Renewable Energy 98 (2016) 108e119

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Renewable Energy
journal homepage: www.elsevier.com/locate/renene

Biogas from anaerobic digestion processes: Research updates

Quanguo Zhang a, Jianjun Hu a, Duu-Jong Lee a, b, c, d, *
a
Collaborative Innovation Center of Biomass Energy, Henan Agricultural University, Henan Province, Zhengzhou, China
b
Department of Chemical Engineering, National Taiwan University of Science and Technology, Taipei 10607, Taiwan
c
Department of Chemical Engineering, National Taiwan University, Taipei, 10617, Taiwan
d
R&D Center for Membrane Technology, Department of Chemical Engineering, Chung Yuan Christian University, Chungli, 32023, Taiwan

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

Article history: Anaerobic digestion (AD) is a biological process that can convert organic substrates to biogas in the
Received 10 January 2016 absence of oxygen. The AD process has been practiced for centuries; however, it is still a research focus in
Received in revised form contemporary literature. This mini-review selected papers published in 2015 and summarized the
6 February 2016
improvement and technological advancement and revealing current research and development trends
Accepted 9 February 2016
Available online 19 February 2016
for the biogas from AD process. A discussion on the challenges and prospects for developing improved
AD technologies is provided.
© 2016 Elsevier Ltd. All rights reserved.
Keywords:
Biogas
Anaerobic digester
Co-digestion
Operation
Modeling

1. Introduction platforms, Bioresource Technology ranked top in number of

Anaerobic digestion (AD) is the biological degradation process of
organic substrates in the absence of oxygen [1]. In natural habitat,
complex organic substrates need hydrolysis, acidogenesis, aceto-
genesis, and methanogenesis for completing AD reactions. The
methanogens can grow at low redox potential with coupling to
substrate-level or electron transport phosphorylation, producing
biogas being one of the main products which is a mixture of
gaseous compounds, principally methane (CH4) and carbon dioxide
(CO2), via volatile fatty acid (VFA) degradation [2,3].
Biogas is a renewable energy source that can be harvested from
organic waste, which received intensive research interested these
decades [4]. Numerous studies were reported on all aspects of
biogas production, processing and utilization. The Web of Science™
database search using topic of “biogas” on 2015.12.30 led to a total
of 9395 papers, in fields such as energy fuels (3317), environmental
sciences (2670), and biotechnology applied microbiology (2472),
and with authors from China, Germany and United States contrib-
uting about 31% of these published papers. In all energy-related
* Corresponding author. Department of Chemical Engineering, National Taiwan
University of Science and Technology, Taipei 10607, Taiwan.
E-mail address: djlee@ntu.edu.tw (D.-J. Lee).
biogas papers published (1075), followed by Biomass Bioenergy
(267), International Journal of Hydrogen Energy (243) and
Renewable Energy (200). The number of these papers had received
128,462 citations, with relevant articles with >500 citations being
available [5e8].
Comprehensive list of biogas papers is exhausting. This mini-
review collected papers published in most recent year in journal
Bioresource Technology, Biomass Bioenergy and Renewable Energy,
a total of 151, as the samples for providing a snapshot of current
trends for biogas from AD research.
2. Status report
AD is applied worldwide as a source for generating biogas from
organic waste. The recent works discussed the current status for
local applications. For instance, Anyanwu et al. [9] discussed the
biogas production from cassava waste in Nigeria and claimed that
the yield of biogas at 0.6 L/kg total solids could augment primary
energy needs of Nigeria. Ruile et al. [10] surveyed the efficiency of
21 full-scale biogas production plants in southern Germany which
handle livestock manure, maize silage, grass silage and grain silage
as feedstocks. Mudasser et al. [11] studied the feasibility of using
wind-biogas hybrid system on energy supply for areas in Green-
wood, Sydney.

http://dx.doi.org/10.1016/j.renene.2016.02.029
0960-1481/© 2016 Elsevier Ltd. All rights reserved.
 Q. Zhang et al. / Renewable Energy 98 (2016) 108e119
Sovacool et al. [12] provided an overview of the International
Fund for Agricultural Development and Biogas International in
Kenya, which helped install about 500 anaerobic digesters over the
rural regimes to power the households. These installed units are
mostly still in operation. The challenges faced for this program and
the difficulties to be solved provided a nice reference for applying
small-scale anaerobic digesters applied in rural areas.
3. Substrate
Substrates are the organic feedstocks for AD applications. Sub-
strates that attracted recent research interests included the algal
biomass and wastes from other treatment units. Maize silage has
become a substrate of focus in Germany since excess AD plants are
recently installed and operated [13]. Estimation of methane pro-
ductivity from specific substrates is also of practical interest for AD
research.
3.1. Algal biomass
Algae can grow much faster than higher plants so the former is
regarded as a promising carbon sink during its cultivation [14].
Producing biogas from microalgae using AD may not be easy since
the cell walls of microalgae are generally thick for slow hydrolysis
and the carbon to nitrogen ratio may be too low since the micro-
algae has high protein contents [15,16].
3.1.1. Microalgae
Numerous microalgae species were cultivated as carbon dioxide
sink and the substrate for AD. For instance, Fan et al. [17] evaluated
the methane productivity by AD of Macrocystis pyrifera in seawater
at mesophilic temperature. Gutierrez et al. [18] applied potato
starch as flocculants to enhance harvesting of Chlorella sp. and then
tested the methane productivity from the collected algal biomass
under AD. Caporgno et al. [19] co-digested marine microalgae,
Isochrysis galbana, and freshwater microalgae, Selenastrum capri-
cornutum, with sewage sludge under mesophilic and thermophilic
conditions. Mahdy et al. [20] co-digested microalgae biomass
(Chlorella vulgaris) and primary or secondary sludge from waste-
water treatment plant.
In general, direct AD of microalgae is not so effective in terms of
biogas productivity. Thermal pretreatment could enhance 62%
methane yield for C. vulgaris [18]. The co-digestion of algal biomass
and other substrates also enhance methane productivity by
providing easy hydrolysis and hence methanogenesis.
3.1.2. Macroalgae
Saline macroalgae biomass was cultivated from water environ-
ments without competition with freshwater resources. AD of
Sargassum muticum needs consideration of the possible adverse
effects by excess salts [21]. However, the relatively thick cell walls
by marine macroalgae need intensive pretreatments for enhancing
the methane productivity. For instance, Hermann et al. [22] ensiled
five seaweed species with their storage up to 90 d and noted that
ensilage could not only lead to loss in VS during storage but also
increased the methane yield during AD. Oliveira et al. [23] co-
digested macroalgae Sargassum sp. with glycerol or with waste
frying oil for increasing methane productivity of macroalgal
biomass. Yazdani et al. [24] studied the AD of Nizimuddinia zanar-
dini, a brown macroalgae from Persian Gulf, with pretreatment by
dilute sulfuric acid and hot water, followed by enzymatic hydrolysis
by cellulase and beta-glucosidase. The pretreatments could in-
crease biogas yields.
109
3.1.3. Algae-bacteria flocs
Bacteria could grow with algae in cultivation systems. The
bacteria compete with algal cells with the available nutrients and
could even utilize algal biomass as their own substrates for growth.
In full-scale applications algae-bacteria flocs rather than pure algal
biomass are harvested from the cultivation unit. van Den Hende
et al. [25] cultivated microalgal bacteria flocs from an outdoor
raceway pond and noted low digestion efficiency and a low biogas
profit of the cultivated biomass. The collected flocs were pretreated
using mechanical and biological pretreatments for enhancing
methane productivity [26].
3.2. Waste from other processes
Recent studies were performed to use the wastes from other
treatment units. The liquor fraction of pyrolysis products (besides
non-condensable gases, tars and biochar at 330, 430 and 530
C)
was utilized as the AD substrates [27]. Narra and Balasubramanian
[28] studied AD of residues from bioethanol manufacture from 10%
rice straw in four combined upflow anaerobic sludge blanket
reactors þ anaerobic filters at thermophilic and mesophilic tem-
peratures. In case of anaerobic recalcitrance, the waste was pro-
posed to be pretreated for enhancing digestibility [28]. The crude
glycerine from biodiesel manufacturing factories was added to
sewage sludge to increase the C/N ratio of substrate for possible
enhancement of methane productivity [29]. These authors noted
adverse effects on methane productivity with added crude glyc-
erine since the latter could be easily hydrolyzed to suppress sus-
pension pH and lead to inhibition effects.
3.3. Co-digested substrates
Co-digestion tests with two or more substrates are a research
focus for the sampled literature works (Table 1). One reason for
adopting co-digestion of substrates is to balance the C/N ratio of the
feedstock. For instance, giant cane or corn silages (hard) with pig
slurry (easy) were co-digested in continuous stirred tank lab-scale-
reactor [30]. Sugar beet cossettes (hard) and pig manure (easy) was
co-digested in a semi-continuous stirred tank reactor under mes-
ophilic conditions [31].
Co-digestion of substrate A that would produce excess metab-
olites to inhibit methanogenesis could be compensated by adding
substrate B. For instance, Battista et al. [32] tested the co-digestion
treatment of the mix of the most abundant agro-food wastes in
Puglia (Italy), olive pomace and milk whey, which are wastes with
pH 3.5 and high total nitrogen, total ammonia and total phospho-
rous quantities in 50-L and 2 m3 digesters. With the olive pomace
from a three phase centrifugation, these authors generated at 35
C
and 10% w/w total solids in continuous mode at 1.23 L/L-d methane
when the inhibitory effects of ammonia and polyphenols concen-
trations are both low. Haider et al. [33] mixed the food waste and
rice husk and co-digested the mix for finding the mixing ratio that
could overcome volatile fatty acid accumulation in mesophilic
digestion. Adding food waste would reduce suspension pH hence
reducing methane productivity.
Certain co-digested substrates considered are to balance the C/N
ratio of the feedstock for AD. For instance, Li et al. [34] co-digested
Manyflower silvergrass of C/N ¼ 45.46 and microalgae of C/
N ¼ 5.48. The addition of microalgae would reduce suspension pH,
increase lactic acid concentration and ammonia concentration, and
shifted the associated microbial communities.
Studies that are hard to hydrolyzed are pre-treated then the li-
quor was co-digested with another substrate for improve overall
methane production. For instance, Zieminski et al. [35] co-digested
sugar beet pulp silage and vinasse in 1-L reactor at mesophilic
110
Table 1
Sampled literature works on anaerobic co-digestion.
Reference Substrates
Luca et al. [30] giant cane (plant gowing on
disturbed soil) or corn
silages þ pig slurry
Aboudi et al. [31] sugar beet cossettes þ pig
manure
Battista et al. [32] olive pomace þ milk whey,
Haider et al. [33] food waste þ rice husk
Li et al. [34] Manyflower
silvergrass þ microalgae
Zieminski et al. sugar beet pulp silage þ vinasse 1-L glass bottles at
[35]
Pokoj et al. [36] Two annual silages, four
perennial crops silages, and
four mixes of the two.
Riggio et al. [37] cow slurry þ apple pulp þ olive 128-L mesophilic batch NA
pomace
Li et al. [38] organic waste fat, oil and
grease þ wastewater sludge
Zarkadas et al. [39] food waste þ cattle manure
Spielmeyer et al. Sludge þ antibiotics
[40]
Shofie et al. [41] mix of coffee grounds þ coffee Thermophilic
wastewater þ milk
waste þ municipal sludge
Moraes et al. [42] vinasse from bioethanol
production plant þ straw and
lime fertilizer or þ cow manure 37 C.
Liu et al. [43] wheat stalks þ pig manure or
cow manure, and rape
stalks þ pig manure or cow
manure
Li et al. [44] rice straw þ cow manure
Li et al. [45] rice straw þ pig manure
Rico et al. [46] cheese whey þ liquid fraction of 21-L continuous-flow
dairy manure
Kim et al. [47] food waste leachate þ saline
microalgae (Chlorella sp.) þ raw 35
C
sludge
Song and Zhang 1e4% H2O2-pretreated wheat
[48] straw þ dairy cattle manure
Razaviarani and biodiesel waste
Buchanan [49] glycerin þ municipal
wastewater sludge
Khoufi et al. [50] olive mill wastewater þ liquid 70-L mesophilic jet-
poultry manure
Menardo et al. [51] rice straw silage þ maize
silage þ triticale silage
Q. Zhang et al. / Renewable Energy 98 (2016) 108e119
Reactor Pretreatment Remark
3-L continuous stirred NA Giant cane has lower methane productivity than corn. However,
tank lab-scale reactor at since the former is gorwing faster than the latter, the biogas yield
38
C. per ha for the former was higher than for the latter.
10-L semi-continuous NA OLR 11.2 gVS/L-d could generate 2.91 L CH4/L-d. Too low hydraulic
mesophilic stirred tank retention time of the reactor would accumulate volatile fatty acids
reactor to reduce suspension pH, which would lead to system failure.
2 m3 mesophilic batch NA 1.23 L methane/L-d when the inhibitory effects of ammonia and
reactor polyphenols concentrations are low.
1-L bottles at 37
C NA Adding food waste would reduce suspension pH hence reducing
methane productivity.
400-mL batch bottles at NA Adding microalgae reduce suspension pH, increase lactic acid
35
C concentration and ammonia concentration, and shifted the
associated microbial communities.
enzyme mix (3:1) The highest biogas productivity (598.1 L/kg VS) was achieved at mix
37
C. of Celustar XL and ratio of 3:1 (w/w). Enzymatic pretreatment of pulp silage was also
Agropect pomace at noted to significantly increase methane yields
50
C for 7 d
6-L semi-continuous NA Methane yield from non-fiber components (raw proteins, raw
stirred tank reactor at lipids, non-fiber carbohydrates) were higher than the fiber (neutral


39 C detergent fiber) components. Also, the digestate residues in all
tested silages can be applied as fertiliers in farmland.
400 L/kg biogas is produced at 40-d hydraulic retention time from a
reactor. 85% cow slurry þ10% olive pomace þ5% apple pulp mixture.
15-L two-stage thermal (55
C) and Thermo-chemical pretreatment enhanced chemical oxygen
thermophilic semi- chemical (pH 10) demand hydrolysis and soluble volatile fatty acid concentrations,
continuous flow hence enhancing biogas production rate from 18.73 L/d to 25.14 L/d.
reactors
50-L thermophilic NA No significant inhibition effects were noted at up to 65.3% food
reactors waste. Methane yields of 281e385 m3/tonne VS can be achieved at
organic loading rate (OLR) of 6.85 kg VS/m3-d and 15.7% total solids
level.
30-L reactor at 41.7
C NA no adverse effects on biogas productivity or methane yields with
<38 mg/kg sulfonamides or < 7 mg/kg tetracyclines, and found that
al antibiotics were partly removed in the anaerobic treatment
NA Reactor could reach steady-state operation at OLR 4 kg COD/m3-
continuous-flow stirred d and HRT of 30 d. Inhibition of methanogenesis occurred when
tank reactor propionic acid was accumulated in the reactor.
20-L continuous NA Direct digestion of vinasse produced no biogas. When
stirred-tank reactors at supplemented with straw amd with lime fertiliser or 3% cow


manure, biogas production of vinasse was largely increased. These
authors also revealed that the AD was the most stable when cow
manure was the co-substrate for digestion.
800 mL-plastic bottles NA effective virus disinfection under mesophilic and thermophilic
at 35
C temperatures.
40-L continuous-flow NA Optimal rice straw/cow manure ratio of 1:1 was noted to yield
mesophilic digester maximum methane yields. At high OLR, the accumulation of volatile
fatty acids inhibited methanogenesis.
40-L continuous-flow NA Optimal rice straw/pig manure ratio of 1:1 was noted to yield
mesophilic digester maximum methane yields. At high OLR, the accumulation of volatile
fatty acids inhibited methanogenesis for the mix.
NA Similar digestion performance over 15e85% cheese whey fraction.
stirred tank reactor at Decrease HRT from 15.6 d to 8.7 d reduced reactor efficiency in a


35 C linear manner. The maximum CH4 yield was 1.37 m3 CH4/m3-d.
500-mL glass bottles at NA Microalgae þ food waste yielded low methane productivity. Adding
raw sludge into the mix significantly increased methane yield.
1-L batch flask at 37
C NA Optimal concentration of H2O2 for treating wheat straw was 3%. A
40:60 ratio of wheat straw and cattle manure maximized methane
yields.
10-L mesophilic NA Adding up to 1.35% glycerin to the digesters increased the biogas
completely mixed production and methane yield. The Methanosaeta (acetoclastic
digesters at 37
C methanogenesis) was noted to dominate in the low glycerin range;
and Methanomicrobium (hydrogenotrophic methanogenesis) was
enriched at high glycerin loadings. Suspension alkalinity, pH, and
biogas production all declined with high glycerin loadings.
NA Adding 10% or 30% of poultry manure to mill wastewater increased
loop reactor methane yields. The methane productivity remained high till OLR
was up to 9.5 kg COD/m3-d.
2-L batch digesters and extrusion The extrusion enhanced hydrolysis and led to increased methane
7-L continuous-flow productivity. For 10% rice straw feed, the increase in yielded energy
reactors at 40
C. was higher than the energy extrusion. No energy benefit when 30%
of rice straw was applied as feedstock.
 Q. Zhang et al. / Renewable Energy 98 (2016) 108e119 111

Table 1 (continued )

Reference Substrates Reactor Pretreatment Remark

Montanes et al. sewage sludge þ sugar beet 250 mL-serum bottles NA The methane productivity was higher at mesophilic than
[52] pulp at mesophilic and thermophilic temperatures.
thermophilic
temperatures
Wang et al. [53] Phragmites australis (a reed), 2.5-L bottles at 36
C NA The clinoptilolite was shown to lead to higher biogas productivity
feces and kitchen waste with enhancement than the use of bentonite or diatomite. The added
clinoptilolite (a zeolite) or other clinoptilolite could enhanced the microbial utilization of Ca2þ/Mg2þ,
natural soils being added as controlled C/N ratio in the feedstock, and improved biogas
adsorbent for C/N ratio production, and metigated ammonia/nitrate inhibition efficiency.
adjustment.
Astals et al. [54] pig manure þ algae 160 mL-glass serum Extracted for Co-digestion of raw algae and pig manure could yield increased
(Scenedesmus sp.). bottles at mesophilic proteins by free methane; however, co-digestion of algae residue and pig manure
temperature nitrous acid or for revealed no synergic effects on methane productivity.
lipids by Soxhlet
extraction.
Marti-Herrero et al. Cow þ llama þ sheep manure psychrophilic 1-m3 NA The biogas productivity for pure llama manure and cow manure
[55] tubular digester. were 0.11e0.14 m3/d and 0.09e0.12 m3/d, respectively. With added
sheep manure, the producity for the llama þ sheep manure was
decreased to 0.065e0.067 m3/d and that for cow þ sheep manure
was increased to 0.17e0.28 m3/d.
Belle et al. [56] forage radish þ dairy manure Mesophilic completely NA Co-digestion increased CH4 productivity than the mono-digestion
mixed, 850-L digesters tests and reduced the H2S concentration in biogas.
Goncalves et al. spent brewery batch tests under NA The biogas productivity was enhanced in the presence of added
[57] grains þ anaerobic mesophilic and glucose or acetate or at thermophilic temperature (50
C). These
biomass þ azo dye Acid Orange thermophilic authors also revealed the color removal together with the digestion
7 temperatures reaction.
Wang and Park [58] Chlorella sp and Micractinium sp Mesophilic 100-mL NA Algae were grown in high nitrogen wastewater. Co-digestion of
and activated sludge stirred bottles algae with waste activated sludimproved volatile solids reduction,
hydrolysis efficiency and biogas yields of algae
Ganesh et al. [59] Cow manure with straw þ fruit NA Single and two-phase digestion were tested.
and vegetable waste

temperature. The feedstocks were hydrolyzed by enzyme mix for
significantly increasing methane yields.
With more than two substrates, the flexibility of feeding strat-
egy could be increased. For instance, Pokoj et al. [36] studied the
semi-continuous AD of two annual silages, four perennial crops
silages, and four mixes of the two. These authors noted from these
tests that the methane yield from non-fiber components (raw
proteins, raw lipids, non-fiber carbohydrates) were higher than the
fiber (neutral detergent fiber) components. Riggio et al. [37] per-
formed anaerobic co-digestion of cow slurry, apple pulp and olive
pomace mixture in 128-L reactor. These authors noted that 400 L/
kg biogas could be produced at 40-d hydraulic retention time from
a 85% cow slurry þ10% olive pomace þ5% apple pulp mix, yielding
63% removal of fed COD.
3.4. Biochemical methane potential
The biochemical methane potential (BMP) tests are a widely
accepted protocol for estimating methane productivity from a
substrate of interest. For instance, Yong et al. [60] measured the
biochemical methane potentials (BMP) of typical food waste (FW)
and straw from northern China in one liter reactor at 35
C. Wahid
et al. [61] compared the MBP of caraway, chicory, red clover and
ribwort plantain using one-cut (in October), two-cut (in July and
October) and four-cut (May, July, August and October) strategies.
Edward et al. [62] proposed the use of inert gas sampling bag for
monitoring biogas productivity for estimating the BMP of macro-
algae feedstock.
One of the main drawbacks of BMP test is the long testing time.
Efforts were made to predict BMP value based on short-term
testing time data. Stromberg et al. [63] proposed the protocol of
predicting methane productivity based on early stage data of BMP
tests so the test duration could be largely reduced. Godin et al. [64]
compared the reliability of near infrared spectrum based models
and of chemical composition based models for predicting BMP of
various plants from a multispecies dataset.
Furthermore, Wang et al. [65] challenged the validity of BMP
tests considering the effects of substrate concentrations. The BMP
of a substrate was noted to increase at a saturating trend with
substrate concentration, which could lead to up to 30% difference
between the tests at low and high concentrations of substrates.
Based on experimental data, these authors proposed that >10 g VS/
L substrate should be applied in BMP tests for avoid un-
derestimations of the methane productivity.
4. Pre-treatment
Lignocellulosic materials are recalcitrant to digestion. Pre-
treatments are often applied for enhance biogas productivity of
substrates so the energy gain can be increased. Physical, chemical
and biological pre-treatments are tested in recent publications.
4.1. Physical pre-treatment
Physical pre-treatments include the involvement of mechanical
disruption and thermal energy disruption. The uses of high shear
mixer (5000 rpm for 10 min) [66], ball-milling grinding [67], and
sandpapers/mesh grating [68] for pre-treating biomass for
enhancing methane productivity were studied. Biogas production
was enhanced after physical treatments.
High temperature could lead to heat transferred from sur-
roundings to substrates so the involved crystalline structure will be
deteriorated. Kratky and Jirout [69] pretreated the wheat straw of
200 mm length using thermal expansion at 170
C and 1.6 MPa for
20 min could yield maximum methane in anaerobic testers. Li and
Jin [70] pre-treated kitchen waste at 55e160
C and tested methane
112 Q. Zhang et al. / Renewable Energy 98 (2016) 108e119
productivity in 5.5-L reactors. Ruffino et al. [66] applied thermal
pretreatment (70e90
C for 1e15 h) on wastewater sludge and
noted that 70
C and 90
C thermal treatments increased methane
productivity by 21% and 31% compared to the untreated control.
Zhang et al. [71] successfully applied AD for converting cephalo-
sporin C residue with hydrothermal pretreatment into biogas. At
high temperature or long treatment time excess hydrolysis
occurred to release soluble substrates, which would yield too fast
acidogenesis to reduce suspension pH so suppressing the biogas
productivity in AD. An optimal hydrolysis temperature for the
maximum production of methane in the subsequent AD tests was
noted [70]. Fu et al. [80] tested thermophilic microaerobic pre-
treatments on corn straw and measured the methane productivity
of the pretreated straw at mesophilic temperatures. The pretreat-
ment improved the methane yield by partial disruption of cellulosic
structures of the corn straw.
Steam explosion adopted mechanical forces produced by sud-
den expansion of steam from high-temperature waters to disrupt
the structure of lignin and other lignocellulosic substrates. Theur-
etzbacher et al. [72] applied steam explosion (140e178
C for
0.5e2 h) on wheat straw and estimated the biogas productivity and
kinetics from the treated straw. Ahring et al. [73] applied oxygen
assisted wet-explosion pretreatment (4 bars oxygen at 170
C for
25 min) on feedlot manure for promoting lignin solubilization and
enhancing biogas productivity during thermophilic AD. All pre-
treatments were claimed to lead to degradation of lignin and in-
crease the subsequent methane productivity during AD.
4.2. Chemical pre-treatment
Acid and alkalines are commonly adopted chemical agents for
pre-treatments [74e78]. Kavitha et al. [79] used added neutral NaCl
to mediate disintegration of waste activated sludge. Organosolv
pretreatment is to contact feedstock with aqueous acetic acid,
ethanol or methanol at 190
C for 60 min for solubilizing lignin and
hemicellulose fractions of the feedstocks [80]. Kabir et al. [81]
pretreated forest residue using organosolv pretreatment for
enhanced methane production.
Ionic liquids are ions in liquid state. Papa et al. [82] tested the
pre-treatment using ([C (2)C (1)Im][OAc] at 100
C for 3 h on corn
stover or switch-grass for bioethanol and methane yields. The ionic
liquid pretreatment led to higher bioethanol and methane yields
(þ18.6% or þ34.5%) than did hot water (þ2.3% or þ23.4%).
4.3. Biological pre-treatment
Storage is needed for biomass handling while biological activ-
ities by unspecified microbal consortium incorporated with
biomass during storage is regarded as a biological pretreatment. For
instance, storage of municipal solids collected in Tyrol, Austria was
noted to enhance methane productivity [83].
Biological consortium could be applied to enhanced hydrolysis
of biomass [84,85]. Wei et al. [86] applied liquid fraction of diges-
tate from anaerobic digester which contained high levels of mi-
croorganisms, ammonia nitrogen and organic substances as the
agent for pre-treatment on cattle manure. The liquid fraction pre-
treatment could yield similar biogas productivity as did the use of
ammonia solution or NaOH solution. Hu et al. [87] also applied the
liquid fraction of digestate as agent to pretreat corn stover for
promoting the efficiencies of biogas productivity. The treated stover
had C/N ratio to decrease from 55.82 to about 30, to degrade con-
tents of lignin, cellulose, and hemicellulose by 8.1e19.4%, and to
increase biogas production by 70.4%.
Use of enzyme as pre-treatment agent is another choice for
enhanced hydrolysis of biomass. Schroyen et al. [88] applied laccase
and peroxidase mix to pretreat seven lignocellulosic substrates
(corn stover, wheat straw, flax, hemp, miscanthus, willow, maize)
and noted the release quantities of total phenolic compounds.
These authors claimed that the released phenolic compounds did
not reach inhibiting values for AD. A linear correlation was noted
between the lignin content and the BMP.
A novel process by pretreated woodchips and digested manure
via Shiitake cultivation was proposed to improve the methane yield
in subsequent solid-state AD stage [89]. The Shiitake mushroom
cultivated produced valuable by-products. The proposed scheme
produced 1.5 times methane than the control tests with untreated
woodchips.
4.4. Combined pre-treatment
Effect of combining steam explosion and biological (enzymatic
saccharification and yeast fermentation) pretreatment on wheat
straw for ethanol production and then the residual for AD was
tested [90]. Reilly et al. [91] pretreated wheat straw using milling,
Ca(OH)2 addition, or enzyme addition, and then tested the methane
productivity from the pretreated biomass. These authors noted that
combined size reduction and Ca(OH)2 pre-treatment could increase
methane potential by 315% after 5 d of AD compared to the control.
Karray et al. [92] pre-treated macroalgae Ulva rigida with ultra-
sound (40 kHz and 120 W), acid (H2SO4 at 100
C), thermos-
alkaline (pH 8e12 and 53 and 105
C) and enzyme (A. niger
filtrate) for enhanced methane productivity at mesophilic tem-
perature. The enzymatic pretreatment was demonstrated as the
best pretreatment for promoting biogas production.
5. AD configurations
Commonly adopted anaerobic digesters include the standard-
rate digesters with segregated liquid layers and high-rate di-
gesters involving mixing, heating and uniform feeding facilities
[93,94]. The feeds for the digesters are often single substrate.
Recent research focuses are novel digester geometry, solid-state
AD, psychrophilic AD, and integrated AD systems.
5.1. Novel digesters
Anaerobic digesters with series chambers were proposed to
provide sufficient buffering capacity and diversed environment for
different microbial populations so AD reactions could be stably
operated [95]. Using a similar protocol, Ahamed et al. [96] studied
the use of four-chambered reactor, a multi-phased anaerobic
baffled reactor, for AD treatment of food waste at mesophilic
temperatures and hydraulic retention time (HRT) 30 d. The multi-
phased digester allowed the growth of different microbic groups
in different chambers. Khemkhao et al. [97] proposed a revised
continuous-flow stirred tank anaerobic digester with deflector to
capture palm fiber from palm oil mill effluent. The proposed
digester could degrade cellulose, hemicellulose and lignin and
produce biogas by the associated methanogens. Ruffino et al. [98]
evaluated the possible saling effects on deteriorated digesters
performances in large digesters.
Membrane bioreactors are device that can separate solid
retention time from hydraulic retention time in operation. Gouveia
et al. [99] tested a pilot-scale anaerobic ultrafiltration membrane
bioreactor for municipal wastewater treatment at 18
C for three
years. This membrane bioreactor could produce oversaturated so-
lution with methane at 1.6e2.0 kg COD/m3-d organic loading rate
and 12.8e14.2 h hydraulic retention time.
Another novel design is to feed H2 and CO2 into thermophilic
hollow-fiber membrane methanogenic bioreactor to produce
 Q. Zhang et al. / Renewable Energy 98 (2016) 108e119
methane. With 0.93 m2 PVDF membrane module, the tested reactor
converted 95% of H2 and CO2 to CH4, confirming that gas sparging
through a membrane module could efficiently transfer H2 from gas
phase to liquid phase and convert H2 and CO2 to methane in pilot
scale [100].
5.2. Solid-state AD
Solid-state (dry) digestion processes are with >15% solid con-
tent, with solid substrate being placed in hermetic reactors and the
digestate being circulate for flowing through the substrates for
digestion. Apparently the bed permeability, bulk density, and vol-
atile solid contents over the AD bed would not be homogeneous
and would evolve during the digestion process particularly for
large-scale reactor [101]. Also, the bed temperature, substrate
concentration, C/N ratio, and substrate premixing methods affect
the methane productivity from solid-state AD [102,103]. Recent
studies revealed that even the bedding materials could affect the
methane productivity from solid-state AD [104].
Air exposure may be inevitable in large-scale solid-state AD
applications. The tests on switchgrass subjected to limited air
exposure at mesophilic and thermophilic temperatures revealed no
significant effects on biogas production [105].
Vasco-Correa et al. [106] discussed the use of fungal (Ceripor-
iopsis subvermispora) pre-treatments to reduce lignin contents of
Miscanthus sinensis and then conducted solid-state AD tests on the
pretreated biomass. The methane productivity from digester bed
was increased.
5.3. Psychrophilic AD
There is a need to apply AD in cold regimes. The psychrophilic
AD (20
C) on co-digestion of cow feces and wheat straw was
successfully achieved in 40-L sequential batch reactors at 21-d cy-
cles [107]. High rate psychrophilic at 20
C AD of undiluted cow
feces of 11.5e13.5% total solids was tested in a similar reactor to
produce 116e154 L CH4/kg VS at organic loading rate (OLR) of
9e12 g/kg-d [108]. At psychrophilic temperatures, the hydrolysis
was claimed as the rate limiting reaction.
Gouveia et al. [109] tested pilot-scale anaerobic membrane
bioreactor with upflow anaerobic sludge blanket reactor (discussed
in Section 4.4) with an external ultrafiltration membrane on
treatment of municipal wastewaters at 18
C. At psychrophilic
temperature, the tested reactor could remove 87% COD for gener-
ating 0.18e0.23 m3 CH4/kg COD removed at HRT of 7 h and OLR of
2e2.5 kg/m3-d. These authors also noted that membrane fouling
could be argely mitigated with intermittent backwash.
5.4. Integration systems
The AD þ X configuration was applied for producing multiple
products or refine product quality during AD treatments. For
instance, biohydrogen and methane was studied to be produced in
sequential reactors [110e112].
Ansari et al. [113] applied forward osmosis (FO) before AD for
concentrating municipal wastewater to make it suitable for
anaerobic treatment. The chemical oxygen demand (COD) in
municipal wastewaters is generally low. With the water being
removed by FO the COD in influent to AD unit could be increased so
the reactor performance could be enhanced.
The integrated system of particular interest is the heat inte-
grated AD systems by use of air source heat pump for transferring
the solar energy collected in a greenhouse for heating up an
anaerobic digestor installed beside the house [114]. These authors
demonstrated that the tested heat pump could provide 8e10 kW
113
heat during daylight period to the digester when the surroundings
was below freezing. Another example is the recovery of waste heat
(17,000e18000 kJ/kg organic waste treated) in the exhaust gas from
AD unit. Another interesting integrated system is to apply an
organic Rankine cycle to recover the waste energy in exhaust gas at
about 340 K [115]. For processing 25,000 tonnes/yr of organic
waste, the Rankine cycle can generate 18 kW power, giving 2% in-
crease in overall energy efficiency. Zhong et al. [116] proposed an
integrated lignocellulosic biofuel production network with food
waste, animal manure and corn stover as feedstocks while the
former two were anaerobically digested to form methane and
residue. The yielded residue was pretreated with acid, alkali and
enzyme with another feedstock, corn stover, to produce hydroly-
sate for further fungal fermentation. Allesina et al. [117] studied an
integrated AD þ gasifier þ internal combustion engine system to
provide an increase energy yields than the conventional AD
process.
Ahern et al. [118] examined the use of power to gas (P2G)
concept to biological methane production with an island energy
system as the study field. The proposed scheme is to use electricity
to electrolyze water into hydrogen gas, and then the formed
hydrogen is fed into the anaerobic digestor for methanation. The
CO2 is yielded during AD reaction so can be used in situ inside the
reactor. This configuration also benefits the carbon capture after AD
unit. These authors proposed the economic analysis on the use of
this proposed biogas system.
6. Operations
Various aspects of operations of anaerobic digesters are still the
focus of research. Biogas to be used as a renewable energy source
counts on stable and consistent operational performance of di-
gesters at as high as possible performances.
6.1. Performance enhancement
To enhance performance of AD operation, various strategies
were proposed. For instance, headspace flushing with 80% N2þ20%
CO2 was applied to increase CH4 productivity, since the removal of
O2 could prevent oxygen stress on methanogenesis and the
increased CO2 solubilization could enhance methane production
[119]. Recycling the effluent from AD unit was applied to neutralize
acidity of substrate residue to enhanced methane production [120].
Regular addition of cellulolytic organisms into the digesters was
also tested for enhancing AD performance [121]. Substrate feeding
frequency also can be a parameter to manipulate AD performances
[122].
Study revealed that the feed composition can be adopted for
controlling microbial community in the digester, hence influencing
biogas productivity. Walter et al. [123] conducted co-digestion
solid-state AD tests of cattle slurry and druit at mesophilic and
thermophilic temperature, and noted that acetoclastic metha-
nogens were enriched in the presence of fruit bunches, while
hydrogenotrophic genera were enriched with the cattle slurry
substrate.
An interesting article by Abdelsalam et al. [124] revealed the
enhancement of biogas production and reduction of lag phase of
anaerobic digestion by adding nanoparticles. These authors noted
that by adding 1e20 mg/L Co, Ni, Fe or Fe3O4 nanoparticles the
biogas yields could be enhanced by 1.5e1.8 times. These authors
proposed a few possible mechanisms on how NPs affect the
methogenesis process in biogas production.
114 Q. Zhang et al. / Renewable Energy 98 (2016) 108e119
6.2. Inhibition mitigation
Numerous compounds (such as ammonia [126], sulfide [132], H2
[125], VFAs [134]) or process factors (like temperature, pH) could
inhibit methanogenesis in anaerobic digesters. Methods to mitigate
inhibitory effects from AD reactions were proposed.
When handling nitrogen-rich substrate, the protein and uric
acid are decomposed to ammonia during fermentation process.
Excess ammonia could inhibit methanogenesis [126,127]. Gas
stripping was applied to reduce ammonia concentrations in liquid
for increasing methane productivity [128,129]. Some authors
adopted step-wise increase in ammonia concentration to acclimate
the functional strains in the digester for handling protein-rich
substances without severe inhibition [130]. Belostotskiy et al.
[131] studied the use of phosphoric acid to shift the microbial
community so can increase the biogas productivity when con-
ducting AD reactions of chicken wastes.
Sulfur-containing compounds could be yielded in the sus-
pended liquor during AD of biomass, which could be converted to
sulfide under anaerobic environment. Ferric chloride was often
adopted for removing H2S in the digester [132]. Aeration with ox-
ygen from pressure swing adsorption generator was applied for
oxidizing sulfide in the digestate [133].
Excess VFAs can be produced from easily hydrolyzed substrates
such as food waste that would inhibit methanogenesis by lowering
pH. Ferric chloride was added to digester for forming iron salt
precipitation or enriching functional strains to mitigate VFA inhi-
bition [132]. Propionate inhibition could occur in certain AD system
when acetogens are relatively weak in activity. Li et al. [134] applied
sulfate to mitigate propionate inhibition effects. Bozym et al. [135]
measured the concentrations of Pb, Cd, Cu, Zn, Cr, Ni, Na, K, Mg and
Ca in brewer's spent grain, apple pomace and strawberry pomace,
rapeseed cake from oil industry, potato peels and pulp, and walnut
and hazelnut sheels from confectionery and fat industries. These
authors noted that the detected concentrations were all well below
the levels that can affect biogs productivity in anaerobic digester.
6.3. Operational stability
The capability of anaerobic digester to keep operation stable
subjected to environmental changes is of essential importance for
practical use of AD for biogas production from waste. At sudden
temperature change, the microbial community would shift to adapt
to the change with the reactor performance being evolve accord-
ingly [136]. At thermophilic temperature, hydrogenotrophic
methanogens were enriched and levels of Fe-hydrogenases and
abundance of hydrogen producer bacteria were increased. At sud-
den change in feed composition, microbial community would also
shift accordingly [137]. Specially, when excess carbohydrates were
fed, the community diversity was increased with dominating
strains being lactobacilli. When fed with protein, only Desulfoto-
maculum revealed significant increase. These authors confirmed
that operational stability correlated closely with the microbial
communities in anaerobic digesters.
Moeller et al. [138] studied the foam formation in sugar beet-fed
digestates. These authors noted that the increased disintegration of
sugar beet led to excess forming but produced no effects on biogas
productivity. Both pectin and sucrose had no forming effects; both
sucrose and calcium chloride had a promoting effect on foaming;
while ammonium chloride and urea had a lessening effect on
foaming.
6.4. Biogas upgrading
Biogas from AD unit contains 55e70% methane and 30e45%
CO2. To apply biogas to applications that needs high CH4 concen-
trations, such as vehicle fuels or as alternative natural gas feed, CO2
and other impurities need removal by upgrading process. The
bottom ash from the incineration of municipal solid waste was
applied to adsorb CO2 and H2S from a biogas stream [139]. The used
ash was also stabilized by its incorporated heavy metals being
immobilized with adsorbed sulfide. Chaiprapat et al. [140] studied
the use of triple stage and single stage biotrickling filters for
desulfurization of biogas. High empty bed retention time would
increase H2S removal and sulfuric acid recovery; conversely, an
optimal fluid velocity existed for H2S removal. Lemmer et al. [141]
studied the high-pressure AD on maize silage and a mixture of
grass and maize silage to upgrade produced biogas. These authors
produced biogas of 77% content at working pressure of 9 bars. The
high ammonia concentrations lead to higher pH-values in the
digester.
Morero et al. [142] conducted a case study analysis on biogas
upgrading based on environmental impact assessment (EIA) and on
life cycle assessment (LCA) with water, physical solvent or amine as
the solvent. The LCA results revealed that the process with amines
has the concern on its high energy use. The EIA considered that the
project is feasible based on cultural and socioeconomic compo-
nents. Water was the solvent giving the lowest payback period.
These authors showed that, for Argentina, biogas upgrading should
be used as energy source for its contribution to the grid.
Meier et al. [143] proposed an interesting trial to apply micro-
algae photosynthesis to remove CO2 from biogas. These authors
noted that one cannot directly contact biogas and microgalal sus-
pension owing to O2 desorption to the gas phase. A photoreactor
and a gas/liquid transfer unit was proposed to remove CO2 in
biogas.
6.5. Monitoring
Accurate, low-cost, reliable on-line monitoring tools are
required for AD processes for implementing improved operation
and control. Tsapekos et al. [68] proposed the use of electrical
conductivity test for predicting the biogas productivity from
meadow grass. Adam et al. [144] applied an electronic nose for on-
line monitoring of anaerobic reactor state in pilot-scale and full-
scale levels and compared its response to the indices of pH, alka-
linity, VFA concentrations. These authors noted that e-nose
response could be classified into steady-state, transient and
collapsing states. Wahid et al. [61] proposed the use of near infrared
spectroscopy for revealing the methane production potential based
on cellulose, hemicellulose, acid detergent fiber, neutral detergent
fiber and crude proteins contents.
7. System analysis
Li et al. [145] presents a mass and energy balance calculation
and an economic analysis for a full-scale rice-wine-pig biogas
production plant in a winery. This case study revealed that 93.7% of
mass was applied for rice fields and the surplus energy gain was
about 823 MJ/yr. Economic analysis demonstrated a return period
of 10.9 yr. Balaman and Selim [146] proposed a decision model for
AD to electricity and fermentiers based on fuzzy multi objective
decision making to optimize economic objectives under inherent
uncertainties and variation and fluctuations of model parameters.
Castellanos et al. [147] conducted optimization and techno-
economic analysis of an off-grid integrated electricity system for
West Bengal, India, considering the biogas combined heat and
power and photovoltaics and storage elements. Hahn et al. [148]
discussed the use of demand-oriented based biogas supply for
adaptive power generation. The demand oriented supply reduced
 Q. Zhang et al. / Renewable Energy 98 (2016) 108e119
the need of biogas storage capacity compared with continuous
supply system.
Coelho et al. [149] studied the 4MWe central receiver systems
with biogas from an anaerobic digester using sludge from a
wastewater treatment plant. These authors claimed that the lev-
elized cost of electricity for the hybrid CRS/anaerobic digester po-
wer plant is 0.15 Euro/kWh, giving investment return for 13 yr.
Bacenetti et al. [150] estimated the impacts of long-distance
transport for three maize silages at different energy density at
increasing transport distance. At <5 km, the whole plant silage
reveals the lowest impact. As distance was increased, silages with
higher energy density become more environmentally sustainable.
The transport by trucks achieves better environmental perfor-
mances compared with by trailer and tractors especially >25 km.
Bacenetti et al. [151] proposed an analysis on effects of maize silage
energy density at increasing transport distance on AD economy,
Fantin et al. [152] provided a life cycle assessment on the envi-
ronmental sustainability of an AD plant considering the crop
cultivation to biogas production and subsequent combined heat
and power unit. Interesting results on the proposed ways of miti-
gating environmental impact by the studied AD plant were
discussed.
8. Research focus and way forwards
The above-mentioned paper summary provides a very wide
spectrum for the research topics, though all are regarding biogas
from anaerobic digestion processes. The sampled papers collected
in the present study show the following sequence in subject level
(Table A1): Substrates (35.0%) > Pretreatments (18.9%) > Operation
(16.8%) >AD configuration (15.4%) > system analysis (5.6%) > status
report (2.8%). In sub-subject level, the sequence is: Co-digested
substrates (21.0%) > algal biomass (9.1%) > inhibition mitigation
(7.7%) > physical pretreatments ¼ chemical pretreatments (6.3%).
The research focuses are therefore identified as to apply AD for
mixed substrates and for algal biomass, ways of mitigating inhibi-
tion caused by metabolites generated, and use of physical and
chemical pretreatments for accelerating hydrolysis (Fig. 1).
The research interests on co-digested substrates are from the
need to provide high flexibility on feeding compositions so the AD
Fig. 1. Research topics covered by the sampled publications.
115
reactions can be undergoing within the appropriate operational
window, considering the C/N ratio, buffering capability, suspension
pH and potential to enhance hydrolysis of hard-to-degraded sub-
strate. Up to now, the research on co-digested substrates is still
lacking systematic summary. Further studies such as done in
Ref. [36] to conclude the correlations between biogas productivities
from non-fiber components and fiber components are needed.
Algal cells, particularly microalgae cells, could grow much faster
than higher plants hence having attracted great research interests
on their use as carbon sink for alternative fuels. However, since the
algal cell walls are relatively thick, their hydrolysis needs intensive
energy input [153,154]. The sampled papers concluded that direct
AD of microalgae is not recommended. However, applying pre-
treatments to enhance hydrolysis reaction would increase the
operational costs. Effective co-digestion and/or cost-effective pre-
treatments are needed to be developed for promising algal biogas
industries.
On pre-treatment studies, most widely adopted processes such
as adding acid/alkaline, ultrasonication, milling etc can improve
biogas productivity from recalcitrant biomass. Use of expensive
chemical agent is not encouraging. However, the simple storage as a
biomass pre-treatment [84] and the use of pre-treatment stage for
producing valuable products [90] are developments of great prac-
tical interests. Novel pre-treatment configurations are desired.
Organosolv pretreatment or ionic liquid pre-treatment are efficient
for substrate hydrolysis and are the focus of pretreatment re-
searches. Large-scale demonstration with comprehensive eco-
nomic feasibility study should be done in future works.
The proposed novel reactors are focused on the self-regulatory
capability for functional strains enrichment and buffering capac-
ity to enhance operational stability. On the other hand, clear
research focus is on the integrated system including the use of
membrane for separating SRT and HRT for AD reactions under
harsh environments. Also, the developments in solid-state diges-
tion processes and psychrophilic AD are of great practical interests
[102,107]. The proposal of using heavy metal nanoparticles on
biogas productivity enhancement [125] is of great practical in-
terests, with its detailed mechanisms remaining unexplored.
Efforts are focused on mitigation of inhibition by ammonia,
sulfide, H2, VFAs on methanogenesis in anaerobic digesters.
116 Q. Zhang et al. / Renewable Energy 98 (2016) 108e119

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