Acta Ecologica Sinica xxx (xxxx) xxx

Contents lists available at ScienceDirect

Acta Ecologica Sinica

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

Methods for the removal and recovery of nitrogen and phosphorus nutrients
from animal waste: A critical review
Muhammad Sajjad a, Qing Huang a, *, Sardar Khan b, Javed Nawab c, Muhammad Amjad Khan a, b,
Abid Ali d, Rahman Ullah e, Aftab Ali Kubar a, Genmao Guo a, Muhammad Yaseen a,
Maryam Sajjad b
a
Key Laboratory of Agro-Forestry Environmental Processes and Ecological Regulation of Hainan Province, Center for Eco-Environmental Restoration Engineering of
Hainan Province, School of Ecology & Environment, State Key Laboratory of Marine Resource Utilization in South China Sea, Key Laboratory for Environmental
Toxicology of Haikou, Centre for Terrestrial Biodiversity of the South China Sea, Hainan University, Haikou, Hainan 570228, China
b
Department of Environmental Sciences, University of Peshawar, Peshawar, Pakistan
c
Department of Environmental Sciences, Kohat University of Science and Technology, Pakistan
d
Department of Zoology, Abdul Wali Khan University, Mardan, Pakistan
e
Department of Biochemistry, Abdul Wali Khan University, Mardan, Pakistan

A R T I C L E I N F O A B S T R A C T

Keywords: Livestock and poultry industries are developing rapidly worldwide, responsible for releasing large volumes of
Phosphate manure and liquid waste. The produced manure containing nitrogen (N) and phosphorus (P) nutrients which are
Ammonia causing eutrophication and algal blooms if released into water bodies without prior treatment. Utilization of bio-
Biogas slurry
waste materials for the production of biogas is one of the most useful technologies providing a pollution free
Recovery
environment and a renewable “green” energy. Physical and chemical methods for removal of N and P from
Biochar
Struvite animal waste include the application of biochar with different chemical and physical modifications (adsorption),
air–cathode single chamber microbial fuel cells (MFCs), an aerobic digested (AD) technique, using ultrasound/
H2O2 digestion joined with HFO/biochar adsorption technique, wet scrubber and stripping process, and gas-
permeable membrane technology, critically discussed in the manuscript. Future research requirements include
integrated approaches and directions regarding the recovery of N and P utilizing organic amendments (like
biochar) are discussed.

1. Introduction
Fast and un-controlled urbanization has led to large volumes of waste
production from various sectors globally. The massive quantities of dung
and associated other wastes generated by various animal husbandries
contain minerals like nitrogen (N) and phosphorus (P) that causes un­
expected ecological problems like eutrophication in water bodies
[59,153]. Poultry breeding and animal husbandry are emerging quickly
on global scale [172], especially in China. >100 million hoggeries are
producing large quantities of manure which is a huge environmental
issue [87]. Presently in China, the whole livestock businesses don’t have
satisfactory manure treatment services in addition to weak pollution law
enforcement [43,171]. The manure produced is treated by anaerobic
digestion (AD) and aerobic composting [182,195]. According to a
census of China’s pollution sources (conducted in 2010), the total
nitrogen (TN), phosphorus (P) and chemical oxygen demand (COD),
from the animal husbandry business accounted for 38%, 56% and 96%,
respectively of the total contaminants generated from agricultural areas.
The amount of COD, TN, and P were 2.3 times higher than the levels
released from industrial sources. This is due to the extremely high
concentrations of these pollutants released from commercial piggery
farming areas in different provinces such as Guangdong, Henan,
Sichuan, Shandong and Zhejiang [18,21]. According to the China Sta­
tistical Year Book, 2016, >450 million pigs are produced [117], annu­
ally. Swine wastewater contains a large amount of both ammonia and
phosphate minerals [139], arising a public concern globally [93]. In the
United States (US), production of animals has become greater than
doubled since the 1950s, but the total of waste treatment facility pro­
cesses has reduced by 80% [153,196].
Animal manure contains high concentration of nutrients such as P

* Corresponding author.
E-mail address: huangqing@hainanu.edu.cn (Q. Huang).

https://doi.org/10.1016/j.chnaes.2023.05.003
Received 12 October 2022; Received in revised form 11 May 2023; Accepted 14 May 2023
1872-2032/© 2023 Ecological Society of China. Published by Elsevier B.V. All rights reserved.

Please cite this article as: Muhammad Sajjad et al., Acta Ecologica Sinica, https://doi.org/10.1016/j.chnaes.2023.05.003
M. Sajjad et al.
and N, which creating major ecological problems [153]. Their release
from slurries into water bodies causes problems such as eutrophication
(the over-enrichment of nutrients in aquatic bodies) and algal blooms.
This destroys fish and other aquatic fauna and has negative effects for
humans by reducing available clean water and aquatic foods [118].
Generally, animal manure contains essential macronutrients (like N, P
and K) needed for crop production and is therefore, often applied as
fertiliser. The increase in use of animal manure in agricultural farmlands
and the livestock husbandry itself has direct impacts on the environ­
ment. Large numbers of swine production units with inadequate areas
for the recycling of slurry nutrients can cause leftover plant nutrients on
farms [91,129]. Further, the cost and energy consumption required for
transporting animal slurry to arable farmland is relatively high
[115,140]. Therefore, all the excreta and contaminated water is not used
as fertiliser.
There are diverse array of livestock waste disposal and treatment
approaches that are applied to minimize the environmental impacts of
swine excrete. These approaches include anaerobic digestion (AD)
[153], thermochemical conversion (TCC) technologies [14], two stages
reverse osmosis (RO), solid-liquid separation [49], biogas-production,
aerated lagoons, composting, and anoxic lagoons [1,26,82]. The ap­
proaches got additional attention because of their useful role in odour
control, enhanced manure handling, weed seed destruction, minerali­
zation of organic nitrogen, nutrient recovery, reduction in flies and
pathogen, and most importantly, energy profit [8,64,154,181,185].
Biogas slurry is the waste produced from intensive livestock farming in
both semi-urban and rural environments. Slurry contains potentially
toxic elements (PTEs) and long-term application of the slurry into soil
leads to addition of these toxic elements in the soil. These elements are
taken by the roots, translocate to other parts of the plants and ultimately
become part plants as well as the food which we obtain from plants [10].
Traditionally, pig slurries are stored on the farms for large periods, and
then applied to agricultural fields as fertiliser [109]. However, during
storage this waste material emits considerable amount of gas to the at­
mosphere, resulting environment and animal health consequences
[3,34].
The purpose of this review is to critically evaluate previous biogas
production research. Various methodologies for nitrogen (N) and
phosphorus (P) recovery are discussed, their merits and limitations are
evaluated and recommended technologies for the future are discussed.
This review article will assist researchers in the future in investigating
and exploring this research area.
2. Biogas production
The conversion of biowaste into biogas is one of the most useful
technologies used to obtain “Green” energy and a pollution free envi­
ronment [28]. Recently, many biogas projects aimed to treat animal
waste and convert it into value added products such as biogas [197].
Anaerobic digestion (AD) is used for the treatment of livestock waste or
manure. Biogas fermentation, also known asbiogas technology or AD
found to be an efficient waste management substitute because it pro­
duces renewable energy (methane), concurrently eliminating organic
contaminants. Anaerobic treatment is more beneficial than aerobic
treatment [182]. AD has achieved attention in the form of technology
that can offer keys in numerous divisions such as nutrient recycling,
sustainable agriculture, waste management, renewable energy [52]. AD
provides pollution free energy (biogas) which can be utilized for power
generation by combining very low input energy with high efficiency
[119]. Additionally, the digestate is full of nutrients that can be utilized
as fertiliser [198]. According to Duan et al. [33], approximately >90%
of the biogas plants are constructed for dung management in China.
Sometimes in biogas production by anaerobic fermentation, the poultry
and livestock manure is mixed with straw, pear (residue and leaves) and
distiller’s grains [183,184]. This mixing is performed in order to
improve the process yield, and is known as co-digestion. Biogas is the
2
Acta Ecologica Sinica xxx (xxxx) xxx
most important source of renewable energy, while the nutrient-rich
digestion sludge can be utilized as organic fertiliser [137]. Biogas is
an inflammable gas of high economic value that is extensively used for
heating, lighting and power generation [135]. Production of biogas from
agricultural waste can cause a significant reduction in fossil-fuel con­
sumption; reducing global warming by 50% [164].
China has a protracted past of exploiting biogas as source of energy.
It is broadly recognized that production of biogas by utilizing agricul­
tural residues plays a significant part in the supply of energy, environ­
mental safety and is encouraged as environmental friendly agricultural
practice in rural regions. Being the leading developing country in the
world, the economy of China is highly dependent on the agriculture
sector. This results in approximately 809 million tons of crop straw and
1629 million tons of animal manure collected annually as a biomass
resource, with a biogas potential of 33.5 × 1010 m3 [160,161]. As
mentioned previously, the study of biogas fermentation commenced
very early in China, but its application has been slow as the technology
continues to evolve [17,53]. Therefore, it is vitally important to un­
dertake relevant research in this area to improve this technology to
ensure the high production of energy and nutrient recovery.
The production of biogas has advantages in lowering energy cost of
farm energy by utilizing directly gas and/or by electricity production.
During biogas production, the solid form by-product (digestate) is usu­
ally used in green house cultivation as an organic substrate or organic
fertiliser [24,25,116]. However, during the AD process, incomplete
nitrification happens where the digestate contains a high concentration
of NH+ 4 -N in addition to the residual biochemical oxygen demand (BOD),
chemical oxygen demand (COD) and P compounds. Any untreated
digestate released into waste streams may become growing areas for
different pathogens like bacteria and fungi. Therefore, the disposal of
residual slurry remains a challenge. The economic cost of slurry man­
agement and transportation is often expensive and depends on the
digester capacity to the animal stocking density. Therefore, many
farmers release the generated waste deprived of any secondary treat­
ment into close water bodies resulting in water pollution.
Biogas can produce electricity or used for both heat and power (CHP)
separately. Once a system has biogas upgrading, CH4 and the natural gas
in the biogas can be focussed to the same values. It can be supplied using
a pipeline system for domestic use. In cryogenic circumstances, the
biogas is transformed into compressed biogas (also called liquid biogas).
This technology can be applied to promote biogas, by lowering the gas
temperature to − 80 ◦ C. Cryogenic technology generally relates to the
production of liquid biogas. The gas temperature can be lowered further
to − 162 ◦ C [71]. In addition, the biogas may be utilized as fuel for
transportation and in several countries, there are filling fuel stations
with 100% CH4 or CH4 mixed with natural gas and used as car fuel [67].
A simple diagrammatic sketch of biogas production is provided in Fig. 1.
Typical characteristics of animal manure are reported in Table 1.
3. Biogas slurry
The liquid portion containing approximately 90% of the total
digestion effluent is called biogas slurry (BGS). BGS is the liquid con­
taining organic waste from air tight anaerobic digestion process, at a
certain temperature and moisture content, containing methanogenic
bacteria produces products of fermentation after the methane and car­
bon dioxide generation [54,55]. General chemical characteristics of BGS
are provided in the Table 2. BGS is obtained mainly from biogas plants
after the gas has been tapped for energy using AD of the animal manure,
which contains an enormously high amount of NH3 and COD [22]. AD of
organic waste is a useful waste treatment method and the best way for
additional resource utilization. The BGS is generally loaded in N, P, K
and some other readily available nutrients [153,166], and can be uti­
lized as an excellent fertiliser in the liquid form at agricultural fields
[180]. Current studies reported that BGS is an eco-friendly amendment
to soil which provides nutrients, especially organic carbon to the soil as
M. Sajjad et al. Acta Ecologica Sinica xxx (xxxx) xxx

Fig. 1. A simple diagrammatic sketch of biogas production (Modified from [127]).

Table 1
Chemical characteristics of manure produced from different sources.
S⋅No Source pH TS (mg VS (mg TKN (mgN Alkalinity (CaCO3 mg P (mg NH+ 4 (mgN COD(mg References
L− 1) L− 1) L− 1) L− 1) L− 1 ) L− 1) L− 1)

1 Swine 7.5 1400 7500 2700 13,350 140 2390 16,780 Garcia− Gonzalez et al.
[45]
2 Swine 8.71 8500 1500 2459 11,337 NA 2097 1695 Dube et al. [188]
3 Live 9.05 2810 1780 63 NA NA NA NA Provolo et al. [126]
stock
4 Swine 7.23 NA NA NA NA 670 NA 60,000 Ichihashi and Hirooka
[66]
5 Swine 16,000 10,000 NA NA NA 200 NA 30,000 Baret et al. [2]
6 Dairy 7.4 81,000 67,000 NA NA 600 NA 13,000 Baret et al. [2]
7 Chicken 7.73 NA NA 53,000 NA NA 100 NA Huang et al. [62]
8 Swine 7.2 7000- NA NA NA 1100 NA 18,000- Wu et al. [165]
35,000 58,000
9 Cattle NA 91,000 73,000 3900 NA NA 1700 111,000 El-Mashad et al. [189]
10 Swine 8.3 NA NA NA 11,400 446 2300 NA Vanotti et al. [152]
11 Swine 7.8 NA NA 426 3135 103 NA 4105 Huang et al. [62]

well as crops for long time [128,166]. Prior studies indicated that the
application of BGS along with man-made fertiliser encouraged crops
production [48,80]. Hence, application of BGS in paddy soil is possible
alternative to man-made fertiliser [170]. This not only reduces the
environmental pollution, but also provides a useful source of biogas,
which is a clean energy free of pollution [120]. However, application of
nitrogen rich BGS to soil may cause increase in NH3 volatilization [199].
BGS, which is a liquid by-product of biogas, full of nutrient to be treated
before application in order to prevent environmental problems such as
eutrophication after of nutrition leaching [86].
However, the main issue concerned is the BGS is not fully consumed
by traditional land use. The transportation of slurry for long distances is
not practically feasible, and its utilization is limited because of having
low value-added properties [6,155,162]. Moreover, the improper
dumping of BGS can produce several environmental problems like
eutrophication [183,184]. The BGS has high amounts of ammonia N
(NH3-N, 500–3000 mg L− 1) and unusually a low C/N ratio resulting from
carbon utilization through anaerobic fermentation [143]. Besides, too
much BGS irrigation may be responsible for the harmful effects on the
growth of crops, causing serious environmental issues to air, soil and
water, and also harming the human health [125,179].
According to Mehmood et al. [103] and Trippathi et al. [146], about
14 billion tons of biomass generated annually on global scale. The
biomass is allowed to natural decomposition or treated via combustion
without proper treatment, creating air and water pollution. For example,
there are >56,856 different sized biogas plants currently operating in
China with the generation capacity of 3.9 billion tons of biogas from
slurry, creating high risks of water eutrophication and human health
[68]. Transporting raw BGS is not feasible because the slurry contains
>90% water [83]. Therefore, onsite recovery of nutrients is necessary to
viably utilize N and P. Various nutrients (N and P) recovery techniques
applied from biogas digestate, given in the Table 3.

3
M. Sajjad et al. Acta Ecologica Sinica xxx (xxxx) xxx

Table 2
Chemical characteristics of typical biogas slurry from different sources.
S⋅No pH TN mg NH+ 4 mg TP mg TS mg COD mg VFA(mg EC mS cm Turbidity Source Reference
L− 1 L− 1 L− 1 L− 1 L− 1 L− 1 ) − 3
(NTU)

1 8.04 6400 4500 510 40,700 28.8 NA 23,500 NA NA Lenz et al.

[85]
2 7.05 284.84 264.17 25.58 1759 0.908 NA 3510 NA Poultry farm, Beijing, China Yang et al.
[172]
3 7.8 25 00 NA 60 6387 7.451 NA 16,600 NA Biogas digestion plant, Hubei He et al.
Province, China [56,57]
4 8 NA 1390 15 15 4.5 NA 104,000 NA Biogas plant for piggery manure, Kizito et al.
Dong Hua Shan, Village, Beijing, [75]
China
5 7.87 NA NA 37.74 4387 2911.98 0.01 16.61 976.96 NA He et al.
[56,57]
6 6.78 289.78 NA 29.82 NA 1521.75 NA NA NA NA Cao et al.
[13]
7 7.93 NA NA NA 5589 2725.47 0.011 25.51 347.17 Biogas digestion plant, Hubei He et al.
Province, China [54,55]
8 7.96 NA NA NA 4844.35 1620.1 0.011 15.51 1011.4 Biogas digestion plant, Yingcheng He et al.
City, Hubei province, PR China [54,55]
9 8.1 1811.1 317 8.2 NA 677.1 NA 3735.7 257.8 NA Han et al.
[190]
10 7.5 NA 234 42 NA 960 NA NA NA Xiasha Swine Farm, Hangzhou, Perera et al.
Zhejiang Province, China [123]
11 7.95 984 NA 11.06 NA 1464 NA 7327 NA Biogas producing company in Ruan et al.
Zhejiang, China [132]

Table 3
Nutrients recovery technologies of biogas digestate [191].
Technology Classification Subject Category Products Requirements References

Direct spreading _ Whole digestate Fertiliser Enough croplands to be spread on [27]

processing
Hydrothermal Thermal conversion Whole digestate Crude oil and hydrochar High initial TS content >20% [149]
liquefaction processing
Thickening and Physical technology Solid-liquid separation Liquid and solid fractions Post treatments for both fractions ([36]; [42])
dewatering are required
Vacuum evaporation Thermo-physical Liquid fraction Pure water, Ammonium Pre-treatment of separation and [20]
technology processing salts, and concentrate post-handling of concentrate are
required
Membrane filtration Physical technology Liquid fraction Pure water and liquid Effective pre-treatment of Fuchs et al.
processing concentrate separation and post-handling of [42]
concentrate are required
Ions Exchange Physic-chemical Liquid fraction Treated wastewater and Effective pre-treatment of separation [4]
technology processing nitrogen and phosphorus and post sorbents washing are
concentrate required
Ammonia stripping physic-chemical Liquid fraction Ammonium salts and low Pre-treatment of separation and [4]
technology processing nitrogen liquid digestate post-treatment of liquid digestate are required
Chemical Chemical technology Liquid fraction Struvite or calcium Pre-treatment of separation and [151]
phosphorus processing phosphate and low post-handling of liquid digestate
precipitation phosphorus liquid are required
digestate
Microalgae Biological technology Liquid fraction Microbial biomass and Pre-treatment of separation and [167]
cultivation processing treated liquid digestate post-handling of liquid digestate
are required. Liquid digestate
dilution is usually required
Composting Biological technology Solid fraction Soil amender or fertiliser Pre-treatment of separation is required ([144]; [38])
processing
Pelletizing Physical conversion Solid fraction Solid fuel Pre-treatment of separation and solid drying are [78]
processing required
Pyrolysis and Thermal conversion Solid fraction Crude oil, syngas, or Pre-treatment of separation and solid drying are [122]
gasification processing biochar required
Incineration Thermal conversion Solid fraction Energy and P-rich ash Pre-treatment of separation and solid drying are [122]
processing required

4. Nitrogen and phosphorus nutrients richness in animal waste
4.1. Nitrogen in animal waste
When ammonical nitrogen is present at high concentration it usually
ranges from 500 to 6000 mg L− 1 [137]. N and N-containing compounds
in water may result in several environmental problems. The large
number of animal husbandries all over the world generate enormous
amount of slurry. In Spain, the number of pigs recorded was 27 million,
producing approximately 6.5 Hm3 of waste [39]. Approximately 80% of
the dietary nitrogen is lost in animal excreta results in NH3 volatilization
[200,201]. The direct application of animal manure in agriculture and
the anthropogenic addition of manure to the environment can cause
serious environmental problems like eutrophication resulting in
inhibited plant growth [160,161,202], animal breeding and survival.
Ammonia (NH3) is a colourless gas produced from the decomposition of

4
M. Sajjad et al.
the organic N compounds by microbes present in poultry manure. The
lacking of an ionic charge, able it quickly to produce it into the atmo­
sphere in a gaseous state. The formation of NH3 in litter or manure de­
pends on the pH, moisture, temperature and nitrogen content of the
manure [141]. Production of NH3, greenhouse gases and other odorous
compounds is a serious problem in livestock manure disposal in compost
or traditional landfill [95]. Manure waste is also a hazardous source of
nitrates and pathogens that can affect surface and ground water if not
properly managed [112]. Globally, management of nutrients which are
releasing from concentrated livestock breeding is a considerable
ecological challenge [108].
Ammonia is an important constituent in fertiliser production.
Ammonium nitrogen (ammonium and ammonia) is also one of the high
ranked significant pollutants in the aquatic environment, globally. High
concentrations can cause algal blooms, health risks to fish and toxicity
problems [30]. The N and P recovery and conservation different sectors
such as animal husbandry, municipal and industrial wastes are vital
because of environmental and economic repercussions. Sustainable ap­
proaches for P recovery from both liquid and solid waste are imperative
to close the P cycle in current society and report upcoming shortage
[31]. Therefore, we attempt to design a review paper based on the
sequestration of these nutrients (P and NH3) from animal wastewater
using different techniques. The variety of methodologies and previous
attempts applied to remove P and N worldwide, are discussed along with
their applications and limitations.
4.2. Phosphorus in animal waste
Phosphorus (P) is mineral nutrient that is important for all creatures
and is essential for most living things as a fundamental part of nucleic
acid [100], and considered as critical material [37]. There is a finite
source of P globally and hence, recovery of P from discarded material is
required [92]. Bhatti et al. [7] reported that high levels of this mineral in
wastewater, because of unprocessed sewage waste materials and agri­
cultural run-off resulted in interruptions in food chain. Ecological
problems in lakes such as eutrophication, in rivers and in seas can result
from uncontrolled and excessive discharge [100]. Biogas slurry contains
large amount of P, which is considered an environmental pollutant
[94,97]. Massive P mineral concentrations releasing from domestic,
industrial and agricultural activities into natural water bodies, which
generally results in an overabundance of phytoplankton. High phyto­
plankton levels reduce the dissolved oxygen (DO) in water bodies, which
destroys other aquatic life and disturbs the balance of the aquatic
ecosystem [113]. In nature, P is the main limiting factor in biomass
growth. Therefore, its sequestration from wastewater is momentous in
diminishing the amount of nutrients entering the aquatic environment
and thereby preventing algal blooms and eutrophication [131].
5. Recovery of nitrogen and phosphorus minerals
5.1. Recovery of nitrogen
Animal dung can contribute to air and water pollution via volatili­
zation of free nitrogen and ammonia transfer from manure storage an­
imal husbandries, and treatment accommodations. According to US,
EPA, anaerobic digestion is progressively used to liquid manure for the
stabilization of the present organic matter along with energy recover
from biogas. Anaerobic digestion transforms organic phosphorus and
nitrogen to phosphate and ammonia, causing nutrient transfer from the
already manure applied agricultural land. The resulted phosphate and
ammonia is even more unsafe for the environment [65]. Biogas slurry is
historically has been utilized as a fertiliser due to its richness in nutrients
like N, P and K. However, the direct application of BGS to soil causes
environmental problems because of the high concentrations of ammo­
nium and N. A variety of technologies has emerged to recover ammo­
nium N as fertiliser from BGS [58,203]. The ammonia recovery from
5
Acta Ecologica Sinica xxx (xxxx) xxx
BGS or animal waste into fertiliser is not only a source of green and
sustainable fertiliser production, but also an important method to
minimize ecological issues related to BGS [56,57,204]. Numerous
methodologies have been used to remove ammonia mineral from
wastewater. These include membrane filtration, ion exchange, chemical
precipitation, biological treatment, adsorption and a few less recognized
technologies like aeration, air stripping and photocatalytic oxidation
[205]. Barampouti et al. [4] reported that ion exchange known to be a
physic-chemical tools, which use adsorption process to recover nutrients
such as N, whereas nutrients are carried away sorbents biologically or
via using chemical like NaCl and HNO3. Solid sorbents such as Zeolite is
utilized for the recovery of P up to 100% and N up to 83% from the liquid
digestate has been documented. Both Nitrification as well as denitrifi­
cation are generally applied to remove N from waste watercourses,
however these techniques do not adhere to the discharge standards [22].
Technique such as chemical precipitation can also be used for nutrient
recovery and is a widely acceptable approach but the process is not
economically feasible due to the requirements of additional chemical
reagents and a long operational period [147,206]. Some authors have
also reported wet scrubber and stripping as efficient technologies for the
recovery of ammonia from BGS [11,89].
The stripping process has been applied to digestate for removing NH3
but there are obstacles to the practical application of this approach as it
is very difficult and not cost effective. The gas permeable membrane
method is an economically efficient technique used to recover ammonia
from animal manure. It converts ammonia into an ammonium salt fer­
tiliser. The major disadvantage of this technique is the cost of the alkali
chemicals used to upsurge the pH of the manure [178]. Shi et al. (2020)
undertook a techno-economic evaluation of ammonia mineral recovery
from BGS using vacuum membrane distillation. Their results revealed
that the highest ammonia separation factor attained up to 8.05 under the
most favourable experimental conditions. This allows for technical
viability of ammonia recovery from BGS by vacuum membrane distil­
lation without pH adjustment. This research offers a sustainable and
green nitrogen fertiliser manufacturing technique.
Multiple systems for ammonia recovery, ammonia pre-treatment,
fertiliser production and biogas upgrading, are applied for biogas pro­
duction simultaneously. A maximum (99.30%) ammonia removal effi­
ciency has been reached with experimental conditions of 10% CO2
content, at 90 ◦ C with a 6 h stripping time. Ammonia absorption of the
ammonia-bearing biogas attained a crystalline ammonia and biogas
upgrading, which is utilized when recovering ammonia [155,162]. The
struvite technique is applied to manage and recover nutrients from an­
imal slurry wastewater containing high nutrient and organic contents.
However, in numerous cases, industrial wastewater treatment plants do
not accept compounds of N because of the lack of a biological waste­
water treatment plant. Struvite precipitation is helpful in the recovery of
ammonia and other nutrients like phosphate [106] from BGS, and can
recover approximately 72.1% of the ammonium‑nitrogen (NH4-N) in
the liquid phase [175]. Struvite technology produces a well-known
fertiliser containing both nutrients of P and N. The production is
confirmed by numerous studies utilizing the N or P containing waste
sources [15,145]. Regardless of the benefits of the technology, the
struvite technique requires additional chemicals (e.g. Mg) in the same
quantity as P and ammonia, which limits its application [81].
Gas-permeable membrane technology is an acceptable option for the
recovery of NH3 from liquid manures [178]. A simple diagrammatic
sketch used in this approach is provided in Fig. 2.
According to Vanotti et al. [152], with greater NH3 recovery, the
captured P contains a higher P2O5 content of approximately 37–46%,
>98% existing, which is alike to the biomineral newberyite composi­
tion. Ammonia recovery from swine manure via dry AD plus ammonia
stripping yields promising results. Huang et al. [61,63] documented that
a maximum (90%) of the total ammonia nitrogen (TAN)) found in swine
waste can be proficiently recovered using air stripping process at total
solids (TS) around 20%. Therefore, the combination of NH3 stripping
M. Sajjad et al.
Fig. 2. Schematic diagram presenting the configuration of the procedure used to remove ammonia and phosphorus from liquid swine manure (Modified from [152]).
along with short-term dry AD attained approximately 60% total nitrogen
recovery. Ammonia stripping is actually physic-chemical technology,
stripping NH3 from digestate up to 95% of ammonia by contacting with
steam or air at optimal conditions including temperature of 70 ◦ C and
high pH of ≥10 [88]. Then, ammonia recovered by acids in the form
ammonium salts, which can be utilized as mineral fertiliser and in the
form of substrates for numerous other commercial processes. The
stripping process is a simple and well-developed technique, only N is
recovered and the released liquid waste has high pH values that require
post-treatment prior discharging, and the high energy requirements for
heating. However, the process is not cost effective and requires high
energy inputs (Qiu et al., 2020). Ammonia can be recovered from swine
manure using gas-permeable membranes by converting ammonia into
an ammonium salt fertiliser. Aeration is helpful in increasing the pH
above 8.5, which allows rapid conversion of NH+ 4 into gaseous NH3 with
efficient recovery by permeation through the submerged membrane.
The efficiency of this process is enhanced because large amounts of al­
kali chemicals are substitued to attain high NH+ 4 recovery with signifi­
cant environmental and economic savings [45]. Homoionic zeolite is
used as an adsorbent material for the recovery of NH+ 4 -N from swine
manure anaerobic digestate. A recovery of approximately 600 mg L− 1 of
− 1
NH+ 4 -N with a sorption capacity of 4.9–5.46 mg g was recorded [114].
Some researchers have also utilized Chinese zeolite for this purpose and
found that 250 mg L− 1 of NH+ 4 -N with a sorption capacity of 9.1–9.6 mg
g− 1 was recorded [50].
Vacuum membrane distillation is an effective technique for ammonia
recovery from BGS [56,57]. A relatively high concentration of aqueous
ammonia (1.0 mol-N L− 1, which is higher than the value in feed BGS <
6
Acta Ecologica Sinica xxx (xxxx) xxx
0.2 mol-N L− 1) can be recovered on the permeate side, with >98% of the
N element in the form of free ammonia. The obtained aqueous ammonia
can be utilized for acid gas scrubbing (e.g. carbon capture) [58]. Some
researchers have suggested that the process of osmotic pressure
[101,110] can recover ammonia nitrogen from the BGS.
Anaerobic digestion is one of the most cost-effective techniques
owing to the high energy recovered in the form of CH4 with limited
environmental impacts [186]. The development of concentrated live­
stock has grown the installation of different scaled biogas plants in order
to control the agricultural wastes. Approximately 90% of poultry and
livestock composts are treated with anaerobic digestion (AD) in China
[33]. The world demand for nitrogenous fertiliser is estimated to be
growing annually at the rate of 1.08% from 2015 to 2020 [40]. There­
fore, the recovery of ammonia by AD provides an efficient source of
nitrogenous fertiliser. However, as different types of waste biomass have
specific features, the bioenergy conversion efficiency of this process is
not ideal. The BGS has high concentrations of ammonia nitrogen (NH3-
N, 500–3000 mg L− 1) and an unusually low C/N ratio resulting from the
carbon utilization by AD [143]. The process is not economically feasible
due to the low production of biogas and the hydrolysis rates may limit its
application. Another problematical feature of AD is that the nutrient rich
sewage can require further treatment before discharge [98]. The emis­
sions of nitrous oxide (N2O) from aerobic treatments is also an envi­
ronmental problem [12]. Moreover, the large volume of biogas slurries
becomes a problem to solve. Activated sludge is unsuccessful for the
effective recovery of nutrients from wastewater. The conventional
activated sludge process is mostly used for the recovery of NH3, how­
ever, there are limitations in this approach. The process is less efficient
M. Sajjad et al.
at trace levels because insufficient phosphate decreases the metabolism
of microorganisms. The pre-treatment of AD (including the removal of
ammonia) may improve the performance of the process by reducing the
quantity of ammonia in the feeding substrate.
Anaerobically digested (AD) swine slurry can be applied to recover
ammonium using biochar prepared from hardwood (WB), corncobs
(MCB) and mixed sawdust pellets (MSB). WB exhibited better recovery
than the other two types with a maximum sorption efficiency of 67–114
mg g− 1 due to its superior surface area and larger pore volume [76]. Air
stripping of the BGS can be developed for ammonia recovery using a
process that is totally temperature and pH dependent. Maximum NH3
(90%) can be recovered by a constant temperature and pH of 35 ◦ C and
10.3 respectively [69]. However, the process is not suitable for pig slurry
in AD as a pre-treatment. In this situation, instead of removing ammonia
during the process, the increased pH is unable to decrease the free
ammonia concentration [11]. Provolo et al., [126] introduced a new
concept in this process by the slow releasing of ammonia by non-stop
mixing of the digestate with a continuous air stream crosswise to the
surface of the liquid. The process achieves an efficiency of approxi­
mately 80–90% for the removal of N in the form of ammonia from the
substrate. However, to apply this process on a large scale requires
further research and the testing of different slurries with different
characteristics. Luo et al. [94,97] worked on the removal of nitrogen
from piggery wastewater utilizing fermented superphosphate within the
pre-treatment stage and an MAP fertiliser pot test. The effect of fertiliser
of the products recovered investigated using pot spots. The optimum
conditions for Nitrogen and phosphorus recovery were 30 g L− 1, initial
pH 9.5 with contact time of 30 min. The percentage of removal for NH3-
N recorded was 50.30% noted to be higher ordinary phosphate fertiliser
(8.9%). The applied combined process showed high efficiency for the
removal of nitrogen and phosphate along with good quality phosphate
fertiliser.
Biochar derived from organic waste biomass is gradually becoming
accepted as a multifunctional material for a wide range of environ­
mental applications, such as the removal and recovery of both organic
and inorganic contaminants from wastewater and polluted soils [105].
TMg-Al-modified biochar can be used for the ammonium, nitrate, and
phosphate removal from eutrophic water. Biochar made from soybean
straw, modified with Mg, Al, and Mg–Al displayed an outstanding
adsorption performance for the nutrients (PO3− 4 , NH4 and NO3 ) from
+ −
eutrophic water. For a single-solute-adsorption, the Al/BC, Mg/BC and
Mg-Al/BC exhibited the optimal removal of NO−3 (40.63 mg g− 1), PO3− 4 P recovery and the biochemical development of BGS. Luján-Facundo
(74.47 mg g− 1) and NH+ − 1
4 (0.70 mg g ) respectively [176]. Kizito et al.,
[76] applied biochar derived from hard wood, corn cobs and mixed
sawdust with a maximum recovery of 500–580 mg L− 1 with a sorption
capacity of 27.2–114 mg g− 1. Biochar has a definite adsorption capa­
bility regarding ammonia nitrate [79], and is about 1 mg g− 1 [32]. Rice
husk biochar can be utilized for the adsorption of ammonium N from
piggery manure. As demonstrated in Table 5, the biochar obtained from
corncobs, wood, rice husk and sawdust had a high adsorption capacity,
indicating potential to be used as alternative low-cost adsorbent for the
removal of ammonium [76]. The excellent adsorption efficiency of the
biochars is due to their physiochemical properties, such as porosity,
BET-N2 surface area and structural polarity (higher O/C values). The
collective effect of the high surface area and surface polarity increases
their ammonium removal by a combination of physical and chemical
adsorption [159]. The feedstocks for biochar production are plentiful
and inexpensive as they are mostly obtained from agricultural biomass
and solid waste.
The percent of ammonium nitrate removal is usually determined
using the following eq. (1):
(Ci − Ce)
Removal (%) = × 100 (1)
Ci
Ci and Ce are the initial and final concentrations (mg L− 1), respec­
tively. The adsorbed amount of ammonium nitrate at different
7
Acta Ecologica Sinica xxx (xxxx) xxx
operational conditions is generally calculated using the eq. (2):
(Ci − Ce)
qe = ×V (2)
W
Where qe (mg g− 1) is the amount of HMs adsorbed, Ci is the initial
and Ce is the final equilibrium concentrations (mg L− 1); V is volume (L)
and W is weight (g L− 1) of the adsorbents. Results indicated that the
− 1
maximum NH+- 4 N separation from the slurry at 1400 mg N L was 44.64
± 0.602 mg g− 1 and 39.8 ± 0.54 mg g− 1 for wood and rice husk biochar,
respectively. The overall results recommend wood and rice husk biochar
for use in ammonium removal from piggery slurry over a broad con­
centration range [75].
Other techniques mentioned previously such as ultrasound/H2O2
digestion coupled with HFO/biochar adsorption process, etc. are also
very useful for the recovery of ammonia and P from biogas and slurries
but are not cost effective at this stage. Although various techniques have
been used for the recovery of ammonia and phosphates from wastewater
and BGS, none of them has achieved 100% success. Despite the
mentioned success, the challenge with all these new methods is the high
cost of raw materials and the initial set-up of the process, particularly in
large-scale projects [138].
5.2. Recovery of phosphorus
The consumable phosphorus (P) resources are progressively
decreasing globally [23], and biogas slurry is enriched with P, which is
categorized as a pollutant. The removal of P from wastewater has
recently received the attention of many researchers. Many methodolo­
gies have been tested, such as biological, chemical, and physical treat­
ment processes. Zeng et al. [182] performed experimental work on P
recovery from pig farm BGS using a catalytic ozonation technique with
MgO for catalytic purpose and magnesium (Mg) source. They experi­
mentally examined the role of pH, the Mg material nature, catalyst and
dosage of ozone applied, on the catalytic ozonation with efficiency and P
recovery. The results demonstrated that MgO is efficient compared to
MgCO3 and other catalyst chemicals such as dolomite and to MgCl2. By
adding MgO at rate of 1.5 g L− 1 and ozone at a rate of 0.58 g L− 1, the
chroma, UV254 and COD recovery rates from the BGS were achieved at
levels of 88.87%, 70.22%, and 55.43% respectively. There was also an
impressive 98.47% recovery of P when catalytic ozonation was per­
formed at pH 10. Results revealed that this is an efficient technology for
et al. [96] assessed two alternatives (including P production and energy
recovery) for managing pig slurry wastewater containing high nutrient
and organic contents. Results indicated that the P and CH4 recovery was
maximum at a elevated pH and optimum temperature. However,
although most phosphates minerals were removed, the low concentra­
tions of phosphate in the urine limited the removal efficiency of
ammonium to 1%. The conventional activated sludge process (biological
methods) are the most efficient and can remove approximately 100% of
phosphate mineral from the BGS [62].
Air–cathode single chamber microbial fuel cells (MFCs) are able to
recover approximately 70–82% of the P from swine slurry [66].
Anaerobic digestion is widely used for the production of biogas and for
the stabilizing treatment of organic effluent streams [33]. P was suc­
cessfully recovered from anaerobically digested swine wastewater in a
pilot-scale experiment. The process involved a sequencing batch reactor
(SBR) and a continuous-flow reactor with struvite accumulation devices.
Approximately 85% of the P was removed and recovered without
chemical additions using this process [138]. Studies have suggested that
Mg-ammonium phosphate precipitation is the most proficient process
[60,74] for the recovery of P since it generates a precious slow-release
fertiliser struvite crystal in the P removal process
[136,156,158,174,177]. Struvite precipitation is useful in recovering
phosphate from BGS [173]. Piveteau et al. [124] introduced an acidi­
fication step in the recycling of P as a struvite from pig slurry to dissolve
M. Sajjad et al. Acta Ecologica Sinica xxx (xxxx) xxx

the inorganic solids containing most of the P (acidogenesis). Their

(Ci − Ce)
research was mostly based on the biological acidification of a number of Removal (%) = × 100 (3)
Ci
pig slurries utilizing sucrose as a model organic co-substrate. Lowering
the pH to 5.5–6 with sucrose causes the most P dissolution, and offers the In the equation, Ci and Ce are the initial and final concentrations
most favourable conditions for recovering P as struvite. However, (mg L− 1) of phosphate respectively. The high P removal capacity of 157
further research is required to identify the relationship between P re­ mg g− 1 showed that the granular form of biochar could be used as an
covery and the production of renewable energy in the successive adsorbent for phosphate sequestration from aqueous solutions [70]. P
methanisation stage. Wang et al. [157,163] used humidification- can be recovered with chemically treated biochar’s, particularly those
dehumidification (HDH) technique for the concentration biogas slurry biochars which modified with acids, alkali metals and salts. The capacity
and to discover feasible and an inexpensive methodology to provide of P uptake was calculated by laboratory batch adsorption experiments.
suitable environments for maintainable application of biogas slurry. The The experimental outcomes showed that P removal can be improved
recovered nutrients such as total P, ammonia N, in addition to soluble from quite low levels (2.1–3.6%) to comparatively high levels
salt in the condensed conditions reached up to maximum level (96%), (66.4–70.3%) by mixing with magnesium [142]. However, further
when the biogas slurry initial pH, temperature, the air flow rate and research approaches are obligatory for the better understanding why the
heating time was maintained at 6, 70 ◦ C, 10 L/min and 30 min adsorbed PO4-P discharge was minimal for most of the selected bio­
respectively. char’s, as this determines the biochar’s efficacy for re-use or for use in
Biological enrichment with algae is also used for the recovery of P amending soil.
from slurries, manures and sludge [156,158]. Biological techniques are Advances in materials with high adsorption and regeneration ca­
economical methods, especially in wastewater from pig farms owing to pacity may enhance phosphate mineral removal and lower the volume
the high concentration of NH3-N, total phosphorus (TP) and low C/N of of sludge requiring disposal thus making adsorption a cost-effective
the BGS [5]. However, it is sometimes difficult for wastewater treatment technique for practical applications. Furthermore, the adsorption
facilities to attain the standard requirements for waste effluent, causing methodology is not limited to phosphate removal and can be used for
water pollution [182]. Approaches like diammonium phosphate (DAP) phosphate recovery [9]. Layered double hydroxides (LDHs) can be used
and enhanced struvite (ES) are useful for the recovery of both N and P in in the elimination of P from wastewaters, because it is a chief and eco-
waste streams [46]. In addition to DAP, there are many other chemical friendly process that produces chemical sludge in low quantities and
species such as ammonium phosphate (AP) which are recovered during the adsorbed P can easily be recovered. The main challenge with LDHs is
the reaction between ammonia and phosphate, including mono- finding and developing a material with a high adsorption capability
ammonium phosphate (MAP) and tri-ammonium phosphate (TAP) etc. [207]. Phosphate mineral recovery from piggery BGS by
[44,47]. These are environmentally friendly and economically feasible ultra-sonication, aeration and the addition of MgO desulfurization waste
processes [111]. residue (MDWR) is considered a promising technology. Using an
Some researchers have also found promising results with the appli­ MDWR, BGS volume of 0.8 g⋅L− 1, with an initial pH of 9.5, and aeration
cation of magnesium oxide desulfurization waste residue (MDWR) for P time of 2 h, the optimal recovery percentage of PO3− 4 -P was 98.90% [94,
recovery from biogas piggery slurry. This is a comparatively more 97]. Other techniques such as magnesium ammonium phosphate pre­
suitable technique than others for the recovery of P from biogas piggery cipitation is known to be the most efficient [90] because the process
slurry [94,97]. Further statistics are provided in the Table 4. Adsorption yields a valued slow-release fertiliser struvite crystal removing P at same
is an efficient process in phosphate removal, due to its impressive ad­ time [174,177]. Several studies have been published on the recovery of
vantages, including simple and easy operation, fast adsorption rate and P from piggery biogas digestate using magnesium ammonium phosphate
high removal efficiency, especially in cases of low phosphate concen­ precipitation [41,73]. Ichihashi and Hirooka [66] reported recoveries of
tration [121]. Marine macroalgae can be used along with biochar for 79–82%, Song et al. [138] documented a P recovery efficiency of 85%,
phosphate mineral removal, which is an ideal technique with added and Liu et al. [90] reported a recovery efficiency of 65%. However, the
value. The removal rate of the selected mineral can be calculated using mentioned research recovered P only from the supernatant of the slurry
the following eq. (3): and not from the biogas residue, so the overall P recovery application
percentage is low.
Phosphorus from BGS can be recovered using ultrasound/H2O2
digestion coupled with a HFO/biochar adsorption technique. The opti­
Table 4 mum total P release efficacy was attained at an inorganic P/total P ratio
Various results for phosphorus recovery from slurry using different techniques. of 95.0% at pH 4.0 with 1 mL of added H2O2 and ultra-sonication for half
S⋅No Wastewater Chemicals P/Mg PO3−
4 -P References an hour [58]. The sorption efficiency of the biochar can be utilized for P
molar recovery recovery from slurries. In different experiments using biochar as the
ratio (%)
adsorbent, 0.24 mg g− 1 PO3−4 was adsorbed from dung using the biochar
1 Swine N, P and Mg NA 79.0–82.0 Ichihashi and that is approximately 50% of the total P in the manure slurry [208].
wastewater in Hirooka [66] Wang et al. [157,163] investigated P recovery utilizing an iron-rich
wastewater
sludge biochar with significant results in the recovery of P (1.843 mg
3 Swine MgCl2 0.8:1.0 65 Liu et al. [90]
wastewater g− 1) from the liquid phase of the anaerobic digestate. The obtained P is
4 Swine MgCl2 2.0:1.0 79 Liu et al. capable of application as a value added fertiliser for garden soil. Phos­
wastewater [192] phate removing, iron-modified biochars manufactured from waste
5 Poultry MgCl2, 1.0:1.0 85.4 Yetilmezsoy
activated sludge is effective and efficient. The maximum phosphate
manure MgSO4, and Sapci-
wastewater MgO, Zengin [193] adsorption capacity of biochar is enhanced by the addition of FeCl3 and
KH2PO4 reached 111.0 mg g− 1. The phosphate adsorption efficiency of biochar
6 Digested Bittern 1.0:0.6 90 Ye et al. [173] remained >60% even after five consecutive recycles [172]. Other
swine studies have revealed that P can be recovered utilizing biochar derived
wastewater
from metal polluted feedstock. From several decades, biochar has been
7 Swine MgCl2 1.6:1.0 91 Burns et al.
wastewater [194] utilized for the nutrients removal from aqueous solution [79]. Biochar
8 Digested MDWR 1.0:0.54 98.9 Luo et al. has become a cost effective and efficient biomaterial for the recovery of
swine [94,97] organic pollutants and nutrients not only from household and agricul­
wastewater
tural wastewater but also from industrial wastewater [72,134,187].

8
M. Sajjad et al.
Kubar et al. [79] carried out the experimental work on the recovery of P
and NH3 minerals from BGS as value-added fertiliser by biochar and
struvite co-recipitation. Their experimental outcomes revealed that
phosphate mineral could be efficiently recovered by biochar using the
struvite precipitation technique. Application of Mg biochar is a suitable
option for recovering phosphate and ammonia minerals from urine as
value-added fertiliser. Mg-biochar showed high removal capabilities for
ammonium and phosphate minerals, reaching up to 47.5 mgN g− 1 and
116.4 mgP g− 1, respectively [169].
5.3. Factors effecting the removal efficiency of biochar
Biochar is a carbonized material prepared by degasification of
organic material or pyrolysis under low supply of oxygen, has recieved
attention of the researchers in modern era [84,150]. The removal effi­
ciency biochar depends on many factors [29]. According to Xie et al.
[168], dose of biochar effect the removal of N and P, by increasing the
dosage of biochar, the removal of ammonia N, but has less effect on the
removal of P. The concentration of N and P also play important role
regarding the removal of N and P by biochar. Kizito et al. [75] revealed
that by increasing the concentration of N, removal efficiency of biochar
decreases. But P absorption increases by increasing the concentration of
P [35]. The removal and recovery of the mentioned nutrients also de­
pends on the pH. Research studies showed that the efficiency of corn
stalk biochar for removal of NH4 + decreased at acidic conditions (below
pH 7) and increased at basic conditions (above pH 7), means the removal
of these two nutrients is highly pH dependent [99]. In the same way the
removal efficiency of carrot biochar for P is lower at pH below 7, and is
maximum upto pH 9, then slightly decreases at pH 10 [29]. Researchers
elucidated that by increasing the pore volume and surface area of bio­
char, NH3 volatilization increased [209]. In the same manner, the
removal of P also increases by increasing the number of pores and sur­
face area of biochar however, this is not valid for all types of biochar
[75]. Studies have demonstrated that temperature also play an impor­
tant role for the removal of P and N by biochar. By increasing the
temperature up to certain degree, the removal efficiency of biochar for P
and N increases [29].
6. Conclusion and recommendations
Different techniques can be utilized to remove and recover and P
from biogas slurry. Due to the increased number of livestock and animal
slurry into natural water bodies without pre-treatment, concentrations
of N and P released from animal husbandry into natural water bodies
have dramatically increased over the last few decades, posing a threat to
the environment, creating environmental problems, globally. Many
techniques for the recovery and removal of N and P were discussed;
however, every technology has its own limitations. The application of
each technology shows enormous potential in nutrient recovery and
waste biomass treatment. However, improvements in the efficiencies of
these technologies for biogas conversion and the treatment of digested
liquid are the key issues that require further investigation before utili­
zation for widespread applications. Among the different technological
process used for the N and P recovery from animal slurry, biochar
application is the most effective due to properties like porous structure,
large specific surface area, enriched surface functional groups and
mineral components, and low cost. Additionally, they are environmen­
tally friendly with a variety of readily availability raw materials, and
therefore recommended for the recovery of N and P from animal waste.
7. Future research considerations
A series of research operations have been conducted for the recovery
of N and P from animal waste. However, there is an urgent need for
innovative methods to utilize the high concentrated animal effluents for
the recovery of the mentioned nutrients to reduce treatment costs.
9
Acta Ecologica Sinica xxx (xxxx) xxx
Furthermore, biochar is the most efficient, cost effective and environ­
mental friendly material for remving and recovering of N and P from the
animal liquid waste. The capacity of biochar can be further enhanced
with additional chemicals, or with nanoparticles. The eco-design and
sustainability of existing approaches for the recovery of these nutrients
will enable the manufacturing of value added products such as fertil­
isers. This will not only provide a pollution free environment but will
also reduce pressure on the use of finite raw materials.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
This study was funded by National Natural Science Foundation of
China (41571288), Research initiation fund of Hainan University (KYQD
(ZR)20032), Hainan Provincial Natural Science Foundation of China
(319MS008), National Science and Technology Support Program of
China (2014BAD14B04), Fujian Provincial Department of Science and
Technology Project (2015Y0084), National Natural Science Foundation
of China (41867047), and Hainan Science and Technology Plan Project
(ZDKJ2017002).
References
[1] M.D. Aitken, M.D. Sobsey, N.A. Van Abel, K.E. Blauth, D.R. Singleton, P.L. Crunk,
C. Nichols, G.W. Walters, M. Schneider, Inactivation of Escherichia coli O157: H7
during thermophilic anaerobic digestion of manure from dairy cattle, Water Res.
41 (8) (2007) 1659–1666.
[2] M. Barret, N. Gagnon, E. Topp, L. Masse, D.I. Massé, G. Talbot, Physico-chemical
characteristics and methanogen communities in swine and dairy manure storage
tanks: spatio-temporal variations and impact on methanogenic activity, Water
Res. 47 (2) (2013) 737–746.
[3] J. Bayo, M.D. Gómez-López, A. Faz, A. Caballero, Environmental assessment of
pig slurry management after local characterization and normalization, J. Clean.
Prod. 32 (2012) 227–235.
[4] E.M. Barampouti, S. Mai, D. Malamis, K. Moustakas, M. Loizidou, Exploring
technological alternatives of nutrient recovery from digestate as a secondary
resource, Renew. Sust. Energ. Rev. 134 (2020), 110379, https://doi.org/
10.1016/j.rser.2020.110379.
[5] N. Bernet, F. Beline, Challenges and innovations on biological treatment of
livestock effluents, Bioresour. Technol. 100 (22) (2009) 5431–5436.
[6] W.H. Bergland, C. Dinamarca, M. Toradzadegan, A.S.R. Nordgard, I. Bakke,
R. Bakke, High rate manure supernatant digestion, Water Res. 76 (2015) 1–9.
[7] H. Bhatti, J. Hayat, M. Iqbal, S. Noreen, S. Nawaz, Biocomposite application for
the phosphate ions removal in aqueous medium, J. Mater. Res. Technol. 7 (2018)
300–307.
[8] N. Bhatnagar, D. Ryan, R. Murphy, A.M. Enright, A comprehensive review of
green policy, anaerobic digestion of animal manure and chicken litter feedstock
potential–global and Irish perspective, Renew. Sust. Energ. Rev. 154 (2022),
111884.
[9] B.K. Biswas, K. Inoue, K.N. Ghimire, H. Harada, K. Ohto, H. Kawakita, Removal
and recovery of phosphorus from water by means of adsorption onto orange
waste gel loaded with zirconium, J. Bioresour. Technol 99 (2008) 8685–8690.
[10] N.S. Bolan, M.A. Khan, D.C. Donaldson, C. Matthew, Distribution and
bioavailability of copper in farm effluent, J. Sci. Total. Environ. 309 (2003)
225–236.
[11] A. Bonmati, X. Flotats, Air stripping of ammonia from pig slurry: characterization
and feasibility as a pre-or post-treatment to mesophilic anaerobic digestion,
J. Waste Manag. 23 (2003) 261–272.
[12] S. Calvet, J. Hunt, H. Misselbrook, Low frequency aeration of pig slurry affects
slurry characteristics and emissions of greenhouse gases and ammonia, Biosyst.
Eng. 159 (2017) 121–132.
[13] W. Cao, X. Wang, S. Sun, C. Hu, Y. Zhao, Simultaneously upgrading biogas and
purifying biogas slurry using cocultivation of Chlorella vulgaris and three
different fungi under various mixed light wavelength and photoperiods,
Bioresour. Technol. 241 (2017) 701–709.
[14] K.B. Cantrell, T. Ducey, K.S. Ro, P.G. Hunt, Livestock waste-to-bioenergy
generation opportunities, Bioresour. Technol. 99 (17) (2008) 7941–7953.
[15] I. Çelen, M. Türker, Recovery of ammonia as struvite from anaerobic digester
effluents, Environ. Technol. 22 (11) (2001) 1263–1272.
[17] Y. Chen, G. Yang, S. Sweeney, Y. Feng, Household biogas use in rural China: A
study of opportunities and constraints, Renew. Sust. Energ. Rev. 14 (2010)
545–549.
M. Sajjad et al.
[18] China Ministry of Environmental Protection, S.S.B.a.M.o.A, First National Census
on Pollution Sources, China Government Press, 2010, p. 200 [February 9, 2010].
[20] A. Chiumenti, F. Borso, R. Chiumenti, F. Teri, P. Segantin, Treatment of digestate
from a co-digestion biogas plant by means of vacuum evaporation: tests for
process optimization and environmental sustainability, Waste Manag. 33 (2013)
1339–1344, https://doi.org/10.1016/j.wasman.2013.02.023.
[21] China Ministry of Environmental Protection, S.S.B.a.M.o.A, First National Census
on Pollution Sources, China Government Press, 2010, p. 200.
[22] E. Choi, D. Kim, Y. Eum, Z. Yun, K.S. Min, Full-scale experience for nitrogen
removal from piggery waste, Water Environ. Res. 77 (2005) 381–389.
[23] R.B. Chowdhury, G.A. Moore, A.J. Weatherley, M. Arora, Key sustainability
challenges for the global phosphorus resource, their implications for global food
security, and options for mitigation, J. Clean. Prod. 140 (2017) 945–963.
[24] P.M. Christy, L. Gopinath, D. Divya, A review on anaerobic decomposition and
enhancement of biogas production through enzymes and microorganisms,
Renew. Sust. Energ. Rev. 34 (2014) 167–173.
[25] A. Comparetti, C. Greco, K. Navickas, K. Venslauskas, Evaluation of potential
biogas production in Sicily, Eng. Rural Dev. 11 (2012) 555–559.
[26] C. Côté, D.I. Massé, S. Quessy, Reduction of indicator and pathogenic
microorganisms by psychrophilic anaerobic digestion in swine slurries, Bioresour.
Technol. 97 (4) (2006) 686–691.
[27] W. Czekała, A. Lewicki, P. Pochwatka, A. Czekała, D. Wojcieszak,
K. Jóźwiakowski, H. Waliszewskad, Digestate management in polish farms as an
element of the nutrient cycle, J. Clean. Prod. 242 (2020), 118454, https://doi.
org/10.1016/j.jclepro.2019. 118454.
[28] J. Dach, P. Boniecki, J. Przybyl, D. Janczak, A. Lewicki, W. Czeka, Energetic
efficiency analysis of the agricultural biogas plant in 250 kW (e) experimental
installation, Energy. 69 (2014) 34–38.
[29] Y. Dai, W. Wang, L. Lu, L. Yan, D. Yu, Utilization of biochar for the removal of
nitrogen and phosphorus, J. Clean. Prod. 257 (2020), 120573.
[30] S. Ding, M. Chen, M. Gong, X. Fan, B. Qin, H. Xu, C. Zhang, Internal phosphorus
loading from sediments cause seasonal nitrogen limitation for harmful algal
blooms, Sci. Total Environ. 625 (2018) 872–884.
[31] E. Desmidt, K. Ghyselbrecht, Y. Zhang, L. Pinoy, B. Van der Bruggen,
W. Verstraete, K. Rabaey, B. Meesschaert, Global phosphorus scarcity and full-
scale P-recovery techniques: a review, J. Crit. Rev. Environ. Sci. Technol. 45
(2015) 336–384.
[32] J. Du, J. Bao, M.A. Hassan, S. Irshad, M.A. Talib, H. Zheng, Efficient capture of
phosphate and cadmium using biochar with multifunctional amino and
carboxylic moieties: kinetics and mechanism, Water Air Soil Pollut. 231 (2020)
1–16.
[33] N. Duan, D. Zhang, C. Lin, Y. Zhang, L. Zhao, H. Liu, Z. Liu, Effect of organic
loading rate on anaerobic digestion of pig manure: methane production, mass
flow, reactor scale and heating scenarios, J. Environ. Manag. 231 (2019)
646–652.
[34] E. Dinuccio, W. Berg, P. Balsari, Gaseous emissions from the storage of untreated
slurries and the fractions obtained after mechanical separation, Atmos. Environ.
42 (2008) 2448–2459.
[35] J.O. Eduah, E.K. Nartey, M.K. Abekoe, H. Breuning-Madsen, M.N. Andersen,
Phosphorus retention and availability in three contrasting soils amended with
rice husk and corn cob biochar at varying pyrolysis temperatures, Geoderma 341
(2019) 10–17.
[36] T.D. Evans, An independent review of sludge treatment processes and
innovations, in: Biosolids Conference, Australian Water Association, Adelaide,
2008.
[37] EU Commission, Communication from the Commission to The European
Parliament, the Council, the European Economic and Social Committee and the
Committee of the Regions, Appl. Counc. Regul. COM, 2017.
[38] T.D. Evans, Recovering ammonium and struvite fertilisers from digested sludge
dewatering liquors, in: Resource Recovery Not Wastewater Treatment
Conference, Aqua-Environment, London, 2009.
[39] FAO, World Fertilizer Trends and Outlook to 2020, Food and Agriculture
Organization, Rome, Italy, 2016.
[40] FAO, World Fertilizer Trends and Outlook to 2020, Food and Agriculture
Organization, Rome, Italy, 2017.
[41] E.L. Foletto, W.R.B.D. Santos, S.L. Jahn, M.M. Bassaco, M.A. Mazutti,
A. Cancelier, A. Gündel, Organic pollutants removal and recovery from animal
wastewater by mesoporous struvite precipitation, Desalin. Water Treat. 51
(13–15) (2013) 2776–2780.
[42] W. Fuchs, F. Wager, R. Kirchmayr, R. Braun, B. Dorsg, Digestate treatment;
comparison and assessment of existing technologies, in: Third International
Symposium on Energy from Biomass And Waste. CISA, Venice, Italy, 2010.
[43] F. Gale, D. Marti, D. Hu, China’s volatile pork industry, in: Economic Research
Service Report, United States department of Agriculture, 2012, pp. 1–27 [LDP-M-
211-01(2012)].
[44] M. Gargouri, V. Chtara, P. Sharrock, A. Nzihou, H.A. Feki, Experimental study of
the purification of an industrial fertilizer(mono-ammonium phosphate) to large
scale using an experimental design, Int. J. Mater. Eng. 2 (4) (2012) 32–37.
[45] M.C. Garcia-Gonzalez, M.B. Vanotti, A.A. Szogi, Recovery of ammonia from swine
manure using gas-permeable membranes: effect of aeration, J. Environ. Manag.
152 (2015) 19–26.
[46] M.R. Gaterell, R. Gay, R. Wilson, T.J. Gochin, J.N. Lester, An economic and
environmental evaluation of the opportunities for substituting phosphorus
recovered from wastewater treatment works in existing UK fertilizer markets,
Environ. Technol. 21 (2000) 1067–1084.
10
Acta Ecologica Sinica xxx (xxxx) xxx
[47] R. Gilmour, Phosphoric Acid: Purification, Uses, Technology, and Economics vol.
6, CRC Press, Boca Raton, 2013, pp. 283–284.
[48] L. De Groot, A. Bogdanski, Bioslurry = brown gold? A review of scientific
literature on the co-product of biogas production, in: Bioslurry = Brown Gold?
Rev. Sci. Lit. Co-Product Biogas Prod, 2013.
[49] M. Gros, E. Marti, J.L. Balcázar, M. Boy-Roura, A. Busquets, J. Colon, A. Sanchez-
Melsio, I. Lekunberri, C.M. Borrego, S. Ponsa, M. Petrovic, Fate of
pharmaceuticals and antibiotic resistance genes in a full-scale on-farm livestock
waste treatment plant, J. Hazard. Mater. 378 (2019), 120716.
[50] X. Guo, L. Zeng, X. Jin, Advanced regeneration and fixed-bed study of ammonium
and potassium removal from anaerobic digested wastewater by natural zeolite,
J. Environ. Sci. 25 (2013) 954–961.
[52] M. Gustafsson, S. Anderberg, Dimensions and characteristics of biogas policiese
modelling the European policy landscape, Renew. Sust. Energ. Rev. 135 (2020),
110200.
[53] Y. Feng, Y. Guo, G. Yang, X. Qin, Z. Song, Household biogas development in rural
China: on policy support and other macro sustainable conditions, Renew. Sust.
Energ. Rev. 16 (2012) 5617–5624.
[54] X. He, T. Zhang, H. Ren, G. Li, L. Ding, L. Pawlowski, Phosphorus recovery from
biogas slurry by ultrasound/H2O2digestion coupled with HFO/biochar adsorption
process, Waste Manag. 60 (2017) 219–229.
[55] Q. He, G. Yu, T. Tu, S. Yan, Y. Zhang, S. Zhao, Closing CO2 loop in biogas
production: recycling ammonia as fertilizer, Environ. Sci. Technol. 51 (2017)
8841–8850.
[56] Q. He, Te Tu, S. Yan, X. Yang, M. Duke, Y. Zhang, S. Zhao, Relating water vapor
transfer to ammonia recovery from biogas slurry by vacuum membrane
distillation, Sep. Purif. Technol. 191 (2018) 182–191.
[57] Q. He, Long Ji, B. Yu, S. Yan, Y. Zhang, S. Zhao, Renewable aqueous ammonia
from biogas slurry for carbon capture: chemical composition and CO2 absorption
rate, Int. J. Green H. Gas. Con. 77 (2018) 46–54.
[58] Q. He, J. Xi, W. Wang, L. Meng, S. Yan, CO2 absorption using biogas slurry:
recovery of absorption performance through CO2 vacuum regeneration, Int.
Green H. Gas. Con. 58 (2017) 103–113.
[59] M.R. Huaitalla, E. Gallmann, X.J. Liu, E. Hartung, Aerial pollutants on a pig farm
in peri-urban Beijing, China. Int. J. Agric. Biol. Eng. 6 (2013) 36–47.
[60] H. Huang, C. Xu, W. Zhang, Removal of nutrients from piggery wastewater using
struvite precipitation and pyrogenation technology, Bioresour. Technol. 102
(2011) 2523–2528.
[61] H. Huang, P. Zhang, Z. Zhang, J. Liu, J. Xiao, F. Gao, Simultaneous removal of
ammonia nitrogen and recovery of phosphate from swine wastewater by struvite
electrochemical precipitation and recycling technology, J. Clean. Prod. 127
(2016) 302–310.
[62] J. Huang, Z. Yu, H. Gao, X. Yan, J. Chang, C. Wang, J. Hu, L. Zhang, Chemical
structures and characteristics of animal manures and composts during
composting and assessment of maturity indices, PLoS One 12 (6) (2017),
e0178110.
[63] W. Huang, Z. Zhao, T. Yuan, Z. Lei, W. Cai, H. Li, Z. Zhang, Effective ammonia
recovery from swine excreta through dry anaerobic digestion followed by
ammonia stripping at high total solids content, Biomass Bioenergy 90 (2016)
139–147.
[64] X. Huang, S. Wang, Z. Shi, L. Fang, C. Yin, Challenges and strategies for biogas
production in the circular agricultural waste utilization model: A case study in
rural China, Energy 241 (2022), 122889.
[65] M. Huchzermeier, W. Tao, Overcoming challenges to struvite recovery from
anaerobically digested dairy manure, Water Environ. Res. 84 (2012) 34–41.
[66] O. Ichihashi, K. Hirooka, Removal and recovery of phosphorus as struvite fro
swine wastewater using microbial fuel cell, Bioresour. Technol. 114 (2012)
303–307.
[67] B. Jha, R.M. Kapoor, V. Vijay, V.K. Vijay, R. Chandra, Biogas: a sustainable and
potential fuel for transport applications, J. Biofuels Bioenergy 1 (2015) 28–33.
[68] X. Jiang, S.G. Sommer, K.V. Christensen, A review of the biogas industry in China,
Energy Policy 39 (2011) 6073–6081.
[69] A. Jiang, T. Zhang, Q.B. Zhao, X. Li, Evaluation of an integrated ammonia
stripping, recovery, and biogas scrubbing system for use with anaerobically
digested dairy manure, Biosyst. Eng. 119 (2014) 117–126.
[70] K. Jung, T. Jeong, H. Kang, K. Ahn, Characteristics of biochar derived from
marine macroalgae and fabrication of granular biochar by entrapment in calcium-
alginate beads for phosphate removal from aqueous solution, J. Bioreso. Technol.
211 (2016) 108–116.
[71] R. Kadam, N.L. Panwar, Recent advancement in biogas enrichment and its
applications, J. Renew. Sustain. Ener. Rev. 73 (2017) 892–903.
[72] W.K. Kim, T. Shim, Y.S. Kim, S. Hyun, C. Ryu, Y.K. Park, Characterization of
cadmium removal from aqueous solution by biochar produced from a giant
Miscanthus at different pyrolytic temperatures, Bioresour. Technol. 138 (2013)
266–270.
[73] T. Kim, Y. Nam, S.J. Lim, Effects of ionizing radiation on struvite crystallization of
livestock wastewater, Radiat. Phys. Chem. 97 (2014) 332–336.
[74] M. Kim, D. Han, D. Kim, Selective release of phosphorus and nitrogen from waste
activated sludge with combined thermal and alkali treatment, Bioresour. Technol.
190 (2015) 522–528.
[75] S. Kizito, S. Wu, W. Kirui, M. Lei, Q. Lu, H. Bah, R. Dong, Evaluation of slow
pyrolyzed wood and rice husks biochar for adsorption of ammonium nitrogen
from piggery manure anaerobic digestate slurry, J. Sci. Total Environ. 505 (2015)
102–112.
[76] S. Kizito, S. Wu, S.M. Wandera, L. Guo, R. Dong, Evaluation of ammonium
adsorption in biochar-fixed beds for treatment of anaerobically digested swine
M. Sajjad et al.
slurry: experimental optimization and modelling, Sci. Total Environ. 563–564
(2016) 1095–1104.
[78] M. Kratzeisen, N. Starcevic, M. Martinov, C. Maurer, J. Müller, Applicability of
biogas digestate as solid fuel, Fuel 89 (2010) 2544–2548, https://doi.org/
10.1016/j.fuel.2010.02.008.
[79] A.A. Kubar, Q. Huang, M. Sajjad, C. Yang, F. Lian, J. Wang, K.A. Kubar, The
recovery of phosphate and ammonium from biogas slurry as value-added
fertilizer by biochar and struvite co-precipitation, Sustainability 13 (2021) 3827.
[80] S. Kumar, L.C. Malav, M.K. Malav, S.A. Khan, Biogas slurry: source of nutrients
for eco-friendly agriculture, Int.J. Extens. Res. 2 (2) (2015) 42–46.
[81] G. Kwon, J. Kang, J.H. Nam, Y.O. Kim, D. Jhang, Recovery of ammonia through
struvite production using anaerobic digestate of piggery wastewater and leachate
of sewage sludge ash, Environ. Technol. 39 (7) (2018) 831–842.
[82] F.J. Larney, L.J. Yanke, J.J. Miller, T.A. McAllister, Fate of coliform bacteria in
composted beef cattle feedlot manure, J. Environ. Qual. 32 (4) (2003)
1508–1515.
[83] C. Ledda, A. Schievano, S. Salati, F. Adani, Nitrogen and water recovery from
animal slurries by a new integrated ultrafiltration, reverse osmosis and cold
stripping process: a case study, J. Water Res. 47 (2013) 6157–6166.
[84] J. Lehmann, J. Gaunt, M. Rondon, Bio-char sequestration in terrestrial
ecosystemsea review, Mitig. Adapt. Strateg. Glob. Chang. 11 (2006) 403–427.
[85] A.M. Lenz, Economic evaluation of the replacement of sugar cane bagasse by
vinasse, as a source of energy in a power plant in the state of Paraná, Brazil,
Renew. Sust. Energ. Rev. 76 (2017) 34–42.
[86] D. Li, Y. Cheng, T. Li, H. Sun, L. Xue, H. Cui, Y. Feng, L. Yang, Q. Chu, Co-
application of biogas slurry and hydrothermal carbonization aqueous phase
substitutes urea as the nitrogen fertilizer and mitigates ammonia volatilization
from paddy soil, Environ. Pollut. 287 (2021), 117340.
[87] S. Li, Y. Zhou, Y. Zhao, W. Li, W. Song, Z. Miao, Avian influenza H9N2 sero
prevalence among pig population and pig farm staff in Shandong, China, J. Virol.
121 (2015) 34–40.
[88] A. Limoli, M. Langonem, G. Andreottola, Ammonia removal from raw manure
digestate by means of a turbulent mixing stripping process, J. Environ. Manag.
176 (2016) 1–10, https://doi.org/10.1016/j.jenvman.2016.03.007.
[89] H. Lin, X. Wu, C. Miller, J. Zhu, L.J. Hadlocon, R. Manuzon, L. Zhao, Pilotscale
field study for ammonia removal from lagoon biogas using an acid wet scrubber,
J. Environ. Sci. Health, Part B 49 (2014) 439–448.
[90] Y. Liu, J. Kwag, J. Kim, C. Ra, Recovery of nitrogen and phosphorus by struvite
crystallization from swine wastewater, Desalination 277 (2011) 364–369.
[91] I.Y. López-Pacheco, A. Silva-Núñez, J.S. García-Perez, D. Carrillo-Nieves,
C. Salinas-Salazar, C. Castillo-Zacarías, S. Afewerki, D. Barceló, H.N. Iqbal,
R. Parra-Saldívar, Phyco-remediation of swine wastewater as a sustainable model
based on circular economy, J. Environ. Manag. 278 (2021), 111534.
[92] P. Loganathan, S. Vigneswaran, J. Kandasamy, N.S. Bolan, Removal and recovery
of phosphate from water using sorption, J. Crit. Rev. Environ. Sci. Technol. 44
(2014) 847–907.
[93] Y. Lou, Zhi-Long Ye, Shaohua Chen, Qunshan Wei, Zhang Jianqiao, Xin Ye,
Influences of dissolved organic matters on tetracyclines transport in the process of
struvite recovery from swine wastewater, Water Res. (2018), https://doi.org/
10.1016/j.watres.2018.02.010.
[94] Z. Luo, D. Wang, J. Yang, H. Huang, G. Su, Nitrogen removal from digested
piggery wastewater using fermented superphosphate within the pretreatment
stage and an MAP fertilizer pot test, J. Clean. Prod. 212 (2019) 372–380.
[95] L. Loyon, Overview of manure treatment in France, J. Waste Manage 61 (2017)
516–520.
[96] M.J. Luján-Facundo, M.I. Iborra-Clar, J.A. Mendoza-Roca, A. Also-Jesús,
Alternatives for the management of pig slurry: phosphorous recovery and biogas
generation, J. Water Process. Eng. 30 (2019), 100473.
[97] Z. Luo, J. Peng, D. Wang, J. Yang, Recovery of phosphate from piggery biogas
slurry by ultrasonication, aeration and addition of MgO desulfurization waste
residue, J. Cean. Prod. 211 (2019) 865–873.
[98] H. Ma, Y. Guo, Y. Qin, Yu-You Li, Nutrient recovery technologies integrated with
energy recovery by waste biomass anaerobic digestion, Bioresour. Technol. 269
(2018) 520–531.
[99] C.Y. Ma, Adsorption characteristics and affecting factors of ammonia nitrogen in
water of Gansu rural area by corn stalk biochar, Environ. Prot. Circular Econ. 38
(12) (2018) 35–39.
[100] A. Magrí, M. Carreras-Sempere, C. Biel, J. Colprim, Recovery of phosphorus
from waste water profiting from biological nitrogen treatment: upstream,
concomitant or downstream precipitation alternatives, Agronomy 10 (7) (2020)
1039, https://doi.org/10.3390/agronomy10071039.
[101] L. Masse, D.I. Massé, Y. Pellerin, J. Dubreuil, Osmotic pressure and substrate
resistance during the concentration of manure nutrients by reverse osmosis
membranes, J. Membr. Sci. 348 (2010) 28–33.
[103] K. Mehmood, S. Chang, S. Yu, L. Wang, P. Li, Z. Li, W. Liu, D. Rosenfeld, J.
H. Seinfeld, Spatial and temporal distributions of air pollutant emissions from
open crop straw and biomass burnings in China from 2002 to 2016, Environ.
Chem. Lett. 16 (2018) 301–309.
[105] D. Mohan, A. Sarwat, Y.S. Ok, C.U. Pittman Jr., Organic and inorganic
contaminants removal from water with biochar, a renewable, low cost and
sustaianable adsorbent-a critical review, Bioresour. Technol. 160 (2014)
191–202.
[106] A. Muhmood, S. Wu, J. Lu, Z. Ajmal, H. Luo, R. Dong, Nutrient recovery from
anaerobically digested chicken slurry via struvite: performance optimization and
interactions with heavy metals and pathogens, Sci. Total Environ. 635 (2018)
1–9.
11
Acta Ecologica Sinica xxx (xxxx) xxx
[108] J. Martinez, P. Dabert, S. Barrington, C. Burton, Livestock waste treatment
systems for environmental quality, food safety, and sustainability, J. Bioresour.
Technol. 100 (2009) 5527–5536.
[109] L. Martínez-Suller, A. Azzellino, G. Provolo, Analysis of livestock slurries from
farms across northern Italy: relationship between indicators and nutrient content,
Biosyst. Eng. 99 (2008) 540–552.
[110] L. Masse, D.I. Masse, Y. Pellerin, J. Dubreuil, Osmotic pressure and substrate
resistance during the concentration of manure nutrients by reverse osmosis
membranes, J. Membr. Sci. 348 (2010) 28–33.
[111] R. Michael, M. Cory, Modeling the Cost of Production of Nitrogen Fertilizer
Produced from Wind Energy, Final Report, University of Minnesota, Minnesota,
2010.
[112] P. Millner, D. Ingram, W. Mulbry, O.A. Arikan, Pathogen reduction in minimally
managed composting of bovine manure, J. Waste Manage. 34 (2014) 1992–1999.
[113] S. Mustafa, M.I. Zaman, S. Khan, Temperature effect on the mechanism of
phosphate anions sorption by β-MnO2, J. Chem. Eng 141 (2008) 51–57.
[114] Z. Milan, E. Sanchez, P. Weiland, C. de Las Pozas, R. Borja, R. Mayari,
N. Rovirosa, Ammonia removal from anaerobically treated piggery manure by ion
exchange in columns packed with homoionic zeolite, J. Chem. Eng. 66 (1997)
65–71.
[115] H.B. Moller, S.G. Sommer, B.K. Ahring, Separation efficiency and particle size
composition in relation to manure type and storage conditions, Bioresour.
Technol. 85 (2002) 189–196.
[116] I.M. Nasir, T.I.M. Ghazi, R. Omar, A. Idris, Anaerobic digestion of cattle manure:
in fluence of inoculum concentration, Int. J. Eng. Technol. 10 (2013) 22–26.
[117] National Bureau of Statistics of the People’’s Republic of China, The China
Statistical Yearbook, 2016, p. 2016. Available online, http://www.stats.gov.cn/t
jsj/tjbz/.
[118] A. Nielsen, D. Trolle, W. Me, L. Luo, B.P. Han, Z. Liu, Assessing ways to combat
eutrophication in a Chinese drinking water reservoir using SWAT, Aust. J. Mar.
Freshwat. Res. 64 (2013) 475.
[119] J. Ning, M. Zhou, X. Pan, C. Li, N. Lv, T. Wang, G. Cai, R. Wang, J. Li, G. Zhu,
Simultaneous biogas and biogas slurry production from co-digestion of pig
manure and corn straw: performance optimization and microbial community
shift, Bioresour. Technol. 282 (2019) 37–47.
[120] J. Nohra, A. Barrington, S. Frigon, S.R. Guiot, In storage psychrophilic anaerobic
digestion of swine slurry, J. Reso Conservat. Recycl. 38 (2003) 23–37.
[121] E.N. Peleka, E.A. Deliyanni, Adsorptive removal of phosphates from aqueous
solutions, Desalination. 245 (2009) 357¬371.
[122] R.H. Perry, Chemical Engineers’ Handbook, McGraw-Hill, 1997 (ISBN 0-07-
049841-5.).
[123] P.A. Perera, Z.Y. Han, Y.X. Chen, W.X. Wu, Recovery of nitrogen and phosphorous
as struvite from swine waste biogas digester effluent, Biomed. Environ. Sci. 20 (5)
(2007) 343–350.
[124] S. Piveteau, S. Picard, P. Dabert, M.L. Daumer, Dissolution of particulate
phosphorus in pig slurry through biological acidification: A critical step for
maximum phosphorus recovery as struvite, Water Res. 124 (2017) 693–701.
[125] A. Pivato, S. Vanin, R. Raga, M.C. Lavagnolo, A. Barausse, A. Rieple, A. Laurent,
R. Cossu, Use of digestate from a decentralised on-farm biogas plant as fertiliser in
soils: an ecotoxicological study for future indicators in risk and life cycle
assessment, Waste Manag. 49 (2016) 378–389.
[126] G. Provolo, F. Perazzolo, G. Mattachini, A. Finzi, E. Naldi, E. Riva, Nitrogen
removal from digested slurries using a simplified ammonia stripping technique,
Waste Manag. 69 (2017) 154–161.
[127] C. Pu, H. Liu, G. Ding, Y. Sun, X. Yu, J. Chen, J. Ren, X. Gong, Impact of direct
application of biogas slurry and residue in fields: in situ analysis of antibiotic
resistance genes from pig manure to fields, J. Hazard. Mater. 344 (2018)
441–449.
[128] A.T. Ren, L.K. Abbott, Y. Chen, Y.C. Xiong, B.S. Mickan, Nutrient recovery from
anaerobic digestion of food waste: impacts of digestate on plant growth and
rhizosphere bacterial community composition and potential function in ryegrass,
Biol. Fertil. Soils (2020), https://doi.org/10.1007/s00374-020-01477-6.
[129] B. Ravindran, M.K. Awasthi, N. Karmegam, S.W. Chang, D.K. Chaudhary,
A. Selvam, D.D. Nguyen, A.R. Milon, G. Munuswamy-Ramanujam, Co-composting
of food waste and swine manure augmenting biochar and salts: nutrient
dynamics, gaseous emissions and microbial activity, Bioresour. Technol. 344
(2022), 126300.
[131] E. Rott, H. Steinmetz, J.W. Metzger, Organophosphonates: A review on
environmental relevance, biodegradability and removal in wastewater treatment
plants, Sci. Total Environ. 615 (2018) 1176–1191.
[132] H. Ruan, Z. Yang, J. Lin, J. Shen, J. Ji, Biogas slurry concentration hybrid
membrane process: pilot-testing and RO membrane cleaning, Desalination. 368
(2015) 171–180.
[134] D.V. Sarkhot, T.A. Ghezzehei, A.A. Berhra, Effectiveness of biochar for sorption of
ammonium and phosphate from dairy effluent, J. Environ. Qual. 42 (2014)
1545–1554.
[135] R. Shea, D. Wall, J.D. Murphy, Modeling a demand driven biogas system for
production of electricity at peak demand and for production of biomethane at
other times, Bioresour. Technol. 216 (2016) 238–249.
[136] L. Shu, P. Schneider, V. Jegatheesan, J. Johnson, An economic evaluation of
phosphorus recovery as struvite from digester supernatant, Bioresour. Technol. 97
(2006) 2211–2216.
[137] J.P. Sheets, L. Yang, X. Ge, Z. Wang, Y. Li, Beyond land application: emerging
technologies for the treatment and reuse of anaerobically digested agricultural
and food waste, Waste Manag. 44 (2015) 94–115.
M. Sajjad et al.
[138] Y.H. Song, G.L. Qiu, P. Yuan, X.Y. Cui, J.F. Peng, P. Zeng, Nutrients removal and
recovery from anaerobically digested swine wastewater by struvite crystallization
without chemical additions, J. Hazard. Mater. 190 (2011) 140–149.
[139] Y. Song, P. Yuan, P. Zheng, J. Peng, F. Yuan, Y. Gao, Nutrients removal and
recovery by crystallization of magnesium ammonium phosphate from synthetic
swine wastewater, Chemosphere 69 (2007) 319–324.
[140] C.G. Sorensen, H.B. Moller, Operational and economic modeling and optimization
of mobile slurry separation, Appl. Eng. Agric. 22 (2006) 185–193.
[141] J.R. Soares, H. Cantarella, M.L.C. Menegale, Ammonia volatilization losses from
surface-applied urea with urease and nitrification inhibitors, J. Soil Biol.
Biochem. 52 (2012) 82–89.
[142] C.A. Takaya, L.A. Fletcher, S. Singh, U.C. Okwuosa, A.B. Ross, Recovery of
phosphate with chemically modified biochars, J. Environ. Chem. Eng. 4 (2016)
1156–1165.
[143] F. Tan, Z. Wang, S. Zhouyang, H. Li, Y. Xie, Y. Wang, Y. Zheng, Q. Li, N and P
removal coupled with carbohydrate production by five microalgae cultures
cultivated in biogas slurry, J. Bioresour. Technol. 221 (2016) 385–393.
[144] G. Tchobanoglous, F.L. Burton, D.H. Stensel, Wastewater Engineering Treatment
and Reuse, 4th edition, McGraw Hill, New York, 2004.
[145] S. Thapa, T.Y. Ha, H. Lee, A.A. Adelodun, Recovery of ammonium ion as struvite
from flue gas scrubbing wastewater, J. Mater. Cycle Waste Manage. 20 (1) (2017)
293–301.
[146] N. Tripathi, C.D. Hills, R.S. Singh, C.J. Atkinson, Biomass waste utilisation in low-
carbon products: harnessing a major potential resource, npj Clim, Atmos. Sci. 2
(1) (2019) 1–10.
[147] S. Uludag-Demirer, G.N. Demirer, S. Chen, Ammonia removal from anaerobically
digested dairy manure by struvite precipitation, Process Biochem. 40 (2005)
3667–3674.
[149] D.R. Vardon, B.K. Sharma, J. Scott, G. Yu, Z. Wang, L.S.Y. Zhang, T.J. Strathmann,
Chemical properties of biocrude oil from the hydrothermal liquefaction of
Spirulina algae, swine manure, and digested anaerobic sludge, Bioresour.
Technol. 102 (2011) 8295–8303, https://doi.org/10.1016/j.
biortech.2011.06.041.
[150] L. van Zwieten, S. Kimber, S. Morris, K.Y. Chan, A. Downie, J. Rust, S. Joseph,
A. Cowie, Effects of biochar from slow pyrolysis of papermill waste on agronomic
performance and soil fertility, Plant Soil 327 (2010) 235–246.
[151] C. Vaneeckhaute, V. Lebuf, E. Michels, E. Belia, P.A. Vanrolleghem, F.M.G. Tack,
E. Meers, Nutrient recovery fromdigestate: systematic technology review and
product classification, Waste Biomass Valorizat. 8 (2017) 21–40, https://doi.org/
10.1007/s12649-016-9642-x.
[152] M.B. Vanotti, P.J. Dube, A.A. Szogi, M.C. Garcia-Gonzalez, Recovery of ammonia
and phosphate minerals from swine wastewater using gas-permeable membranes,
Water Res. 112 (2017) 137–146.
[153] M. Vanotti, M. Garcia-Gonzalez, A. Szögi, J. Harrison, W. Smith, R. Moral,
Removing and recovering nitrogen and phosphorus from animal manure, in:
Animal Manure: Production, Characteristics, Environmental Concerns, and
Management 67, 2020, pp. 275–321.
[154] E. Vega, L. Paredes, E.A. Marks, B. Singla, O. Castaño-Sánchez, C. Casas,
R. Vilaplana, M. Mora, S. Ponsá, L. Llenas, Application of vibrating reverse
osmosis technology for nutrient recovery from pig slurry in a circular economy
model, Membranes 12 (9) (2022) 848.
[155] F. Wang, D. Zhang, X. Shen, W. Liu, W. Yi, Z. Li, S. Liu, Synchronously electricity
generation and degradation of biogas slurry using microbial fuel cell, renew,
Energ. 142 (2019) 158–166.
[156] L. Wang, Y. Li, P. Chen, M. Min, Y. Chen, J. Zhu, R.R. Ruan, Anaerobic digested
dairy manure as a nutrient supplement for cultivation of oil-rich green microalgae
Chlorella sp, Bioresour. Technol. 101 (2010) 2623–2628.
[157] P. Wang, X. Zhang, S.G. Gouda, Q. Yuan, Humidification-dehumidification
process used for the concentration and nutrient recovery of biogas slurry,
J. Clean. Prod. 247 (2020), 119142.
[158] X. Wang, Z. Qiu, S. Lu, W. Ying, Characteristics of organic, nitrogen and
phosphorus species released from ultrasonic treatment of waste activated sludge,
J. Hazard. Mater. 176 (2010) 35–40.
[159] B. Wang, J. Lehmann, K. Hanley, R. Hestrin, A. Endres, Adsorption and desorption
of ammonium by maple wood biochar as a function of oxidation and pH,
Chemosphere 138 (2015) 120–126.
[160] Y. Wang, J. Wang, X. Zhao, X. Song, J. Gong, The inhibition and adaptability of
four wetland plant species to high concentration of ammonia wastewater and
nitrogen removal efficiency in constructed wetlands, Bioresour. Technol. 202
(2016) 198–205.
[161] X. Wang, X. Lu, G. Yang, Y. Feng, G. Ren, Development process and probable
future transformations of rural biogas in China, J. Renew. Sustain. Energy. Rev.
55 (2016) 703–712.
[162] D. Wang, Y. Xin, H. Shi, L. Yu, X. Li, S. Chen, Closing ammonia loop in efficient
biogas production: recycling ammonia pretreatment of wheat straw, Biosyst. Eng.
180 (2019) 182–190.
[163] H. Wang, K. Xiao, J. Yang, Z. Yu, W. Yu, Q. Xu, Q. Wu, S. Liang, J. Hu, H. Hou,
B. Liu, Phosphorus recovery from the liquid phase of anaerobic digestate using
biochar derived from iron− rich sludge: A potential phosphorus fertilizer, Water
Res. 174 (2020), 115629.
[164] A. Whiting, A. Azapagic, Life cycle environmental impacts of generating
electricity and heat from biogas produced by anaerobic digestion, Energy. 70
(2014) 181–193.
[165] J.J. Wu, S.H. Park, S.M. Hengemuehle, M.T. Yokoyama, H.L. Person, S.J. Masten,
The Effect of Storage and Ozonation on the Physical, Chemical, and Biological
Characteristics of Swine Manure Slurries, 1998.
12
Acta Ecologica Sinica xxx (xxxx) xxx
[166] B. Xi, Q. Dang, Y. Wei, X. Li, Y. Zheng, X. Zhao, Biogas slurry as an activator for
the remediation of petroleum contaminated soils through composting mediated
by humic acid, Sci. Total Environ. (2020), https://doi.org/10.1016/j.
scitotenv.2020.139117.
[167] A. Xia, J.D. Murphy, Microalgal cultivation in treating liquid digestate from
biogas systems, Trends Biotechnol. 34 (264) (2016) 275, https://doi.org/
10.1016/j.tibtech.2015.12. 010.
[168] T. Xie, Characterization of Biochar and its Application in Yellow Water
Treatment, Ph. D. Dissertation,, Tsinghua University, 2015.
[169] K. Xu, F. Lin, X. Dou, M. Zheng, W. Tan, C. Wang, Recovery of ammonium and
phosphate from urine as value-added fertilizer using wood waste biochar loaded
with magnesium, J. Clean. Prod. 187 (2018) 205–214.
[170] Y. Xue, Z. Shi, J. Chen, S. Yan, J. Zheng, Promotion of the growth and quality of
Chinese cabbage by application of biogas slurry of water hyacinth, Appl. Mech.
Mater. (2012), https://doi.org/10.4028/www.scientific.net/AMM.195-196.1200.
[171] Y. Yang, P. Zhang, G. Li, Regional differentiation of biogas industrial development
in China, J. Renew. Sustain. Energy Rev. 16 (2012) 6686–6693.
[172] A. Yang, G. Zhang, G. Yang, H. Wang, F. Meng, H. Wang, M. Peng, Denitrification
of aging biogas slurry from livestock farm by photosynthetic bacteria, Bioresour.
Technol. 232 (2017) 408–411.
[173] Z. Ye, S. Chen, M. Lu, J. Shi, L. Lin, S. Wang, Recovering phosphorus as struvite
from the digested swine wastewater with bittern as a magnesium source, Water
Sci. Technol. 64 (2011) 334–340.
[174] K. Yetilmezsoy, E. Kocak, H.M. Akbin, D. Ozcimen, Utilization of struvite
recovered from high-strength ammonium-containing simulated wastewater as
slow-release fertilizer and fire-retardant barrier, Environ. Technol. (2018) 1–18.
[175] Y.D. Yilmazel, G.N. Demirer, Nitrogen and phosphorus recovery from anaerobic
co-digestion residues of poultry manure and maize silage via struvite
precipitation, Waste Manag. Res. 31 (2013) 792–804.
[176] Q. Yin, R. Wang, Z. Zhao, Application of mg-Al-modified biochar for simultaneous
removal of ammonium, nitrate, and phosphate from eutrophic water, J. Clean.
Prod. 176 (2018) 230–240.
[177] K. Yetilmezsoy, E. Kocak, H.M. Akbin, D. Ozcimen, Utilization of struvite
recovered from high-strength ammonium-containing simulated wastewater as
slow-release fertilizer and fire-retardant barrier, Environ. Technol. 22 (2018)
1–18.
[178] A. Zarebska, Nieto Romero, K.V. Christensen, L. Fjerbaek Sotoft, B. Norddahl,
Ammonium fertilizers production from manure: a critical review, J. Crit. Rev.
Environ. Sci. Technol. 45 (2015) 1469–1521.
[179] M. Zacharof, S.J. Mandale, P.M. Williams, R.W. Lovitt, Nanofiltration of treated
digested agricultural wastewater for recovery of carboxylic acids, J. Hazard.
Mater. 112 (2016) 4749–4761.
[180] L. Zhang, P. Zhou, Y.C. Chen, Q. Cao, X.F. Liu, D. Li, The production of single cell
protein from biogas slurry with high ammonia-nitrogen content by screened
Nectaromyces rattus, Poult. Sci. 100 (9) (2021), 101334.
[181] X. Zhang, C. Liu, W. Liao, S. Wang, W. Zhang, J. Xie, Z. Gao, Separation efficiency
of different solid-liquid separation technologies for slurry and gas emissions of
liquid and solid fractions: A meta-analysis, J. Environ. Manag. 310 (2022),
114777.
[182] W. Zeng, D. Wang, Z. Luo, J. Yang, Z. Wu, Phosphorus recovery from pig farm
biogas slurry by the catalytic ozonation process with MgO as the catalyst and
magnesium source, J. Clean. Prod. 269 (2020), 122133.
[183] L. Zhao, C. Wang, M.M. Tian, X.Y. Li, Characteristics of anaerobic fermentation of
mixed livestock manure and straw, China Biogas. 33 (2015) 32–37.
[184] Y. Zhao, S. Sun, C. Hu, H. Zhang, J. Xu, L. Ping, Performance of three microalgal
strains in biogas slurry purification and biogas upgrade in response to various
mixed light emitting diode light wavelengths, Bioresour. Technol. 187 (2015)
338–345.
[185] S. Zhao, K. Yan, Z. Wang, Y. Gao, K. Li, J. Peng, Does anaerobic digestion improve
environmental and economic benefits of sludge incineration in China? Insight
from life-cycle perspective, Resour. Conserv. Recycl. 188 (2023), 106688.
[186] G. Zhen, X. Lu, H. Kato, Y. Zhao, Y.Y. Li, Overview of pretreatment strategies for
enhancing sewage sludge disintegration and subsequent anaerobic digestion:
current advances, full-scale application and future perspectives, Renew. Sust.
Energ. Rev. 69 (2017) 559–577.
[187] K. Zhu, H. Fu, J. Zhang, X. Lv, J. Tang, X. Xu, Studies on removal of NH+ 4 -N from
aqueous solution by using the activated carbons derived from rice husk, Biomass
Bioenergy 43 (2012) 2–18.
[188] P.J. Dube, M.B. Vanotti, A.A. Szogi, M.C. García-González, Enhancing recovery of
ammonia from swine manure anaerobic digester effluent using gas-permeable
membrane technology, Waste Manag. 49 (2016) 372–377.
[189] H.M. El-Mashad, W.K. Van Loon, G. Zeeman, G.P. Bot, Rheological properties of
dairy cattle manure, Bioresour. Technol. 96 (5) (2005) 531–535.
[190] W.B. Han, Y.Z. Zhao, H. Chen, Study on biogas production of joint anaerobic
digestion with excess sludge and kitchen waste, Procedia Environ. Sci. 35 (2016)
756–762.
[191] M. Sobhi, J. Guo, M.S. Gaballah, B. Li, J. Zheng, X. Cui, H. Sun, R. Dong, Selecting
the optimal nutrients recovery application for a biogas slurry based on its
characteristics and the local environmental conditions: A critical review, Sci.
Total Environ. 814 (2022) 152700.
[192] Y. Liu, S. Kumar, J.H. Kwag, C. Ra, Magnesium ammonium phosphate formation,
recovery and its application as valuable resources: a review, J. Chem. Technol.
Biotechnol. 88 (2) (2013) 181–189.
[193] K. Yetilmezsoy, Z. Sapci-Zengin, Recovery of ammonium nitrogen from the
effluent of UASB treating poultry manure wastewater by MAP precipitation as a
slow release fertilizer, J. Hazard. Mater. 166 (1) (2009) 260–269.
M. Sajjad et al.
[194] R.T. Burns, L.B. Moody, Phosphorus recovery from animal manures using
optimized struvite precipitation, in: Proceedings of Coagulants and Flocculants:
Global market and technical opportunities for water treatment chemicals, 2002,
pp. 1–4.
[195] C. Mao, Y. Wang, X. Wang, G. Ren, L. Yuan, Y. Feng, Correlations between
microbial community and C: N: P stoichiometry during the anaerobic digestion
process, Energy 174 (2019) 687–695.
[196] J.P. Graham, K.E. Nachman, Managing waste from confined animal feeding
operations in the United States: the need for sanitary reform, J. Water Health 8 (4)
(2010) 646–670.
[197] C. Junjie, Z. Hongguang, Study on two-stage air-recirculation ammonia stripping
process for membrane concentrate in livestock and poultry breeding, in: E3S Web
of Conferences Vol. 194, EDP Sciences, 2020, p. 02015.
[198] Z. Yang, Y. Liu, J. Zhang, K. Mao, M. Kurbonova, G. Liu, R. Zhang, W. Wang,
Improvement of biofuel recovery from food waste by integration of anaerobic
digestion, digestate pyrolysis and syngas biomethanation under mesophilic and
thermophilic conditions, J. Cleaner Prod. 256 (2020) 120594.
[199] M. Nakamura, F. Oritate, Y. Yuyama, M. Yamaoka, N.P. Dan, D.V.B. Hanh,
Ammonia volatilization from Vietnamese acid sulfate paddy soil following
application of digested slurry from biogas digester, Paddy Water Environ. 16
(2018) 193–198.
[200] V.H. Varel, J.A. Nienaber, H.C. Freetly, Conservation of nitrogen in cattle feedlot
waste with urease inhibitors, J. Anim. Sci. 77 (5) (1999) 1162–1168.
[201] M. Ganesapillai, P. Simha, S.S. Beknalkar, D.M.R. Sekhar, Low-grade rock
phosphate enriched human urine as novel fertilizer for sustaining and improving
agricultural productivity of Cicer arietinum, Sustain. Prod. Consum. 6 (2016)
62–66.
13
Acta Ecologica Sinica xxx (xxxx) xxx
[202] A. Beckinghausen, M. Odlare, E. Thorin, S. Schwede, From removal to recovery:
An evaluation of nitrogen recovery techniques from wastewater, Appl. Energy
263 (2020) 114616.
[203] A. Folino, D.A. Zema, P.S. Calabrò, Organic matter removal and ammonia
recovery by optimised treatments of swine wastewater, J. Environ. Manag. 270
(2020) 110692.
[204] M. Shi, Q. He, L. Feng, L. Wu, S. Yan, Techno-economic evaluation of ammonia
recovery from biogas slurry by vacuum membrane distillation without pH
adjustment, J. Cleaner Prod. 265 (2020) 121806.
[205] R.R. Karri, J.N. Sahu, V. Chimmiri, Critical review of abatement of ammonia from
wastewater, J. Mol. Liquids 261 (2018) 21–31.
[206] J. Qiu, H. Hou, S. Liang, L. Yang, Q. Gan, S. Tao, W. Yu, R. Lv, L. Ding, K. Xiao,
J. Hu, Hierarchically porous biochar preparation and simultaneous nutrient
recovery from sewage sludge via three steps of alkali-activated pyrolysis, water
leaching and acid leaching, Resour. Conserv. Recycl. 176 (2022) 105953.
[207] X. Cheng, X. Huang, X. Wang, D. Sun, Influence of calcination on the adsorptive
removal of phosphate by Zn–Al layered double hydroxides from excess sludge
liquor, J. Hazard. Mater. 177 (1–3) (2010) 516–523.
[208] D.V. Sarkhot, T.A. Ghezzehei, A.A. Berhe, Effectiveness of biochar for sorption of
ammonium and phosphate from dairy effluent, J. Environ. Quality 42 (5) (2013)
1545–1554.
[209] S. Mandal, E. Donner, S. Vasileiadis, W. Skinner, E. Smith, E. Lombi, The effect of
biochar feedstock, pyrolysis temperature, and application rate on the reduction of
ammonia volatilisation from biochar-amended soil, Sci. Total Environ. 627
(2018) 942–950.