turn it to a suitable substrate for co-digestion.
Estevez et al. [53] reported that co-digestion of Salix with cattle
manure increased the methane yield by 18% in comparison to mono-
digestion of cattle manure. However, co-digestion decreased the
methane content of the produced gas by about 6% but higher stability
of the system was the remarkable advantage of the co-digestion
process.
Algae is commonly used for biodiesel production but due to its
attractive specifications such as capacity to grow almost everywhere
with sufficient moisture content, adaptability to tough environmental
conditions and being produced in all seasons, it has become one of the
favorite substrates for co-digestion with animal manure. Astals et al.
[54] undertaken an investigation on co-digestion of algae with pig
manure. They compared the results of co-digestion of pig manure and
pristine algae as well as residues of algae obtained after intracellular
material extraction. They reported that co-digestion of manure and
pristine algae increased methane yield by about 29–37% as compared
to mono-digestion of algae. Nevertheless, no significant increase in
methane yield was observed in co-digestion of cattle manure with algae
residues.
Sugar beet byproduct is the residue remained after extraction of
sugar from sugar beet plant; it mainly consists of pulp and molasses.
High carbon content of this waste turns it into a favorable material for
anaerobic co-digestion with animal manures. Aboudi et al. [55] co-
digested sugar beet byproduct and pig manure in a semi-continuous
stirred tank reactor at mesophilic condition. The highest methane
production yield they reached was 57.5%. In another attempt for
valorization of agricultural waste, Abouelenien et al. [56] studied the
co-digestion of a mixture of agricultural wastes consisting of cassava
waste, coconut waste and coffee grounds with chicken manure and
observed a maximum of 93% enhancement in methane production
yield compared to sole cattle manure digestion.
Switchgrass is an energy grass which has high carbon content and
less need to pest control and fertilization for growth. This non-food
grass can grow on marginal lands and is an excellent substrate for co-
digestion [57,58]. Ethanol production is one of the main applications of
switchgrass but the high lignin content makes it expensive for ethanol
production, as break down of lignin needs expensive pretreatment
processes [59,60]. Lehtomäki et al. [61] reported that addition of
energy crops to cow manure for anaerobic digestion increased the
methane production per digester volume by 16–65%, while the crops
ratio to manure was about 1:3. Increasing the crops to manure ratio up
to 1.4:3 decreased specific methane yield by about 4–12%.
Beside lignocellulosic residues, there are some other organic wastes
such as cheese whey which can be potential substrates for co-digestion
with animal manures. Cheese whey is characterized by high COD
(about 80 g COD/ L), high protein, high lactose concentration, low
alkalinity and very high biodegradability [62,63]. Due to its low
alkalinity, cheese whey is not a suitable substrate for sole anaerobic
digestion. Low alkalinity of cheese whey leads the anaerobic digestion
to acidification which consequently results in failing the whole process
because of producing VFAs and low pH level [64,65]. Co-digestion of
S.A. Neshat et al.
cheese whey with cattle manure was evaluated by Rico et al. [29] in a
UASB reactor. A COD removal efficiency of 95.1% at HRT of 1.3 day
was achieved.
In spite of several reports on improvement of methane production
in co-digestion of lignocellulosic materials and animal manure, there
are some works that obtained lower specific methane yield in co-
digestion process compared to mono-digesting of animal manure
[35,66]. Hashimoto [35] investigated the anaerobic co-digestion of
wheat straw and cattle manure in a laboratory scale batch bioreactor.
They expected to reach to higher methane yields upon increasing the
straw portion in the feed, as the C/N ratio was enhanced. However, the
results showed that the highest methane yield (4 m3/kg VS) was
obtained from digestion of manure and addition of straw as co-
substrate decreased the methane yield by 31%. In another study,
Fischer et al. [66] reported that co-digestion of wheat straw and swine
manure decreased the amount of produced biogas but increased the
digester stability. As a disadvantage of co-digestion, Cheng and Zhong
[50] pointed to lengthy lag phase, where the lag phase of their system
in mono-digestion of cotton stalk was 6 days, while it prolonged to 10
days in co-digestion of swine manure with cotton stalk. Nevertheless,
higher methane yield and other advantages made the extended lag
phase reasonable.
5. Impact of process parameters
Anaerobic digestion is a highly complicated process to produce bio-
energy from organic wastes. This process proceeds through the
interactions of many biotic (microbial community) and abiotic (reactor
parameters) factors yet to be elucidated. To exploit anaerobic digestion
to the full and to achieve the maximum potential of this technology,
much more about the fundamental process parameters should be
learnt. Precise control of some of these parameters is crucial as any
deviation from their optimum levels can even cease the whole process.
Temperature, pH, C/N ratio, OLR, HRT, alkalinity and concentration
of VFAs are among the most important parameters that affect the
performance of an anaerobic digestion system. Furthermore, there are
some materials and conditions that can cause inhibitory effect on the
process. Some studies have been conducted in this regard that are
discussed here. Despite the significance of the mentioned parameters
for stable operation and proper performance of the system, some of
them have been neglected in investigations carried out so far on
anaerobic co-digestion process and very few works have addressed
their effects.
5.1. Temperature
Temperature is one of the most influential parameters which affect
the performance and stability of anaerobic digestion. Anaerobic diges-
tion can take place in all temperature regimes; i.e., mesophilic
condition, thermophilic condition and ambient temperature; very few
studies also reported the investigation of anaerobic digestion under
psychrophilic condition [67]. This process is very sensitive to tempera-
ture and any temperature fluctuation can seriously affect the whole
process. Effect of temperature can appear in metabolic activity of
organisms and other factors such as settling characteristics and gas
transfer rate. Temperature variations can affect hydrolytic bacteria
which are responsible for degradation of complex materials. Also,
acidogenic bacteria cannot tolerate temperature changes and are active
in a specific temperature range; deviation from optimum temperature
can cause acidification due to the accumulation of VFAs. Methanogenic
bacteria cannot also tolerate temperature fluctuations over 1 °C/d [7].
Working at thermophilic conditions ( > 45 °C) can enhance the
performance of anaerobic digestion because of higher solubility of
organic compounds, higher chemical and biochemical reaction rates,
lower solubility of gas in the liquid, lower liquid viscosity, higher
pathogen deactivation and less odor emission [68,69]. On the contrary,
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higher temperatures increase the inhibitory effect of ammonia and VFA
by increasing and decreasing their pka, respectively [70,71]. It was
reported that methane and biogas production yield during anaerobic
digestion of food waste at thermophilic condition was higher than that
of mesophilic condition [72].
Suitable operating performance, stability and less sensitivity to
inhibitors are considered as the advantages of mesophilic operations
(25–40 °C). Sanchez et al. [73] reported that anaerobic digestion
process conducted under mesophilic temperature regime was more
stable than the one operated under ambient temperature. In spite of
pros and cons counted for thermophilic and mesophilic anaerobic
digestions, there is no consensus among researchers regarding the
optimum temperature range for anaerobic digestion. Risberg et al. [33]
reported that change of operation temperature did not affect the
degradation, biogas or methane production yield significantly. The
only difference between thermophilic and mesophilic operations was
degradation of phenolic compounds. Degradation efficiency of phenolic
compounds at mesophilic condition was higher than that of thermo-
philic operation. Westerholm and Hansson [46] performed an inves-
tigation to see the effect of temperature on methane production in co-
digestion of whole stillage and cattle manure in a CSTR reactor which
was operated as anaerobic digester. They found that both mesophilic
and thermophilic temperature regimes showed high potential for
methane production. They could achieve a methane yield of 0.31 N L
CH4/g VS.
Reaction rate dependency of biological processes to temperature
can be expressed as [74,75]:
kT = k20 θ (T −20) (7)
where kT is the reaction rate constant at temperature T, k20 denotes the
reaction rate constant at 20 °C, θ represents the temperature activity
coefficient and T is temperature. Also, Arrhenius equation can explain
the temperature dependency of the reaction:
−Ea
k = Ae RT (8)
where A is the pre-exponential factor, Ea is the activation energy, R
represents the universal gas constant and T is temperature.
Considering the above equations, increase of the temperature corre-
sponds to enhanced degradation rates of organic solids, probably due
to the effective use of resources and enhanced occupation of ecological
niches [76]. However, reports [33,46] show that operation at higher
temperatures did not result in higher methane yields. In fact, higher
temperatures conclude to higher biogas production, but not higher
methane yields. Considering the fact that biogas mainly consists of
methane and CO2, higher biogas production with lower methane
content means increased amount of CO2. Although increase of CO2
can increase the product gas pressure and helps to deliver it easier;
however, higher CO2 content corresponds to lower heating value of the
produced biogas and the need for further purification processes.
Although thermophilic anaerobic digestion was reported to be
superior over mesophilic digestion due to the mentioned advantages,
most of studies on co-digestion of lignocellulosic materials and animal
manures were carried out at mesophilic temperatures due to the higher
robustness of the process [76]. Anaerobic digestion plants aim to
produce biogas for energy applications, thus consumption of energy to
heat up the reactors for thermophilic digestion is not economical.
Working at mesophilic condition needs less energy and can enhance
process stability and pathogen inactivation.
5.2. pH
pH is known as a very important parameter with direct impact on
the performance of anaerobic digestion systems. The pH dependency of
anaerobic digestion relates to enzymatic reactions of the involved
microorganisms in the process. Any enzyme has its own optimum pH
S.A. Neshat et al.
range. According to the literature [26,77,78], the optimum pH for
anaerobic digestion is around 6.8–7.2. Growth of methanogenic
bacteria highly reduces at pH values below 6.8; on the contrary, high
alkalinity leads to granules disintegration which adversely influences
on methane production. Accumulation of short chain fatty acids can
descend the pH below the optimum level and reduce methane
production; however, in co-digestion process the high buffering
capacity of manure can somehow protect the process. Bah et al. [45]
investigated the effect of pH in the range of 6.9–8.9 on the anaerobic
co-digestion of palm pressed fiber and cattle manure to obtain the best
condition for activity of methanogenic microorganisms. They found
that the optimum pH range was 6.8–7 at which, the highest methane
production yield was achieved. In another study undertaken by Cheng
and Zhong [50], the optimum pH for anaerobic digestion of cotton
stalk and cattle manure, either as sole substrate or co-substrate, was
determined as 6.5. They expected lower pH levels in co-digestion
wherein the concentration of VFAs was much higher than mono-
digestion; however, because of the buffering capacity of manure, pH
level did not change significantly. Zhai et al. [48] also studied the effect
of initial pH on the anaerobic co-digestion of kitchen wastes and cow
manure. They found that initial pH can affect pH variation during
anaerobic digestion, VFA concentration, alkalinity and ammonia con-
centration. They emphasized on the significance of initial pH on the
start of digestion and reported pH 7.5 as the optimum pH for their
system.
Acidification of the medium is one of the reasons which concludes
to failure of anaerobic digestion which can take place as a result of
presence and accumulation of VFAs at very initial stages of digestion
(startup period). In processes with high gas phase CO2 concentrations,
the pH is also largely affected by production of carbonic acid. At this
condition, addition of alkali chemicals such as NaOH and CaCO3
solutions can obviate the problem until the system become stable;
nevertheless, some of these chemicals can cause other problems [55].
For instance, addition of NaOH releases Na+ ions in the medium which
can inhibit the anaerobic digestion.
5.3. Organic loading rate
Organic loading rate (OLR) shows the amount of dry organic solids
which is loaded per volume of the system per time. OLR is an
important factor for viability of the microorganisms and their optimum
activity. Loading of high amount of organic materials into the system at
once can lead to a shock which is the consequence of higher activity of
hydrolyzing and acidogenic bacteria compared to methanogens. The
accumulation of VFAs in the medium will eventually conclude to
inactivation of all bacteria due to the low pH. Li et al. [47] carried
out a study on anaerobic digestion of kitchen wastes and also co-
digestion of kitchen wastes and cattle manure. They found that
digestion of kitchen wastes as the sole substrate failed in the 1 L batch
bioreactor at high OLR (20 mg/L) due to acidification of the medium
resulted from the produced VFAs. However, this case was not observed
in the co-digestion process due to the high alkalinity of the manure; the
highest achieved methane yield in co-digestion process was 313.4 mL/
g VS.
For biogas production, 4 kg of dry solids per cubic meter of reactor
per day was reported as the highest rate that microorganisms can
tolerate [73]. Aboudi et al. [55] reported that 12.8 g VS/ L reactor was
critical in co-digestion of sugar beet byproduct and pig manure and
their system was not able to digest the feed and produce methane. In
fact, the stability of their system faded in that OLR. In another set of
experiments conducted by Li [79], different OLRs were loaded to a
semi-continuous digester performing co-digestion of horse manure and
grass. The methane yields of 159.2, 149.6 and 141.1 mL/g VS were
obtained at the OLRs of 1.25, 1.88 and 2.5 g VS/day, respectively; the
optimum OLR was found to be 1.88 g VS/day at HRT of 14 days.
Besides the effect of OLR on the activity of microorganisms, OLR is also
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important for proper performance of pumps which have the duty of
circulating the fluids or feeding the system. High OLR can damage the
pumps due to limitations of pumps for carrying solids [29].
5.4. Hydraulic retention time
Hydraulic retention time (HRT) plays a significant role both in
treatment of waste and wastewater and also production of precious
byproducts by the microorganisms. In any bioprocess, appropriate
HRT should be carefully determined as any microorganism needs its
specific time to consume its favorite substrate and synthesize the
product. If the process could not be maintained at its optimum HRT,
unfavorable metabolic activity of microorganisms and undesirable
products will be resulted. Long HRTs can lead to the death of
microorganisms due to the shortage of nutrients; in contrast, short
HRTs can result in cell intoxication or low methane yield.
Accumulation of VFAs can also be resulted from short HRTs [7].
HRT is defined as:
V
HRT =
Q (9)
where V is the volume of the bioreactor and Q is the flow rate of the
influent.
Salminen and Rintala [80] investigated the effect of HRT on the
anaerobic digestion of solid poultry slaughterhouse wastes. They
studied five different HRTs in a semi-continuous system and observed
lower amounts of VFA and higher pH for longer HRTs; although higher
VS and total solid (TS) removal was achieved at longer HRTs. In their
experiment, the methane production yield increased from 0.09 m3/kg
VS at HRT of 13 days to 0.55 m3/kg VS at HRT of 50 days and then
decreased to 0.52 m3/kg VS as the HRT was prolonged to 100 days.
5.5. Alkalinity
Alkalinity is defined as the capacity of an aqueous solution to
neutralize acids. Alkalinity is an influential parameter on the sustain-
able performance of anaerobic digestion systems. Production of
methane which is a valuable product of these systems takes place
around pH 7. Substrates with high alkalinity can maintain this pH level
against carbon dioxide, which is produced during anaerobic digestion
and forms carbonic acid in the liquid phase, and also VFAs. Animal
manures have high alkaline capacity which turns them into suitable
substrates for anaerobic digestion. In order to show the high alkalinity
of manure, Cheng and Zhong [50] determined the concentration of
VFAs both in mono-digestion of cotton stalk and its co-digestion with
manure. The concentration of VFAs in mono and co-digestion was 320
and 3000 mg/L, respectively; while the pH was about 6.5 in both
experiments without any significant change. The high VFA concentra-
tion could cease the process if the buffering capacity of the medium was
not enough.
For maintaining the pH at desired level, some chemicals can be
used. Chemicals such as sodium bicarbonate (NaHCO3), lime (CaO)
and sodium carbonate (Na2CO3) are examples of materials that can
increase the alkalinity of the system [47,49,81]. However, use of
chemicals to maintain pH level can have some side effects. Ionization
of these chemicals and production of certain ions can inhibit the
process. As an instance, presence of Na+ at high concentrations can
inhibit anaerobic digestion and decay the whole process. Llabrés-
Luengo and Mata-Alvarez [81] reported that addition of CaCO3 for
increasing the alkalinity of the solution during co-digestion of wheat
straw with pig manure resulted in significant improvement in methane
yield. In another investigation performed by Li et al. [49], the effect of
addition of NaOH to a 1 L laboratory scale digester in co-digestion of
corn stover with cattle manure was considered. The outcomes verified
the positive effect of alkalinity on anaerobic batch digestion. They
reported 4.2 g CaCO3/L as alkalinity index of cattle manure; this level
S.A. Neshat et al.
of alkalinity prevented the acidification of digester and improved the
methane production yield. In another study conducted by Li et al. [47]
the alkalinity of kitchen wastes was reported as zero. Lack of alkalinity
led one of their experiments to failure. They used NaOH, cattle manure
and CaCO3 to increase the alkalinity of their samples and reported
significant improvement in methane production yield and stability of
the digester.
5.6. Carbon to nitrogen (C/N) ratio
There is a certain need to carbon and nitrogen for microorganisms
in any growth environment as well as anaerobic digestion systems.
Reports are different for the optimum range of C/N; a value in the
range of 15–30 has been reported as the optimum C/N ratio [33,82–
84]. Deviation from the optimum C/N ratio affects the biogas produc-
tion. Reports confirmed that higher C/N ratios cause nitrogen defi-
ciency for microbial growth and then lack of nitrogen leads the process
to lower methane production yield due to deactivation of methanogens
and possible failure of the entire process [82]. On the contrary, lower
C/N ratios limit the microbial growth due to carbon shortage which can
lead to accumulation of ammonia nitrogen and VFAs in the digester
[83,84].
As prior mentioned, for plant based materials, C/N ratio is too high
and their complicated lignocellulosic structure makes them improper
substrates for biogas production [33]. While, the low C/N ratio of
manure and its carbon deficiency retards its efficient anaerobic
digestion. However, co-digestion of these two substrates can be a
solution to address the imbalance C/N ratio of each substrate.
Lehtomäki et al. [61] reported that the optimum C/N ratio for
anaerobic digestion is 25–32; while, the C/N ratio of their cow manure
was 11–14. To alleviate this issue, they added 30–40% crops to cow
manure; upon its addition, the C/N ratio of the mixture increased to
15–25 which was close to the optimum values for co-digestion. Cheng
and Zhong [50] reported that C/N ratio of their cotton stalk sample was
about 50 which was far away from the optimum range for anaerobic
digestion. Addition of swine manure to their lignocellulosic sample was
effective to modulate the C/N ratio to 25; as a result, the biogas
production enhanced. In another study carried out by Zhang et al. [85]
the C/N ratio of the influent in co-digestion of sorghum stem and cow
manure was adjusted to25 by urea. By this, they were able to achieve
the biogas yield of 413 mL/g VS which was 26% higher than that
obtained from digestion of sorghum stem as the mono-substrate.
5.7. VFA concentration
Volatile fatty acids (VFAs) are the intermediate products of
methane production pathway. Acetic acid, butyric acid and propionic
acid are the major products of anaerobic digestion. These acids are
indicators of anaerobic digestion and can be used for evaluation of the
anaerobic digestion performance. Nevertheless, accumulation of these
organic acids can lower the pH level to below 6. Consequence of this
low pH is inactivation of methanogenic microorganisms and/or change
of the pathway of microorganisms in the microbial consortium which
eventually concludes to the production of unwanted or worthless
products [45]. A concentration of about 1500–2000 mg/L of VFAs
can possibly inhibit the anaerobic digestion [86,87]. Use of manure
with high alkaline capacity can substantially neutralize the acids. Cheng
and Zhong [50] determined the concentrations of VFAs in anaerobic
digestion of cotton stalk as the sole substrate and compared the results
to those obtained from co-digestion of cotton stalk and swine manure.
Although the concentration of VFAs in co-digestion was almost ten
times that of mono-digestion, the system could sustain its performance
due to the presence of manure. They reported that acetic acid was the
main VFA produced in the digester. In another study carried out by
Bah et al. [45], a high concentration of VFAs in the range of 300–
1000 mg/L was observed in co-digestion of palm pressed fiber and
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cattle manure. It was inferred that the high concentration of these acids
could be related to the breakdown of lipids of the substrate. Estevez
et al. [53] reported that in co-digestion of cattle manure and Salix, the
highest concentration of VFAs was 320 mg/L which was far below the
inhibitory concentration of VFAs; this was the advantage of using cattle
manure with high alkaline capacity. Rico et al. [29] conducted an
investigation on a UASB reactor for co-digestion of dairy manure and
cheese whey. They reported that there was no VFA in their effluent
until the condition of reactor changed and stability of the system faded
out as a result of increase of cheese whey to manure ratio in the feed
(85% cheese whey).
The best strategy for stopping the acidification of the system due to
increase of VFA concentrations is to cease the feeding of the system and
let the acetoclastic microorganisms to grow and increase the pH level
by consuming the VFAs [55]. Aboudi et al. [55] reported that in a study
conducted on a semi-continuous anaerobic digestion reactor for co-
digestion of pig manure and sugar beet byproducts, they recovered
their system after acidification by stopping the feeding to decrease the
VFAs concentration; the method was successful without any inhibition
effect.
6. Pretreatment
Pretreatment of substrate is a common step in processing ligno-
cellulosic feedstock where tough materials such as hemicellulose and
cellulose are turned to soluble compounds. These natural biopolymers
are not directly useable by microorganisms and have poor biodegrad-
ability. Lignin also can poorly be degraded in anaerobic digestion and
to have an effective digestion, it has to be disrupted or the material
should be delignified. Upon pretreatment of complex lignocellulosic
materials, simple soluble compounds are produced which can be easily
consumed by microorganisms. Pretreatment of substrate increases the
COD level of the system which is an indication of the efficiency of the
pretreatment process. Pretreatment methods can be divided into three
main categories including chemical, physical and biological pretreat-
ments. A combination of these pretreatment methods can also be used.
An overview of the effective pretreatment processes is provided here;
although some of these methods are quite potential to deliver well
prepared substrates for anaerobic co-digestion, they are still under-
utilized and few works have been published in this regard.
6.1. Physical pretreatment
Heating and pressurizing lignocellulosic materials are common
methods to crush these complicated materials to simple compounds.
For instance, use of autoclave has been reported as an effective method
for degrading lignocellulosic feedstock [88]. Though, high energy
demand and operation at high pressure are considered as the dis-
advantages of these methods. The most common pretreatment meth-
ods used in anaerobic digestion are thermal pretreatment, steam
explosion and mechanical pretreatments, while use of other methods
such as ultrasonic and irradiation are less common.
Thermal pretreatment is commonly performed using steam or hot
water. Kalamaras and Kotsopoulos [52] used 2% (w/v) NaOH for
pretreatment of different crops and autoclaved the chemically treated
biomass at 120 °C (thermochemical pretreatment). They repeated
same experiment except that the substrate was soaked in water for
20 min and then autoclaved at 120 °C (thermal pretreatment). The
result of their investigation revealed that thermal pretreatment did not
improve the solubilization of organic matters, as cellulose and hemi-
cellulose become soluble at temperatures above 150 °C. In contrast,
thermochemical pretreatment increased the soluble fraction of organic
matter and it was justified that high temperature in the presence of
dilute NaOH broke the links between lignin and carbohydrates and also
disrupted the lignin structure. They reported that thermally and
thermochemically pretreated agricultural wastes co-digested with cattle
S.A. Neshat et al.
manure resulted in methane production of 271 and 255 L/kg VS,
respectively.
Steam explosion which is known as high-pressure steam treatment
is one of the most effective methods for disrupting the lignocellulosic
structure of substrates. This method combines high temperature and
rapid reduction of pressure that leads to the destruction of lignocellu-
losic structure. Thermal pretreatment of lignocellulosic biomass with
steam explosion was used by Bauer et al. [89] and Vivekanand et al.
[90]; they reported that pretreatment increased the biodegradability of
the lignocellulosic materials by 20%.
Boussaid et al. [91] and Estevez et al. [53] reported that steam
explosion could increase the methane production potential of Salix by
50%. However, a different observation was reported by Risberg et al.
[33] who used steam explosion for pretreatment of wheat straw. They
investigated anaerobic digestion of cattle manure as the sole substrate
as well as co-digestion of manure and pretreated wheat straw; they did
not observe any enhancement in biogas production. In fact, in their
experiment steam explosion was not as efficient as they expected and
did not improve biogas production and just imposed additional cost to
the process. They concluded that steam explosion could be effective at
temperatures above 160 °C. As a disadvantage of steam explosion
pretreatment is the release of phenolic compounds and furfural that
can have inhibitory effect on methane production yield by affecting the
methanogenic microorganisms [53,92].
Mechanical pretreatment is performed with the aim of reducing the
size of materials and enhancement of heat and mass transfers so that
consequent digestion process can be facilitated. Milling is a common
method of mechanical pretreatment which provides smaller particles.
In a set of experiments carried out by Kalamaras and Kotsopoulos [52],
the crops were blended before being co-digested by cattle manure.
Results showed that the implemented pretreatment did not enhance
the solubility of organic matters; however, it was a required pretreat-
ment to reduce the biomass size to below 1 cm.
Ultrasonic waves have been used to crush the cell walls of plants in
recent years. Use of ultrasound waves can increase the soluble COD
and hence the accessible nutrients for microorganisms will increase.
Increased availability of nutrients can encourage the microorganisms
to consume substrates faster and can reduce the HRT. Chiu et al. [93]
undertaken a study to examine the effect of ultrasound on the soluble
COD of waste activated sludge before anaerobic digestion. They
reported that use of ultrasound increased the soluble COD from 36%
to 89%; also, the soluble organic nitrogen increased from 34% to 42%.
It should be mentioned that although this method is effective for
breaking down the plant cells membranes and extraction of their
content and also increase of soluble COD concentration, however, the
high cost of the ultrasonic pulse generator and high energy consump-
tion are considered as the major drawbacks of this pretreatment
method [94,95].
6.2. Chemical pretreatment methods
Use of chemicals to break down the bonds and transform non-
biodegradable materials to biodegradable compounds which could be
utilized as substrate in anaerobic digestion is a common method for
pretreatment of lignocellulosic materials. Chemical pretreatments are
usually performed at ambient condition without the need to high
temperature and pressure. The high cost of chemicals and environ-
mental pollution caused by chemical agents however are considered as
the disadvantages of chemical pretreatment.
Lignocellulosic materials can barely be degraded by hydrolytic
microorganisms. The poor degradability of these materials under
anaerobic condition hinders the use of them as the sole substrate for
anaerobic digestion. Alkali pretreatment using NaOH, KOH, etc.
solution is a cost effective method which can efficiently enhance the
biodegradability of lignocellulosic materials. Cheng and Zhong [50]
reported a remarkable improvement in methane production in anae-
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robic digestion of cotton stalk and swine manure with alkali pretreat-
ment; whereas, without pretreatment, cotton stalk had a very low
methane yield. They found that alkali pretreatment was more effective
than acid hydrolysis pretreatment. The COD level of their alkali
pretreated substrate was more than that of acid hydrolyzed sample
which was an indication of superior performance of alkali pretreatment
for disruption of lignocellulosic structure of cotton stalk. It was also
reported that pretreatment using 2% NaOH solution in an autoclave at
121 °C for 90 min resulted in a delignification efficiency of 65.63% and
converted 60.8% of cellulose to glucose. Li et al. [49] carried out alkali
treatment on corn stover before being subjected to anaerobic digestion
along with cattle manure. They drenched corn stover in 2% NaOH
solution at room temperature for 3 days. The NaOH solution was
effective in delignification of corn stover and decreased the lignin
content from 8.4% to 7.5% which could facilitate the access of
microorganisms to the nutrients. Similar finding was reported by You
et al. [96] who investigated the effect of alkali pretreatment on biogas
production in anaerobic co-digestion of corn stover and swine manure.
Upon alkali pretreatment of corn stover, its lignin content reduced by
78.5%. They emphasized on shorter digestion time, higher methane
content and higher biogas yield as advantages of alkali pretreatment of
corn stover. In another co-digestion process performed by Mel et al.
[97], corn husk was soaked in NaOH solution at room temperature for
5 days prior to be co-digested with cow dung. In their experiment, OLR
was also increased. As a result, methane content of biogas improved
from 60% to 80%. They explained this enhancement as a synergic effect
of OLR and alkali pretreatment. Alkali pretreatment degraded lignin
content of corn husk and higher OLR provided more nutrients for the
microorganisms. Wei et al. [98] evaluated the effect of three different
pretreatments methods on anaerobic co-digestion of corn stover and
cattle manure including alkali, ammonia and biological pretreatments.
They reported that pretreatment by a 4% NaOH solution increased the
VS removal by 14.48–16.84%; also, pretreatment enhanced the
methane production by about 25.40–30.12%. Although NaOH has
been extensively used for alkali pretreatment of lignocellulosic materi-
als, however, the inhibitory effect of Na+ ion on anaerobic digestion
cannot be neglected. The Na+ ion can inhibit the activity of some
microorganisms, especially methanogenic bacteria [99].
Acid hydrolysis is an alternative method for degradation of lignocel-
lulosic materials. Sulfuric acid, hydrochloric acid and nitric acid were used
for acid pretreatment of lignocellulosic feedstock. In this method, tough
materials such as hemicellulose and cellulose are partially broken down to
simple carbohydrates. Dilute acid pretreatment can degrade hemicellulose
components to monomeric sugars including pentoses and hexoses and
oligomers which are soluble in water. Acid hydrolysis can be performed
either at high or low concentrations of acid. Commonly high concentration
acid pretreatment is carried out at low temperatures; whereas, low
concentration acid hydrolysis is along with use of high temperatures
[94]. Despite the high efficiency of this method, the high cost of acid
recovery, both to reuse the acid and protect the environment, is
considered as a disadvantage; also in case of using sulfuric acid remaining
sulfur could lead to H2S production [100,101]. Cheng and Zhong [50]
reported that acid hydrolysis improved the production of biogas in co-
digestion of cotton stalk and swine manure. They found that acid
hydrolysis was not that much effective for cellulose conversion but so
effective in delignification, where use of 2% acid at 121 °C within 90 min
removed 95.23% of lignin content while cellulose conversion was only
23.85%. In another study undertaken by Li et al. [47], dilute sulfuric acid
was used for pretreatment of cattle manure before being co-digested with
kitchen waste. Results showed that acid pretreatment was effective for
decomposition of lignocellulosic materials where cellulose, hemicellulose
and LCH (lignin + cellulose + hemicellulose) degraded by 9.4%, 28% and
13.1%, respectively. It was reported that soluble COD increased from
8.7% to 24.5% after acid pretreatment which was a confirmation of the
effectiveness of the implemented acid pretreatment.
Use of ammonia solution is one of the physicochemical methods in
S.A. Neshat et al.
pretreatment of lignocellulosic materials. This method is known as one
of the most effective routes for lowering the lignin content of
lignocellulosic materials [102,103]. In this method, lignocellulosic
materials are soaked in liquid ammonia at high temperatures (90–
100 °C) [94]. In fact, ammonia, high temperature and pressure are
considered as the three sides of delignification triangle. To examine the
effect of ammonia pretreatment on promotion of anaerobic digestion,
Zhang et al. [104] used 2% ammonia solution for pretreatment of
maize stalk to be co-digested with swine manure and achieved 17.5%
increase in biogas yield. Dongyan et al. [105] reached to 52% increase
in biogas yield by treating straw with 4% ammonia solution. Wei et al.
[98] reported that use of ammonia solution for pretreatment of corn
stover for co-digestion with cattle manure increased the VS removal by
25.4–30.12%.
6.3. Biological pretreatment
Biological pretreatment is defined as use of any living organism to
destruct the lignocellulose matrix of biomass. Low energy consump-
tion, no production of toxic materials and high yield are the advantages
of biological pretreatment [106]. Compared to chemical and physical
methods, biological pretreatment methods consume less energy and
have no need to chemicals and are environmentally benign [106].
However, biological processes are slow and sensitive processes that
hardly can be controlled. Use of fungi such as white, brown and soft-rot
fungi is common in treatment of lignocellulosic materials [107–111].
Also use of hydrolytic enzymes, either for pretreatment or as direct
additive, as well as cellulose-degrading bacteria is known to enhance
the degradation efficiency [6112]. In a recent study conducted by Wang
et al. [113] enzymatic pretreatment was carried out on corn straw
before being co-digested with cow manure. They reported an increment
of 110.79% and 103.20% in methane yield by addition of amylase and
cellulase enzymes, respectively. Although enzymatic pretreatment
route is yet to be fully utilized and to the best of authors’ knowledge
implementation of this method in anaerobic co-digestion in the
literature is very scarce, it seems this technology has high potential
for improving the degradation efficiency and thus enhancement of
biogas production.
A summary of anaerobic co-digestion studies of manures and
lignocellulosic materials available in the literature along with the
detailed operation conditions and methane production yields is pro-
vided in Table 1.
7. Inhibitors
Any severe deviation from optimum process conditions can disturb
the anaerobic digestion. Considering that many parameters are in-
volved in anaerobic digestion, various intermediates and compounds
can play the role of inhibitor. Inhibitory effect of some agents has been
proved by researchers and many others are suspicious to be inhibitor
for anaerobic digestion. The inhibitors of anaerobic digestion can be
categorized into two groups: the substances which introduce to the
system through feed stream and the intermediate components which
are inhibitor at high concentrations. Some of the main inhibitors are
discussed here. VFAs act as a double edge blade; they are one of the
indicators of correct balance between hydrolysis, acidogenesis and
methanogenesis. In a stable anaerobic digester, concentration of VFAs
is about 50–250 mg/L [121]. On the other hand, high concentrations of
VFAs can inhibit anaerobic digestion by lowering the pH level. Li et al.
[41] reported that during co-digestion of rice straw and cow manure,
VFAs were the most important inhibitors by lowering the pH, where
increase of OLR led to the increase of VFAs and thus reduction of pH.
Among VFAs, the most important inhibitor is propionate. Propionate
degradation rate is the lowest among VFAs [41]. It has been reported
that the inhibitory concentration of VFAs is around 1500 mg/L [86];
yet there are other studies reporting that anaerobic digestion didn’t fail
317
Renewable and Sustainable Energy Reviews 79 (2017) 308–322
up to 10,000 mg/L of acetic acid or butyric acid [121].
Phenolic compounds, furans and also furfurals are produced during
the steam explosion pretreatment process [92,122]. Risberg et al. [33]
reported that phenolic compounds and furans were produced during
the steam explosion of wheat straw; these materials caused inhibition
on methane production during subsequent co-digestion with manure.
Ammonia has both advantages and disadvantages for anaerobic diges-
tion. It can act as a pH neutralizer against VFAs and maintain the pH at
optimum level; ammonia is also a valuable nitrogen source for
methanogenic bacteria. On the contrary, high concentrations of
ammonia can intoxicate the microorganisms and inhibit anaerobic
digestion. A critical concentration of 3000 mg/L for NH4+-N was
reported by McCarthy [123] above which, no anaerobic digestion can
take place. Several attempts have been made to alleviate the inhibition
caused by ammonium. Working under mesophilic condition was
proposed as a solution which can stabilize the digestion against
ammonia inhibition [59]. Use of industrial clay residues as inorganic
additive to reduce the ammonia inhibition was investigated by Jimenez
et al. [116] in co-digestion of pig manure and rice straw. Results
showed that digestion of high manure concentration could be con-
ducted without any inhibition. The positive effect of clay in reducing
ammonia inhibition can be explained by its ammonia adsorption
capacity where ammonium ions are trapped in aluminosilicate pores
and removed from aqueous solution [124].
Cyanide at high concentrations is considered as an inhibitor for
methanogenic activity [125,126]. In a study conducted by Glanpracha
and Annachhatre [127], anaerobic co-digestion of cyanide contained
cassava pulp and pig manure was performed. They achieved methane
yield and VS removal of 82% and 0.38 kg VS/ m3.day, respectively.
They reported that their semi-continuous digester had stable perfor-
mance and could tolerate up to 9 mg/L of cyanide.
Use of sulfur oxide as electron acceptor by sulfate reducing bacteria
and producing S2- can affect acidogenesis and methanogenesis. In the
presence of sulfate, sulfur reducers compete with methanogens for
substrate; also reports showed that at high sulfate concentration they
compete with both acidogens and methanogens and convert all of the
anaerobic digestion products to CO2 and H2S [67]. The hydrogen
sulfide produced during degradation of sulfur containing proteins
[121] can inactivate various microorganisms such as methanogenic
bacteria [46]. Any process which may introduce Na+ ion into the
medium should be controlled; otherwise, high concentration of this ion
can inactivate the microorganisms and lead them to death phase and
eventually terminate the anaerobic digestion [97].
Much of the antibiotic fed to animals and livestock goes literally to
their waste. High concentrations of antibiotic residues in manure can
also have inhibitory effect on anaerobic digestion. As the nature of
antibiotic is to kill or deactivate living organism, the anaerobic
digestion consortium is not exempted from this rule. Use of antibiotics
at dosages recommended by veterinary organization does not have any
inhibition effect on anaerobic digestion [128]. Accumulation of solids is
another source of inhibition during anaerobic digestion. Estevez et al.
[53] reported that in co-digestion of cow manure and Salix, accumula-
tion of solids in the bioreactor which happened after 90 days decreased
the methane yield.
8. Methane upgrading of biogas
The biogas produced from anaerobic digestion is predominantly
comprised of methane (55–65%) and carbon dioxide (30–35%) and
minor amounts of other gases including hydrogen sulfide with con-
centrations from several hundred to a couple of thousand ppm, water
vapor and other trace gases [129,130]. The heating value of biogas is
estimated around 5300 kcal/m3 (600 BTU/ft3) [129]. This heating
value is associated with the methane content and the presence of CO2
in the biogas lowers its heating value. The heating value of biogas can
be improved by about 30% through reducing its CO2 content [131]. In
 Table 1
Summary of anaerobic co-digestion studies of animal manures and lignocellulosic residues for biogas production.

Manure type Co-substrate Reactor type Operating condition Pretreatment Manure/ Inoculum Methane yield Ref.
residue ratio
S.A. Neshat et al.

Cattle manure Palm pressed fiber (C:N= 57.03) 1 L batch bottles Mesophilic condition (37 ± No pretreatment 1:3 Running anaerobic digester using piggery and 346.2 mL/g [45]
1 °C) chicken manure VS.day
OLR= 30 g VS/L
HRT= 45 days (running time)
C:N= 46.61a
Cattle manure Whole stillage (C:N= 10) 5 L laboratory scale Mesophilic condition No pretreatment 15:85 Originated from a large scale biogas plant 0.31 L/g VS [46]
CSTR anaerobic OLR=2.8 g VS/L day operating at mesophilic temperature with
reactor HRT= 45 days source separated municipal household waste
Alkalinity=2.4–6.6 g CaCO3/L and grass silage
C:N= 11.65a
Cattle manure Kitchen waste 1 L laboratory scale Mesophilic condition (35 ± Dilute acid pretreatment of 1:1 (VS ratio) Sludge from a swine waste treatment plant 0.31 L/g VS [47]
anaerobic batch 1 °C) cattle manure
reactor OLR=10 & 20 g VS/L
HRT= 45 days (running time)
Alkalinity=1.7 g CaCO3/L
Cattle manure Corn stover (C:N= 59) 2 L laboratory scale Mesophilic condition (35 ± NaOH solution 1:3 Sludge from a mesophilic anaerobic digester 0.194 L/g VS [49]
anaerobic batch 1 °C)
reactor OLR= 50–80 g TS/L
HRT= 45 days (running time)
Alkalinity= 2.1 g CaCO3/L
C:N=32–45
Swine manure Cotton stalk (C:N= 50) 500 mL serum 35 °C Acid hydrolysis or alkali 1:1 Wastewater treatment plant 0.267 L/g VS [50]
bottles HRT= 19–24 days (technical pretreatment (acid)
digestion time) 0.296 L/g VS

318
C:N=25 (alkaline)
Pig manure Dewatered sewage sludge (C:N= 250 mL serum Mesophilic condition NA 2:1 Sludge from a wastewater treatment plant 315.8 mL/g VS [114]
6.76) bottles HRT= 85 days (running time)
C:N=11
Cow manure Salix 6 L CSTR (semi 37 °C Steam explosion 53:47 Sludge from anaerobic digester 0.235 L/g VS [53]
continuous) OLR= 2.6–3.1 g VS/L. day
HRT= 30 days
C:N=23–39
Pig manure Algae 160 mL glass serum Mesophilic temperature Lipid and protein extracted 85:15 Bottom of an anaerobic lagoon ~ 0.325 L/g VS [54]
bottle HRT= 70 days (running time) algae
Cattle manure Wheat straw (C:N= 100) 8 L laboratory scale 37,44 and 52 °C Steam explosion 75:25, Large scale biogas plant 0.13–0.21 L/g VS [33]
CSTR OLR= 2.8 g VS/L.day 26:74,
HRT= 25 days 78:22,
C:N=11–75 100:0
Chicken manure Agricultural wastes (coconut 500 mL anaerobic 55 °C Ammonia removal from 7:3 (V/V) Sludge from wastewater treatment plant 695 mL/g VS [56]
waste, cassava waste and coffee vials HRT= 62 days chicken manure
grounds) C:N= 21
Pig manure Sugar beet byproduct CSTR (semi Mesophilic condition NA Mixed to have NA 362.2 mL/g VS [55]
continuous) OLR= 7.4 g VS/Lreactor fixed C/N=18.5
HRT= 12 days
C:N=18.5
Dairy manure Switchgrass (C:N= 35.1) Laboratory scale Mesophilic condition NA 2:2 Sludge from a 50 L anaerobic digester 158.6 mL/g VS [115]
anaerobic batch OLR= 5.02% TS/L
reactor HRT= 30 days (running time)
Alkalinity= 4.88 g CaCO3/L
C: N= 29.4a
Pig manure Rice straw (C:N= 48) Laboratory scale Mesophilic and thermophilic NA NA NA NA [116]
batch anaerobic condition
reactor OLR= 28.35 g VSS/L for
(continued on next page)
Renewable and Sustainable Energy Reviews 79 (2017) 308–322
 Table 1 (continued)

Manure type Co-substrate Reactor type Operating condition Pretreatment Manure/ Inoculum Methane yield Ref.
residue ratio
S.A. Neshat et al.

manure, 17.6 g VSS/L for rice

straw
HRT= 30 days (running time)
C:N=7
Swine manure Olive mill wastewater 3.9 L CSTR Mesophilic condition NA 60:40 Digested sludge from a mesophilic anaerobic 373 mL/g VS [117]
OLR= 4.4 g VS /Lfeed. day reactor
HRT= 20 days
Cow manure Energy crops and crops residues 5 L CSTR (semi Mesophilic temperature NA 60:40 Mesophilic farm digester treating dairy 268 L/kg VS [61]
(grass silage, sugar beet tops continuous) OLR= 2 kg VS/m3 day manure and industrial confectionary
and oat straw) (C:N= 15–25) HRT= 20 days byproducts
Cow manure Rice straw (C:N= 47.5) 40 L continuous Mesophilic condition NA 1:1 Sludge from anaerobic pig manure digester 383.5 L/kg VS [41]
bench size anaerobic OLR= 6 kg VS/m3.day
reactor HRT= 19 ± 1 days
C:N= 20–30
Cattle manure Corn stover (C:N= 39.03) 1 L bottle Mesophilic condition Biological and alkali NA Sludge from anaerobic digester of wastewater 0.228 L/g VS [98]
OLR= 65 g TS/L pretreatment (ammonia treatment plant
HRT= 35 ± 1 days solution)
Alkalinity= 5837.5 mg
CaCO3/L
Cow manure Kitchen wastes (C:N= 31.18) 1 L laboratory scale 35 °C NA 1:1 Mesophilic anaerobic digested sludge 179.8 mL/g VS [48]
anaerobic digester HRT= 45 days (running time)
Alkalinity= 6.5–10.5 g
CaCO3/L
Swine manure Corn stover 150 mL serum 35 °C Alkali pretreatment of corn NA Sludge from anaerobic digester of corn stover 350 mL/g VS [96]
bottles HRT= 30 days (running time) stover and swine manure

319
C:N=25
Dairy cattle Shredded and briquetted wheat 30 m3 CSTR Thermophilic condition Mechanical pretreatment 95:5 Sludge from mesophilic and thermophilic 351 L/kg VS [118]
manure straw HRT= 20 days reactors of the Agricultural Research Center
Cattle manure Sheep bedding (C:N= 24) 6 L homemade Room temperature (18.4 ± NA 75:25 No inoculum was used 171 L biogas/ kg [119]
benchtop digester 4 °C) TS
HRT= 21 days (running time)
Cattle manure Silage of cardoon 1 L glass batch Mesophilic temperature No pretreatment 85:15 Well digested beef cattle manure 308 L/kg VS [52]
reactor HRT= 45 days (running time)
Cow dung Corn husk 160 L semi batch Mesophilic temperature Alkali pretreatment NA NA 75.8 mL/min [120]
reactor OLR= 45 g VS/L.day
HRT= 30 days
Liquid fraction Cheese whey 8 L UASB reactor Mesophilic temperature NA 40:60 Biomass from a pilot UASB reactor 9.5 m3/m3 day [29]
of dairy OLR= 28700 g COD/ m3 day
manure HRT= 1.3 days

a
As calculated by the authors of this work, NA: Data were not available.
Renewable and Sustainable Energy Reviews 79 (2017) 308–322
S.A. Neshat et al.
addition to reducing the heating value, the presence of CO2 in biogas
increases the costs for compression and transportation and limits the
economic feasibility for utilizing the biogas at the point of production.
Traces of hydrogen sulfide (H2S) should also be removed from biogas
as it corrodes certain mechanical components of engine generators and
diesel engine [130,131]. To be used as a fuel and also to meet the
environmental standards such as ISO: TC 25 [129], biogas should be
refined and CO2 and H2S should be eliminated from the biogas.
The existing methods for scrubbing CO2 and/or H2S from biogas
include chemical absorption using alkaline and amine solutions, water
and polyethylene glycol scrubbing, pressure swing adsorption, mem-
brane separation, cryogenic separation, use of bio-filter, etc. [130]. H2S
can also be removed by passing the biogas through beds of ferric oxide
and iron [131]. Each of these biogas purification techniques has its own
strengths and weaknesses which include cost considerations, robust-
ness, possibility of in-site biogas upgrading and environmental im-
pacts. In recent years, some attempts have been made to develop
environmentally benign and green technologies for biogas clean-up.
Use of micro algae for elimination of carbon dioxide from biogas which
simultaneously produces oxygen is a new attitude in this regard.
Heubeck et al. [132] conducted a study on CO2 scrubbing from biogas
using algal pond. They investigated different factors on the efficiency of
this method and reported that use of algal ponds for CO2 scrubbing
from biogas is feasible. Kampanatsanyakorn et al. [133] registered a
patent for enhancing methane content of biogas. They claimed that use
of algal pound containing sodium bicarbonate in liquid phase for algae
growth can absorb CO2. They claimed that the method could eliminate
97% of carbon dioxide from the biogas.
9. Future perspective and concluding remarks
Nowadays, there is a global concern over the environmental impact
of landfill gases as they contain considerable amounts of greenhouse
gases including methane and carbon dioxide. The emission of these
gases into the atmosphere largely contributes to the devastating “global
warming” phenomenon, with CH4 being a powerful greenhouse gas
having a greenhouse effect 23 times that of CO2 [133]. Although
dispose of carbon containing wastes without contribution to the
greenhouse effect is impossible, exploitation of the landfill gas as a
renewable energy source can reduce the impact. Production of biogas
through anaerobic digestion of organic wastes has experienced im-
pressive progress during recent years. Yet, due to deficiencies enum-
erated for animal manures, their anaerobic digestion, instead of being
used as fertilizer in farms, needs some developments. Anaerobic co-
digestion of animal manures with lignocellulosic residues offers a
promising route for efficient biogas production which is also in line
with climate friendly farming practices. As this review indicated, so far
many research studies have been undertaken to improve the perfor-
mance and stability of the anaerobic co-digestion process. The pro-
duced biogas, after some refinement can be utilized as energy carrier
for running vehicles, heating applications and electricity production
which makes a great saving in consumption of precious fossil fuels.
Although several investigations have been conducted for production of
biogas via anaerobic co-digestion of manure and lignocellulosic wastes,
little has been done to develop cost effective methods for upgrading and
refinement of the produced biogas. While purified biogas can provide
farmers with revenue and enhance the economic feasibility of the
anaerobic co-digestion.
A major prerequisite for commercializing the technology of anae-
robic co-digestion is to locate the livestock and agricultural farms as
close as possible so that huge amount of lignocellulosic residues and
animal manure will be available abundantly. Otherwise, the cost for
collection of massive quantities of biomass residues, their transporta-
tion and delivery at the plant gate should be reasonable enough to
make the process economically feasible. Combination of a treatment
plant and combined heat and power generation unit will provide
320
Renewable and Sustainable Energy Reviews 79 (2017) 308–322
simultaneous waste management and power generation; the generated
heat and electricity may then be utilized at the same plant. The number
of full scale plants in recent years is increasing [134], but most of them
are treating lignocellulosic materials and sewage sludge [135–137].
Among the active full scale plants which are treating agricultural wastes
and livestock manure is the one located in Marcon, Venice, Italy [138]
which handles 140 t of mixed agro-waste and solid manure and 25 m3
of liquid manure per day at thermophilic condition. A conventional
fixed roof digester is used in this plant and the HRT for anaerobic co-
digestion in the plant is 34 days. Although the number of industrial co-
digestion plants is limited and use of anaerobic digestion as the best
long-term solution for management of organic waste is yet to be
assured, as long as it is economic and benefits the environment, it will
continue to grow.
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