International Master of Science in Environmental Technology and Engineering
Master’s dissertation submitted in partial fulfilment of the requirements for the joint degree of
EU Erasmus+ Master course organized by
University of Chemistry and Technology, Prague, the Czech Republic
IHE Delft Institute for Water Education, Delft, the Netherlands
Ghent University, Ghent, Belgium
Academic year 2018-2020
Assessment of sustainable technologies for pig manure
valorization – a meta-analysis Ghent University, Ghent, Belgium
Vaibhav Shrivastava Thesis ID identifier: ES-IMETE.20-28
Promotors: Prof. Filip Tack, Prof. Erik Meers
Tutor: Caleb Elijah Egene
International Master of Science in Environmental Technology and Engineering
Master’s dissertation submitted in partial fulfilment of the requirements for the joint degree of
EU Erasmus+ Master course organized by
University of Chemistry and Technology, Prague, the Czech Republic
IHE Delft Institute for Water Education, Delft, the Netherlands
Ghent University, Ghent, Belgium
Academic year 2018-2020
Assessment of sustainable technologies for pig manure
valorization – a meta-analysis Ghent University, Ghent, Belgium
Vaibhav Shrivastava Thesis ID identifier: ES-IMETE.20-28
Promotors: Prof. Filip Tack, Prof. Erik Meers
Tutor: Caleb Elijah Egene
i
Copyright Statement
This is an unpublished M.Sc. dissertation and is not prepared for further distribution. The
author and the promoter give the permission to use this Master dissertation for consultation and
to copy parts of it for personal use. Every other use is subject to the copyright laws, more
specifically the source must be extensively specified when using results from this Master
dissertation.
The Promoter 1: The Author:
Prof. Filip Tack Vaibhav Shrivastava
The Promoter 2:
Prof. Erik Meers
ii
Preamble
This preamble concerns the impact of Coronavirus COVID-19 (outbreak in 2020) on the
master's dissertation work conducted on the initial topic of “Use of digestate and charred
digestate (biochar) to increase stable organic carbon in soils”.
The intended focus of the study was to employ the use of various valorization mechanisms for
the recovery of phosphorous from raw pig manure. Initially, for the month of February and
March 2020, the experiments with pig manure were conducted at the Faculty of Bioscience
Engineering (ECOCHEM lab), Ghent University. However, after the ban on 16th March 2020
on all lab activities at UGent, no further experiments could be carried out. Due to this
inaccessibility, the application and analysis of prepared samples in pot experiments could not
be continued, and not enough data was obtained from the previous experiments for proper
interpretation.
To deal with the following crisis, a reorientation towards a detailed critical literature-based
statistical study (meta-analysis) was proposed for the final thesis writing. This further led to
the modification of the master’s dissertation title to “Assessment of sustainable technologies
for pig manure valorization – a meta-analysis”. The current thesis focuses majorly on the trend
of nutrients recovery (particularly focusing on N and P) via use of various valorization
mechanisms over the span of last two decades.
This preamble was drawn up after consultation between the student and the supervisor and is
approved by both the parties.
The Promoters: The Author:
Prof. Filip Tack Vaibhav Shrivastava
Prof. Erik Meers
iii
Abstract (English)
During the last decades, the increasing concern about the environmental sustainability,
especially in terms of natural resources consumption and intensive agro-livestock practices,
became widely recognized. In this context, the production of fertilizers from waste resources
(manure) plays a crucial role. Moreover, the livestock sector produces an important source of
nitrogen and untapped nutrients whose direct use is restricted due to potentially negative
environmental consequences. Accordingly, there is an increasing interest in translating a
quantitative waste problem into an important recovery and reuse opportunity. The goal of this
study was to evaluate the valorization mechanisms related to different scenarios focused on pig
manure treatment: (a) ammonia stripping (b) pyrolysis and hydrothermal carbonization (c)
crystallization (d) solid-liquid separation and (e) biological processes. The following categories
were considered for assessment in accordance with literature: yearly distribution, country wise
distribution, recovered nutrients, technological feasibility, and economics. The reported factors
such as nutrient concentration in initial and final product were analyzed by the software Review
Manager 5.4 to identify the effectiveness of different valorization pathways in comparison to
initial products. Pyrolysis and crystallization have come forward as the most efficient options
for N and P recovery, respectively. Furthermore, an economic analysis was performed. The
price trend for fertilizers over the period of last 20 years has shown an overall growth trend,
attaining an all time high in the year 2009. Additionally, comparison between the cost-to-
benefit ratio of different valorization mechanism evaluated crystallization and pyrolysis with
the lowest payback periods and a good profit margin over initial products.
iv
Abstract (Dutch)
In de afgelopen decennia werd de toenemende bezorgdheid over de ecologische duurzaamheid,
vooral in termen van het gebruik van natuurlijke hulpbronnen en intensieve
landbouwhuisdieren, algemeen erkend. Hierbij speelt de productie van meststoffen uit
afvalbronnen (mest) een cruciale rol. Bovendien produceert de veehouderij een belangrijke
bron van stikstof en onaangeboorde nutriënten waarvan het directe gebruik beperkt wordt
vanwege mogelijk negatieve gevolgen voor het milieu. Dienovereenkomstig is er een
toenemende interesse om een kwantitatief afvalprobleem te vertalen naar een belangrijke kans
op terugwinning en hergebruik. Het doel van deze studie was om de valorisatiemechanismen
te evalueren die verband houden met verschillende scenario's gericht op de behandeling van
varkensmest: (a) strippen van ammoniak (b) pyrolyse en hydrothermische carbonisatie (c)
kristallisatie (d) vaste stof-vloeistofscheiding en (e) biologische processen . De volgende
categorieën kwamen in aanmerking voor beoordeling in overeenstemming met de literatuur:
jaarlijkse distributie, verdeling per land, teruggewonnen nutriënten, technologische
haalbaarheid en economie. De gerapporteerde factoren zoals nutriëntenconcentratie in begin-
en eindproduct werden geanalyseerd door de software Review Manager 5.4 om de effectiviteit
van verschillende valorisatiepaden in vergelijking met de oorspronkelijke producten te
identificeren. Pyrolyse en kristallisatie zijn naar voren gekomen als de meest efficiënte opties
voor respectievelijk N- en P-terugwinning. Verder is er een economische analyse uitgevoerd.
De prijsontwikkeling voor meststoffen over de periode van de afgelopen 20 jaar heeft een
algemene groeitrend laten zien, en bereikte een recordhoogte in het jaar 2009. Bovendien
evalueerde een vergelijking tussen de kosten-batenverhouding van verschillende
valorisatiemechanismen kristallisatie en pyrolyse met de laagste terugverdientijden en een
goede winstmarge ten opzichte van initiële producten.
v
Acknowledgement
I would like to express my appreciation and gratitude for the ones who have been supporting
and involving for the completion of this master thesis.
First and foremost, my praise is to ALLAH, the Almighty, the most Merciful and Beneficent,
for giving me opportunity, determination, and strength to do my research. His continuous grace
and mercy were with me throughout my life and ever more during the tenure of my research.
My sincere gratitude goes my promoter, Prof. Filip Tack and Prof. Erik Meers of the Laboratory
of Applied Analytical and Physical Chemistry, for allowing me to embark on this project. His
valuable guidance, advice and feedback during the course of this thesis helped make this work
a success.
I would like to thank my tutor, Caleb Elijah Egene, for his continuous assistance ranging from
setting up laboratory experiments, practical advice, editing of the thesis and full cooperation
during the entire period of this study. Even off-field, Caleb helped me by going off his way
many times, hence making the word “tutor” whole in every aspect. During my journey with
him, I not only earned a “Guru” but also a true friendship, which will hopefully last for our
lifetimes.
I must also thank European Union for providing me with opportunity to take part in Erasmus
Mundus and made it possible for me to study at Ghent University. Furthermore, I would also
like to thank all the staff members at UCT Prague, IHE Delft and Ghent University for
organizing an excellent IMETE programme.
Finally, this document will go incomplete without thanking my parents for their prayers,
support and encouragement that have helped me get to where I am today. And how can I forget
to thank the most priceless person, my friend, Izba Ali, who has stick to me through all thick
and thin and has been always been on my side. This is a debt that I can’t pay back in their entire
lifetime (but perhaps small installments in the form of cakes, chocolates and sweets can appease
a bit). I dedicate this work to all of them.
Vaibhav Shrivastava
vi
Acronyms and abbreviations
CI: Confidence Interval
df: Degrees of Freedom
DOC: Dissolved Organic Carbon
DOI: Digital Object Identifier
EEA: European Environmental Agency
EPA: Environment Protection Agency
EU: European Union
FAO: Food and Agriculture organization
of United Nations
HM: Heavy metals
HTC: Hydrothermal Carbonization
JSTOR: Journal storage
LPELC: Livestock and Poultry
Environmental Learning Community
MD: Mean Difference
MPCA: Minnesota Pollution Control
Agency
MT: Metric Tons
NPK: Nitrogen-phosphorus-potassium
NVZ: Nitrate Vulnerable Zones
OC: Organic Carbon
OM: Organic matter
p: Probability
RE: Recovery Efficiency
RevMan: Review Manager
SD: Standard Deviation
SP: Struvite precipitation
TKN: Total Kjeldahl nitrogen
UNDESA: United Nations Department of
Economic and Social Affairs
USGS: US Geological Survey
VMD: Vacuum Membrane Distillation
vii
Table of Contents:
Copyright Statement ................................................................................................................... i
Preamble .................................................................................................................................... ii
Abstract (English) .................................................................................................................... iii
Abstract (Dutch)........................................................................................................................ iv
Acknowledgement ..................................................................................................................... v
Acronyms and Abbreviations ................................................................................................... vi
List of figures ............................................................................................................................ ix
List of tables ............................................................................................................................... x
Table of Contents: ........................................................................................................................... vii
Introduction .................................................................................................................................... 1
Literature review ............................................................................................................................. 4
2.1 Manure as a fertilizer .............................................................................................................. 4
2.2 Relevance of N and its availability in the ecosystem .............................................................. 4
2.3 Relevance of P and its availability in the ecosystem............................................................... 6
2.4 Concerned legislation.............................................................................................................. 7
2.5 Use of manure for agriculture ................................................................................................ 9
2.6 Heavy metals ......................................................................................................................... 10
2.7 Factors affecting composition of pig manure ....................................................................... 11
2.8 Valorization technologies...................................................................................................... 14
2.8.1 Hydrothermal carbonization ......................................................................................... 14
2.8.2 Ammonia stripping ........................................................................................................ 14
2.8.3 Crystallization ................................................................................................................ 15
2.8.4 Pyrolysis ........................................................................................................................ 15
2.8.5 Mechanical Solid-liquid separation ............................................................................... 17
2.8.6 Biological Treatment ..................................................................................................... 17
Methodology ................................................................................................................................. 21
3.1 Data and literature sources .................................................................................................. 21
3.2 Study selection ...................................................................................................................... 21
3.3 Data extraction ..................................................................................................................... 22
3.4 Data analysis ......................................................................................................................... 22
3.5 Strategy for data assessment ................................................................................................ 22
3.5.1 Qualitative assessment ................................................................................................. 22
viii
3.5.2 Quantitative assessment ............................................................................................... 23
3.5.3 Heterogeneity assessment ............................................................................................ 23
3.6 Risk-of-Bias assessment ........................................................................................................ 24
Results and discussion .................................................................................................................. 25
4.1 Overview of the data collection ............................................................................................ 25
4.2 Data distribution ................................................................................................................... 27
4.2.1 Year wise distribution of studies ................................................................................... 27
4.2.2 Country wise distribution of studies ............................................................................. 28
4.2.3 Nutrient wise distribution of studies ............................................................................ 29
4.3 Risk-of-Bias ............................................................................................................................ 32
4.4 Quantitative analysis of studies ............................................................................................ 32
4.4.1 Ammonia Stripping ....................................................................................................... 32
4.4.2 Pyrolysis ........................................................................................................................ 33
4.4.3 Crystallization ................................................................................................................ 34
4.4.4 Hydrothermal Carbonization ........................................................................................ 35
4.4.5 Separation ..................................................................................................................... 36
4.4.6 Biological ....................................................................................................................... 37
4.5 Economics ............................................................................................................................. 39
4.5.1 Economic evaluation of fertilizers ................................................................................. 39
4.5.2 Economic assessment of available technologies .......................................................... 41
4.6 Overall techno-economic comparison .................................................................................. 43
Conclusions ................................................................................................................................... 44
References .................................................................................................................................... 45
Annex 1 ......................................................................................................................................... 60
Annex 2 ......................................................................................................................................... 64
ix
List of figures
Figure 1. Cycle for biogas generation and utilization (Shrivastava et al, 2019). ..................... 19
Figure 2. Data screening and selection steps for systematic review ........................................ 26
Figure 3. Distribution of concerned dataset across last two decades ....................................... 27
Figure 4. Country wise distribution of studies ......................................................................... 29
Figure 5. Comparison of RE various valorization technologies for nitrogen (x = mean, --- =
median and dot = datapoints) ................................................................................................... 30
Figure 6. Comparison of RE various valorization technologies for phosphorous (x = mean, ---
= median and dot = datapoints) ................................................................................................ 31
Figure 7. Risk-of-bias assessment for the dataset .................................................................... 32
Figure 8. Trend of valorization against initial product for nitrogen recovery across studies
(values in dg/L) ........................................................................................................................ 33
Figure 9. Trend of valorization against initial product for phosphorous recovery across
pyrolysis (values in mg/g) ........................................................................................................ 34
Figure 10. Trend of valorization against initial product for nitrogen recovery across
crystallization (values in mg/kg) .............................................................................................. 34
Figure 11. Trend of valorization against initial product for phosphorous recovery across
crystallization (values in mg/g). ............................................................................................... 35
Figure 12. Trend of valorization against initial product for nitrogen recovery across
hydrothermal carbonization (values in g/kg) ........................................................................... 36
Figure 13. Trend of valorization against initial product for phosphorous recovery across
hydrothermal carbonization (values in g/kg) ........................................................................... 36
Figure 14. Trend of valorization against initial product for nitrogen recovery across
separation processes (values in mg/dL) ................................................................................... 37
Figure 15. Trend of valorization against initial product for phosphorous recovery across
separation processes (values in mg/L) ..................................................................................... 37
Figure 16. Trend of valorization against initial product for nitrogen recovery across biological
processes (values in mg/L) ....................................................................................................... 38
Figure 17. Trend of valorization against initial product for phosphorous recovery across
biological processes (values in mg/L)...................................................................................... 38
Figure 18. Trend of market price (global) for fertilizers over the last 20 years (The World
Bank, 2020). ............................................................................................................................. 40
x
List of tables
Table 1. Phosphorus (total) application standards in Flanders region (Amery and Schoumans,
2014) .......................................................................................................................................... 8
Table 2. Nutrient application rate requirements for manure (MPCA, 2019) ............................. 9
Table 3. Manure production (liquid content) and nutrient content for major livestock species
(Shrivastava et al, 2019). ......................................................................................................... 10
Table 4. Quantity of nutrient elements excreted in manure of various animals during
reproduction cycles* ................................................................................................................ 13
Table 5. Treatment processes diversification in the selected dataset....................................... 27
Table 6. Economic comparison for various valorization technologies .................................... 42
1
Introduction
The European Union is the world's 2nd largest meat producer, behind China, with 63.85 million
tons contributing to about 14% of the world's production (Ritchie and Roser, 2019). The United
states comes 3rd in the list, with a meat production of 46.66 million tons. In January 2020, the
swine herd population in the world was estimated at 677.6 million animals (Shahbandeh, 2020).
This activity resulted in generation of 178 million m3 per year of swine manure in Europe alone,
a volume that would fill up to 71,000 Olympic-sized swimming pools (European commission,
2018). This has shifted focus of environmental enthusiasts on manure related problems such as
emissions of greenhouse gases from livestock production, runoff, over fertilization of soils and
leaching. It is estimated that pig supply chains generate 0.7 gigatons of CO2 equivalent per
year, representing 9% of total emissions from the livestock sector of world (MacLeod et al,
2013). Furthermore, emissions from cattle production contributes to 41% of total emissions
from livestock sector.
Pig manure is rich in organic matter and nutrients including nitrogen, phosphorus, and
potassium. However, use of pig manure for agriculture is only possible when it is a balance
with the number of livestock. The EU Nitrate directive recommends maximum dosage quantity
as 170 kg of nitrogen per ha per annum (Council Directive 91/676/EEC). When animal
husbandry is intensive, production of pigs with enhanced diets will release large quantities of
nitrogen and phosphorus and lead to accumulation of copper and zinc, fed to pigs, in the soil.
Such imbalances can lead to severe environmental problems affecting soil quality (drainage,
plants toxicity, pathogenic activity), water (nitrate pollution of the groundwater or
eutrophication of the surface water) and air (bad odours, greenhouse gas emissions) (Camargo-
Valero et al, 2015). On the other hand, production of conventional synthetic fertilizers has
tremendous environmental impacts. Alone, fertilizer industry accounts for 1.2% of the overall
energy consumption of the planet. Ammonium is the basic component for nitrogen fertilizer
production, but the process of its production is very energy intensive (36.6 GJ/t NH3) and
produces high CO2 emissions (1,966.8 kg CO2 eq/kg) and nitrogen oxides (European
commission, 2018).
For dealing with the problems of manure management and fertilizer production sustainability,
different valorization approaches of manure have been proposed. More rudimentary
approaches involve designing storage such that the release of greenhouse gases is significantly
reduced. However, more focus has recently been given to the application of different
2
technologies to valorize pig manure as organic soil amendments or mineral fertilizer
substitutes.
Among the alternatives for pig manure treatment, aerobic composting is a relatively simple
operation that yields a valorized product with high nutrient content (Chen et al, 2010). Another
useful method to treat pig manure is biogas production through anaerobic digestion. The
process of anaerobic digestion can also yield renewable energy (clean and cheap methane), soil
conditioner and liquid fertilizer. Moreover, the biogas production could be enhanced by the
anaerobic co-digestion technique compared to the single-substrate digestion (Wang et al,
2012). However, the anaerobic digestion is a complex process and microbial reactions can be
inhibited by many factors such as sunlight-dark conditions. Recycling of pig-manure can also
be achieved by applying it as a fertilizer for pond carp production (Zoccarato et al, 1995).
Furthermore, it can be incorporated into algal biomass production, via aerobic fermentation,
which can be used for animal feeding (Martin, De la Noüe and Picard, 1985). Swine manure
derived biochar through slow pyrolysis has the potential to be used as an excellent soil
amendment (rich in NPK) as well as a cheap adsorbent to immobilize contaminants (Tsai et al,
2012; Zhang et al, 2013).
The goal of this study is to quantitatively assess and compare the techno-economic
sustainability of existing valorization technologies for pig manure by pooling the results of
several previously conducted studies.
The specific objectives of this study are to:
• Summarize the state of the art of options for the down processing and valorization of
pig manure.
• Evaluate and compare the various transformed products based on the recovery
efficiency and mean difference obtained for various nutrients.
• Quantitatively compare the replacement value of products derived from pig manure for
mineral N and P fertilizers based on nutrient availability and nutrient use efficiency.
This work is organized under 5 chapters. Introduction (chapter 1) provides a brief summary
and statistical data about the background information on manure, problem statement and
objectives of the thesis. Literature Review (chapter 2) consists with an overview of the
environmental relevance and significance of nutrients (nitrogen and phosphorus) and
importance of manure in agricultural application and nutrient valorization. It also describes
various legislations and other concerns regarding agricultural application of manure
3
Methodology (chapter 3) describes the procedure of data extraction from various online
databases as well as the inclusion/exclusion criteria. Furthermore, procedure of data
interpretation through RevMan and other methods are also explained. Results and Discussion
(chapter 4) provides a summary of the research trends on the basis of year wise and country
wise studies and explains the significance of the results obtained from the statistical analysis
(through RevMan and recovery efficiency) of the collected dataset. A brief discussion on
economics of various technologies is also performed. Conclusion (chapter 5) conveys the
conclusion of this study discussing best valorization technology for different nutrients.
4
Literature review
2.1 Manure as a fertilizer
Manure is in many cases the main fertilizer source for farmers, which has long been closing
the nutrient cycling. However, the overall sum of nutrients in regions with intensive livestock
farming systems often exceed the nutrient requirements of the crops. In these areas, the excess
nutrients such as nitrogen (N) and phosphorus (P) results in their high concentrations in soil,
surface waters, and atmosphere (Velthof et al, 2014). The demands for minerals, on the other
hand, are high, and many minerals, such as phosphorus (P) and potassium (K), now mined, are
becoming increasingly scarce. Therefore, nutrient removal and recovery from manure has
recently received a lot of attention in regions with intensive livestock farming such as The
Netherlands and Belgium (esp. Flanders) (Schoumans et al, 2015).
In order to boost water quality and to compel the member states to set up an action plan, the
European Nitrates Directive was been implemented in 1991 (EEA, 2020). Manure production
was developed in these vulnerable areas since the 1990's to extract excess nitrogen or export
nutrients to less nutrient-dense areas (Velthof et al, 2014). Now, with the high costs of fossil-
based fertilizer and lower stocks of phosphorus and potassium, the focus of the farmers and
fertilizers producers is towards shifting from the manure processing to more advanced
techniques for nutrient recovery.
In the recent times, the extraction of nutrients from pig slurry has gained a strong interest
among researchers. However, handling and application of the valorized product always remain
a question of interest. Nowadays, the most effective method of handling pig slurry is to
biologically treat the thin fractions and dry them or composting the dried solid fraction and
export them to nutrient deficient areas (Schoumans et al, 2015). The composting and pelleting
processes are well known and relatively easy to execute. However, in contrast to raw manure,
the costs of transport are not much lower and much compost in crop farms is denied because it
has a low N/P ratio that does not meet the needs of the majority of arable crops. Therefore, it
is more interesting to valorize the components of manure into valuable products (Schoumans
et al, 2015).
2.2 Relevance of N and its availability in the ecosystem
Nitrogen is an abundant element on Earth; it makes up 78.1% of Earth's atmosphere and is an
essential nutrient for all forms of life. Most of this Nitrogen is available in the form of
unreactive nitrogen (N2) that most living organisms cannot use. However, part of it, which is
5
fixed by natural or anthropogenic processes [N, which includes nitrogen oxides (NOX), reduced
nitrogen (NHX), nitrous oxide (N2O), nitric acid (HNO3), and other organic and inorganic
forms] is available for use by living organisms (Stevens, 2019). The quantity of N released into
the aquatic environments from human activities has increased over the past century to such a
degree that it is now beyond natural fixation, resulting in a more than doubled global cycling
of nitrogen (anthropogenic N production, 210 Tg N per year; natural N production, 203 Tg N
per year) (Stevens, 2019). In many parts of the world, due to this increase in nitrogen fixation,
air, water and soil pollution has become an important aspect of concern.
Nitrogen use is, however, substantially disproportionate worldwide. In countries outside the
Organization for Economic Co-operation and Development (OECD) and major emerging
economies, the amount of nitrogen taken up by the crops remains low. Not only are there
insufficient fertilizers, the available nutrients are also inefficient in usage. Sub-Saharan Africa
provides an appropriate example. In 2012, nutrient-poor soils yielded an average of 1 metric
ton (MT) ha−1 for grain crops, with fertilizer use averaging 9 kg ha−1 of the cultivated soil
(Stevens, 2019). On the other hand, Asia, where there are major emerging economies, has
achieved crop yields exceeding 4.5 MT ha−1 with fertilizer applications of 96 kg ha–1. Lack of
nitrogen obviously contributes to significant problems in fulfilling people's nutritional
requirements. These problems are just as difficult to address as the problems that nitrogen
pollution causes in other parts of the world.
For the preparation of chemical fertilizers, the Haber Process, also called the Haber-Bosch
Process is employed. It is a complex chemical procedure which uses nitrogen from the air and
combines it with hydrogen to produce ammonia under high pressures and temperatures. Today,
this ammonia is the basis of the widely used synthetic nitrogen fertilizer worldwide (Gellings
and Parmenter, 2016). Haber processes produce approximately 500 million tons of fertilizer
per year (453 billion kilograms). This fertilizer helps feed about 40% of the population of the
planet. Even after so many advantages, on the curse side, we have several socio-environmental
issues with the production of nitrogen fertilizers using this technology (Gellings and Parmenter,
2016). First, this is a high energy process and takes up about 1 – 2% of the world’s energy
supply every year (Harford, 2017). According to 2017 statistics, this number corresponds to
around 500 TWh. Furthermore, fertilizers seep into rivers which causes algae blooms. In turn,
bacteria feed on the dead algae using up oxygen in the water, as a result killing aquatic animals.
This further contributes in causing ocean dead zones.
6
2.3 Relevance of P and its availability in the ecosystem
Phosphorus is the 11th most common element found on Earth with a concentration in the crust
of about 1 g/kg and it is safe to say that is fundamental to all biotic species (Tiessen 2008). It
is important for creating DNA, cell membranes, and also for the creation of human bones and
teeth. This is important for food production because it is one of three nutrients used in
commercial fertilizer (nitrogen, potassium, and phosphorus). It is not present free in nature but
is widely dispersed, generally as phosphates, in many minerals. Inorganic phosphate rock
partially consisting of apatite is the source of most of the world’s phosphorus up to date
(Tiessen 2008).
In agriculture and food production, around 90% of the world's mined phosphate rock is used,
more as fertilizer, less as animal feed and food additives (FAO 2020). Moreover, the market
polarity makes this resource more inaccessible due to political or geographical reason.
According to the US Geological Survey (USGS), about 50% of the global reserves of
phosphorus are with the Arab nations. Major apatite deposits are also found in China, Russia,
Morocco and USA (in Florida, Idaho, Tennessee and Utah). Moreover, the phosphorus that is
available in the nature cannot be extracted up to the demands of the modern world due to
physical, economic, energy or legal constraints (USGS 2020). In addition to this, majority of
this extracted phosphorus is lost in the processing. About 30 – 40% is lost during mining and
processing and another 50% is wasted in the complexity of the food chain (Renee, 2013). Just
20% of phosphorus in phosphate rock enters global food consumption. Much of the excess
phosphorus from farm or fertilizer runoff or from phosphates in detergent and soda washed
into drains reaches our rivers, lakes and oceans and results in eutrophication (Renee, 2013). It
is a severe form of water contamination in which algae blooms produce, then die, consume
oxygen, and create a "dead zone" in which nothing can survive. There are over 400 dead coastal
areas at river mouths that are rising at a rate of 10% per decade (Renee, 2013).
The current extractable phosphorus reserves, according to the reliable estimates show the
capability of phosphate rock resources to last an additional 300 – 400 years. With a world
population predicted to hit 9 billion by 2050 and needing 70% more food than we currently
generate, and a rising global middle class that consumes more meat and milk, phosphorus is
crucial to global food security (Renee, 2013). Yet there are no international bodies or laws that
control capital from global phosphorus. In these crucial times, the experts are looking at the
other sources of phosphorus which can be used to meet the global P demand in the future.
7
Animals and people excrete nearly all of the phosphorus they consume in food. For ages,
animal manure has been applied to soil for improving the nutrient composition of soil, aiding
crop production. Even today, in some parts of the world (e.g. Vietnam), manure is directly
applied to the soil as a fertilizer (Shrivastava et al, 2019). However, this practice is mostly done
in developing countries or in others with fragile or undrafted legislation.
In the context of the EU countries, phosphate rock is classified as a critical raw material by the
European Commission (European Commission, 2019). The phosphorus is completely imported
to serve the necessary demands therefore making it vulnerable to market fluctuations in
fertilizer and mineral P prices (The World Bank, 2020). Many studies have been done in recent
years to understand the P-flow analysis (PFA) that provide insight into how people use and
reuse P and how P on various spatial scales is lost to the environment (Chowdhury et al, 2014).
PFA findings indicate that significant amounts of P are lost outside agriculture, by wastewater
and biodegradable solid waste, in manufacturing, consumption and waste handling sectors.
National PFA studies show that there are significant variations in phosphorus flow within
countries and within regions. However, the research on the extraction of phosphorus from
different sources is developing rapidly. Municipal wastewater, sewage sludge and animal
manure are some of the promising sources of P recycling to replace P derived from phosphate
rocks (Ehmann et al, 2017).
2.4 Concerned legislation
Due to the environmental threats (such as organic micropollutants and pathogens) associated
with sewage sludge, its agricultural application is prohibited by legislation or is not practiced
in many European countries. Owing to these possible environmental and health threats,
acceptance of direct applications and thus direct P recovery in many European countries is poor
or declining (Ott and Rechberger, 2012). For the latest alternative methods of handling waste,
such as cement co-incineration, caloric power plants and waste incinerators, P is irreparably
lost. Moreover, one of the biggest flaws in the current EU legislation regarding the soil
application of manure is its “status”. The manure, even after any kind of treatment or digestion
is particularly considered as waste, which further limits its application as a fertilizer alternative.
However, this legislation is under revision currently at the EU, increasing the chances of more
usage of manure in the future applications.
One way to reduce the direct risk of P losses to surface waters is to restrict the P application by
setting maximum application levels. In addition, general legislation regarding the use of
manure or fertilizers can indirectly restrict the use of P in agriculture. Manure typically has a
8
N/P ratio of 2 to 8, as opposed to the N/P ratio of 7 – 11 required by crops for efficient growth
(Amery, 2014). This results in an excess of P if the crop's N requirement is met using only
manure. The application of manure in (NVZ) is limited to 170 kg N/ha/yr or a higher value in
case of derogation. It helps to restrict the application of P to soil, depending on the N/P ratio
of the manure applied (Amery, 2014). The limits may have a standard value (which are
established according to local legislations) but may also be distinguished with respect to crop
type, soil phosphorus status or even crop yield. Most laws apply to all the types of (acceptable)
phosphorus application but often only the use of manure or inorganic fertilizer is regulated.
If the case of Belgium, a new Manure Decree comes into effect in Flanders every four years as
a means of enforcing the Nitrates Directive. This new Manure Decree (Anon, 2011) tackles the
distribution of phosphorus and nitrogen. The current application standards generally fluctuate
between 65 and 95 kg P2O5/ha/yr depending upon the type of crop. The average application
levels for phosphorus are around 5 kg P2O5/ha/yr less than the crop's general uptake of
phosphorus, resulting in a low, negative injection of phosphorus into the soil (Amery, 2014).
Phosphorus can be supplied to the soil in the form of compost, organic materials or natural
fertilizers (only chemical P fertilizers cannot be used by derogation farms). Table 1 shows the
directive principles for various crops.
Table 1. Phosphorus (total) application standards in Flanders region (Amery and Schoumans, 2014)
Crop
Application limits (kg P2O5/ha/y)
2011-
2012
2013-
2014 2015-2016* 2017-2018*
Grassland (only mowing) 95 95 95 90
Grassland (not only mowing) 90 90 90 90
1 cut grass/rye + maize 95 95 95 90
Maize 80 80 75 70
Winter wheat - triticale 75 75 70 70
Other cereals 75 70 70 70
Other crops 75 65 55 55
* limits for 2015-2018 are indicative
Just 40 kg of P2O5/ha/yr can be added to soils found in saturated phosphate areas. No
phosphorus can be used on soils located in security zone category 1 i.e. the drinking water
extraction areas. No phosphorus can be added to these agricultural soils in vulnerable natural
areas (Anon, 2011).
9
In case of United States, the legislations define the limits in the form of Animal Units. The
overall application levels of manure on all soils are limited by crop-available nitrogen.
Nevertheless, criteria for the phosphorus-based rate must also be met in certain specific
circumstances (MPCA, 2019). Table 2 shows the summary of nutrient application rate
requirements for manure.
Table 2. Nutrient application rate requirements for manure (MPCA, 2019)
Nutrient type Application rate requirement
Nitrogen (N) a) Cannot exceed crop N needs for non-legumes.
b) Cannot exceed crop N removal for legumes.
Phosphorus (P) a) No long-term soil P build-up near waters.
b) Manure management plan with P management strategy required
if applying to extremely high P soils and facility is over 300 animal
units.
Potassium (K) No restrictions in rule.
There is no legislation in India governing the use of P fertilizer, as a result of which the soil
check for P showed a moderate status in cultivated soils whereas the P deficiency in soils was
maximum two decades earlier. The excess N-P-K complex fertilizer is more of a compulsion
than an exception in most irrigated soils due to extensive ads from chemical fertilizer
manufacturers and traders to improve their industry with complete disregard for soil and water
quality and the related environmental pollution problems. Sadly, soil testing for P or any
nutrient for that matter is not needed to decide on crop need or otherwise fertilization. Thanks
to the increase in chemical fertilizer prices that ultimately swayed farmers from opting for
organic fertilization such as composting, vermicomposting, green manure, green leaf manure,
oil cakes etc. (Reddy, 2015). Legislation to encourage the use of chemical fertilizers and
pesticides, herbicides are imperative for every nation, if not the planet, to ameliorate the quality
of natural resources and the life of all Earth's species.
2.5 Use of manure for agriculture
As per 2017 census, over 115 million tons of nitrogen (Mt N) has been supplied as an
input into agricultural soils by animal manure globally (FAO, 2019). 75 % (88 Mt N) of
this animal manure is left permanently in paddocks and pastures. One quarter (27 Mt N
yr-1) was treated in manure management systems and applied as fertilizer; and another one
10
third of N deposited or applied to soils (34 Mt N) was lost to leaching (FAO, 2019). More
than 50% of all animal manure was produced by cattle. The overall livestock manure N
production increased by 0.6%, compared with the mean growth of 0.9% for previous ten-
year cycle (2008-2017). The average cumulative growth rate was 1.3% per year, between
1961 to 2017. In 2017, the production of cattle manure was 75% higher than in 1961. In
2017, Brazil (7.9 Mt N from beef cattle), the United States of America (3.0 Mt N from
beef cattle) and China (2.0 Mt N from goats) reported the highest N inputs of pasture by
country and animal type (FAO, 2019). Furthermore, the largest inputs of manure treated
and applied to soils by country and animal type were in China (1.4 Mt N from pigs), India
(1.0 Mt N from buffalo) and again China (0.9 Mt N from chicken) (FAO, 2019).
Table 3. Manure production (liquid content) and nutrient content for major livestock species (Shrivastava et al,
2019).
Animal Manure Produced
(kg yr-1)
Nutrient Concentration (kg 1000 l-1)
Total N Total P NH3-N
Swine (Farrow-finish) 17007 3.4 1.3 1.9
Dairy (Cow) 24490 3.7 0.8 0.7
Dairy (heifer) 11338 3.8 0.7 0.7
Beef (Cow) 13605 2.4 0.8 0.8
Poultry (layer) 59 6.8 2.7 4.4
Poultry (broiler) 38 7.6 2.1 1.6
Poultry (turkey) 128 6.4 2.1 1.9
2.6 Heavy metals
Pig manure is a sustainable nutrient source that has been commonly used as organic fertilizer
in agriculture. Nevertheless, the presence of antibiotic residues and heavy metals (HM) in pig
manure restricts its direct land use (Wang et al, 2016). Trace elements may be taken up from
the soil by plants or biota and cycle in biological tissues before ultimately returning to the soil
through decaying biological remains (Tack, 2010). Under nominal concentrations, HM such as
Cu, Zn, Se, etc. are important for the plant life cycle, but the metals become toxic to the edaphic
organisms and crops above different threshold ranges. HM are absorbed by the root and are
translocated to the shoot by different transport mechanisms that mediate the movement of non-
essential HMs such as Pb and Cd in certain circumstances (Holzel et al, 2012). Trace metals
like Cu and Zn (Cd appears as a contamination in Zn feed) are used globally to prevent
11
infectious diseases in intense animal breeding and as promoters of growth (Cang et al, 2004;
Mccarthy et al, 2013). Mineral feed contributes to emissions of Cd Pb, As and Hg. Other
potential sources of HMs, such as Cu, Cd, Cr, Zn and Ni, are added for the prevention of
corrosion in metal structures, ash alteration of manures for odour control and lime alteration
for disinfection purposes (Anonymous, 2004). Such heavy metals can accumulate in soil, up
taken by plants and affect animal and human health through the food chain (Buelna et al, 2008;
Qureshi et al, 2008). The prolonged application of HM into the soil can also reduce the soil
buffering capacity, and thus contribute to permanent soil and groundwater pollution. While
certain mechanisms of heavy metal tolerance may be linked to mechanisms of antimicrobial
resistance (Akinbowale et al, 2007; Bass et al, 1999), heavy metals may select bacteria that are
resistant to antibiotics. This was observed in the case study done by Berget et al (2005), where
copper-resistant soil-isolated bacteria that were substantially more resistant to antibiotics (e.g.
ampicillin, tetracycline, sulfone-amides, chloramphenicol) than copper-sensitive strains. For
the remediation of heavy metals from pig slurry, composting and anaerobic digestion
approaches have typically been employed (Marcato et al, 2008; Lu et al, 2015), however these
demonstrate other limits, such as the heavy metals can only be fixed and the total heavy metals
cannot be reduced. Organic modifications such as effective application of cattle manure have
also been reported to regulate heavy metals (HM) content in soil (Wei et al, 2015). Nonetheless,
applying organic matter (OM) as soil enhancers is an effective technique for heavy metal
immobilization by complexion components, thus potentially decreasing plant uptake.
Pig manure has a higher Cu and Zn content than cattle manure in general. After they have been
applied to the soil, HMs are subject to reactions that alter the plants' bioavailability. Moreover,
adsorption on to clay and/or organic, precipitation as insoluble salts (carbonate and phosphate)
and changes in the oxidation state of HM affects its solubility (Provolo et al, 2018).
2.7 Factors affecting composition of pig manure
The composition of manure from livestock and within different lots of a specific domestic
animal varies greatly. Azevedo & Stout (1974) has confirmed that certain variations in manure
nutrient concentrations have been caused due to factors such as digestion processes and feed
preferences of various animal species (Table 4). For instance, due to the ability of the ruminants
to extract the organically bound P from plant feeds, its manure generally has lower P value in
comparison to poultry and swine manure. Based on overall composition, liquid fraction of
swine manure contains on an average of 9% of total N by mass and 4% dry matter in
comparison to 7% and 10% is case of liquid fraction in cattle manure (Evans et al, 1977).
12
Furthermore, as per the data collected by Azevedo and Stout stated in Table 3, 10 hogs produce
as much as 80% of manure N as two beef cows. The concentration of different dietary salts and
other mineral additives (Cu, As and other minerals) in swine manure are directly affected by
the concentration of the aforementioned minerals in swine rations (Sutton et al, 1976; Brumm
& Sutton 1979; Sutton et al, 1984a). Thus, high use of manure from such sources can therefore
be harmful to plants and can reduce productivity of the soil.
It is stated by Sutton et al (1984a) that swine manure from 0.5% salt averaged diet is more than
twice the sodium content in comparison with diet containing 0.2% salt. The use of manure,
however, did not contribute to soil pollution or phytotoxicity. Wallace et al (1960) reported
addition of dietary copper to swine rations at levels of 125 mg/L to 250 mg/L to stimulate
growth. However, a 16 to 32-fold increase in Cu concentration in manure has been observed in
the study done by Kornegay et al (1976); where swine fed with a 250–300 mg/L Cu diet.
The housing system, the manure collection, storage, and handling process may also influence
the manure composition (Szoegi, Vanotti and Hunt, 2015). Usually 50% of N in pig manure
slurry is present in the form of ammonium nitrogen and the remaining 50% in the form of
organic nitrogen. (Choudhary et al, 2015). The organic nitrogen constitutes microbial N, labile
organic N and stable organic. Beauchamp (1983) determined that approximately 20% of
organic N will be mineralized and usable throughout the growing season, and that 25% of
ammonia will be volatilized, resulting in a net supply of approximately 50% of N used for crop
growth. According to the work done by Nasiru et al (2014), the method of storage of manure
and the treatment process contributes to about 10 – 30% ammonia nitrogen losses from manure.
Moreover, manure storage leads to gases such as ammonia, nitrous oxide, and methane in the
atmosphere (Kulling et al, 2001). The amount of gas emissions depends on the digestibility of
feed and the general output of animals. The lowest loss was from closed shelters such as aerated
storage and the maximum loss was the open storages like feed-lot surfaces and anaerobic
lagoons. Al-Kanani et al (1992) reported that use of sphagnum peat moss reduced NH3 losses
by 75%. Nasiru et al (2014) suggested the use of vermicast for the reduction of ammonia
nitrogen losses. Losses relating to P and K are mostly minimal only contributing to 5 – 10%.
However, these losses increase significantly in case of open-lot or lagoon handling systems
where 40 – 50% of P can be lost to runoff and leaching (Sutton et al, 1984a).
The rate, time and method of applying manure varies, including weathering, soil
characteristics, crop type and mineralization rate of nutrients. When integrated immediately
after land application to mitigate loss of nutrients, the maximum nutrient gain from swine
13
manure is obtained. For minimizing the localized salt concentration, the uniform application of
manure must be practiced, especially in the case of Na which can significantly reduce
germination and crop yields. In case of severe odour problems resulting because of manure,
knifing the manure into the soil is recommended. However, this procedure also limits the rate
of manure application. In the study performed by Dickey and Vanderholm (1975), 30 – 90%
losses of NH3 − N from manure were observed with ploughing down respectively.
Table 4. Quantity of nutrient elements excreted in manure of various animals during reproduction cycles*
Number and type of animal, length
of production period, and animal
weight during production period
Element excreted (kg)
N P K
1000 broilers: 10 weeks: 0-1.8 kg 70 14 23
100 hens: 365 days: 2.3 kg 57 20 19
10 hogs: 175 days: 14-91 kg 52 13 15
10 beef: 365 days: 181-500 kg 64 13 66
2 dairy cows: 365 days: 544 kg 64 13 66
*Adapted from Webber et al (1968) as in Azevedo & Stout (1974)
In case of the areas with high rainfall and highly permeable soils, the nutrient availability of
the crop could be maximized by application of manure close to the planting date. However,
germination and growth in the planting process may be reduced immediately after application
of heavy manure due to the accumulation of salt. In the areas with low temperature climates,
application of manure may not be possible in early spring, because of the possibility to be
frozen in the pit, particularly when it is stored in open lagoons. The fall–winter application may
cause a decrease of 25 – 30% N from the manure, a longer field duration will allow soil micro-
organisms to decompose the manure and make the nutrient more available to spring seeded
crops (Madison et al, 1995). The loss of N from fall–winter application of manure can be
minimized either by injecting it into the soil or by addition of a nitrification inhibitor. To obtain
the best possible results from manure application, the rate should be such that the amount of
available nutrients is equal to the amount required by the crop. However, a problem is
encountered as only 45% of N is mineralized in the first year of application.
A study done by Larson (1991) also shows that even after the period of 5 years, only 80% of
the total N is mineralized from the manure. Alternatively, almost all the P and K present in
manure are available at the time of application. Low permeability for heavy-structured soils
and low decomposition levels further corresponds to lower rates of manure application in
comparison to highly permeable coarser textured soils, promoting faster decomposition of
14
manure. However, high levels of application of manure in coarse soil textured can pollute
groundwater by nutrient release, while high application rates of manure on heavy textured soil
may be beneficial because of the high nutrient holding capacity of these soils. Manure should
not be applied to snow or frozen land, particularly if the soil is subjected to accelerated spring
runoff. Furthermore, the leaching of N contaminating the groundwater can be prevented by
restricting on use of the heavily manured fields during summers.
2.8 Valorization technologies
2.8.1 Hydrothermal carbonization
Hydrothermal carbonization (HTC) was first introduced by Friedrich Bergius in 1913. It is
often used to convert waste feedstock/biomass (f) into a solid fuel of relatively high calorific
value as compare to brown coal (Oliveira et al, 2013). The process of HTC involves the
temperature treatment of organic matter in saturated conditions, generally rich in moisture
content, at around 180-250℃ (Román et al, 2012) and 2-10 MPa of pressure for a certain time.
Thus, HTC is a combination of processes such as dehydration, hydrolysis, polymerization and
decarboxylation (Román et al, 2012). Although, the rudimentary resemblance of HTC lies with
torrefication (dry pyrolysis), but, in comparison to torrefication, it requires less time and can
be employed for wide range of biomass types. In general, this process leads to an increase in
carbon content of the matter while lowering its oxygen and hydrogen share and the final solid
product is termed as hydrochar. The hydrochar can be used as soil amendment whereas the
liquid products of HTC are usually acidic and contain organic and inorganic compounds (e.g.,
nitrogen, phosphorus and some mineral matter originated from raw material) (Oliveira et al,
2013). The key advantage of the HTC is its ability to transform wet biomass into highly useful
and carbonaceous solid fuel without depending upon the initial drying (Román et al, 2012).
However, the installation cost and sophisticated maintenance requirements are among the main
concerns of this technology.
2.8.2 Ammonia stripping
Ammonia stripping (AS) works on the principle of mass transfer, where wastewater is brought
in contact with air to strip the ammonia gas present in it. Ammonia in wastewater is found in
the form of ammonium ions and ammonia gas and their relative concentration depends upon
the pH and temperature of the wastewater (Wang, 2018) The ammonia stripping is carried out
in two steps. First, the influent, containing high nitrogen content, is ammonified and
anaerobically predigested (3 – 5 days). In this step the ammonification bacteria break down
15
proteins and ammonium ions (NH4+) are formed. The second step is stripping, ammonium ions
are transformed into ammonia (NH3) by adjusting the pH up to 10 (Guštin and Marinšek-Logar,
2011). The increase in pH gives rise to increase in ammonia gas formation, therefore lime is
typically used to raise the pH value of the wastewater prior to stripping step (Wang, 2018).
Along with raising the pH of the influent, lime (calcium oxide) also generates calcium
carbonate which act as a coagulant for particulate matter. Ammonia is then recovered in the
form ammonium sulphate [(NH4)2SO4] by scrubbing with acidic solution.
2.8.3 Crystallization
Struvite precipitation is a well-recognized process for the recovery of phosphorus. This method
not only solves the problem of environmental pollution caused by the discharge of phosphorus
into natural streams but can also be utilized as a useful resource in the form of fertilizer (Suzuki
et al, 2007). Numerous studies have been carried out on the topic of struvite precipitation of
swine wastewater and it has been identified that phosphate recovery depends on the
concentration of magnesium, ammonium and phosphate ions as well as pH, N/P ratio and
influent flow rate (Kozik et al, 2013; Desmidt et al, 2013; Tansel, Lunn and Monje, 2018). The
addition of magnesium salts along with pH adjustment for struvite precipitation is among the
most commonly employed approach (Suzuki et al, 2007; Kruk, Elektorowicz and
Oleszkiewicz, 2014).
2.8.4 Pyrolysis
Pyrolysis (PL) is a process of thermal decomposition where lignocellulosic biomass is
degraded under oxygen-deficient conditions and inert environment. At around 350 – 550℃ the
organic matter in the biomass starts to degrade and can persist until 700 – 800℃ in the absence
of oxygen (Bridgwater, Meier and Radlein, 1999; Bridgwater and Peacocke, 2000). The end
products of this process include biochar, bio-oil and gases (e.g., CH4, H2, CO2 and CO and their
relative proportion depends upon various parameters such as the temperature, heating rate,
residence time, pressure, types of precursors and reactor configuration. Depending upon the
form of final products, pyrolysis can be categorized into two types; (i) slow pyrolysis (yields
heat and biochar) and (ii) fast pyrolysis (yields bio-oils along with biochar) (Zaman et al, 2017).
Unlike pyrolysis, the gasification process allows the biomass to react with a regulated oxygen
amount with steam or air (Brewer 2012; Mohan et al, 2014). In gasification, the biomass is
heated to a temperature higher than 800°C with an average residence time ranging between
several seconds to multiple hours (Inyang and Dickenson 2015).
16
Biochar may be defined as “the product of thermal degradation of organic materials in the
absence of air (pyrolysis) and is distinguished from charcoal by its use as a soil amendment”
(Lehmann and Joseph, 2009). It could be used for soil improvement, due to its water holding
properties and the improvement of nutrient content, thus increasing the overall soil fertility and
crop productivity.
Biochar has gained significant recognition in recent years for its multi-functionality including
carbon sequestration and soil fertility enhancement (Laird et al, 2010), bio-energy production
(Field et al, 2013), and environmental remediation via adsorption process (Mohan et al, 2014).It
also provides a stable pool of organic carbon for extended periods, contributing to the beneficial
effects of organic matter in soils (Tack and Egene, 2019). This may therefore decrease the
solubility of pollutants, mobilize and leach from soil solids, and minimize the movement of
pollutants to other compartments of the environment and dispersion into adjacent areas (Tack
and Egene 2019). The production of biochar from biomass (agriculture residues, forest waste,
manure, food waste etc.) can substantially reduce the quantity of waste produced in the
environment (Ahmad et al, 2013). Furthermore, greenhouse gases emissions are reduced by
biochar application due to its composition as a high carbon content material (Lehmann et al,
2007, Liu et al, 2014). Biochar could also be used as a sorbent for contaminants, including
organic and inorganic contaminants, due to its high surface area and large pore volume (Zhang
and Ok, 2014).
Lehmaan and Joseph (2009) performed experiments using manure-based biochar has obtained
high degree of usable nutrients that can increase crop productivity. The increased crop
productivity is also attributable to the reduction of nutrient leaching and the increase in
microbial activities following the use of biochar for soil application (Verheijen et al, 2010,
Lehmann et al, 2011). However, when applying a biochar form such as solid waste-derived
biochar, careful consideration should be taken as the heavy metal contents or toxic compounds
can severely inhibit the mechanisms of soil organisms (Ahmad et al, 2014a).
Biochar is typically formed by slow pyrolysis, rapid pyrolysis and gasification, differentiated
with heating, temperature and residence time (Ronsse et al, 2013, Inyang and Dickenson,
2015). In slow pyrolysis, biomass is heated at a slow pace from 5 to 30 min in the absence of
oxygen to 400 to 500oC (Mohan et al, 2014). This process leads to secondary reactions
(between the vapor and solid phase) that can allow the production of carbonated solids to
increase or optimize the production of biochar (Brewer, 2012). In comparison, during fast
pyrolysis, the biomass is heat-degraded for about 2 seconds during a short residence time
17
(Inyang and Dickenson, 2015). It aims to rapidly extract vapors and aerosol components in
order to maximize the output of liquid (bio-oil) (Brewer, 2012).
2.8.5 Mechanical Solid-liquid separation
When the liquid and solid fractions of raw manure or digestate are separated through
mechanical separation, it results into the enrichment of nitrogen (as well as potassium) in the
liquid phase and the enrichment of phosphorus and organic matter in the solid phase. This way,
a high amount of phosphorus can be concentrated in a small volume. This technique is generally
applied as a pre-treatment step in nutrient recovery processes. However, this technique can also
help in substantial manure management. Separation can be performed by various technologies
such as screw press, centrifuge of belt press (Hjorth et al, 2010). The N-containing liquid
fraction can be applied on cultivable land which helps to reduce the usage of mineral fertilizer.
Whereas the P-rich solid fraction can be employed in regions where P-content in soil is low or
carbon demand is high.
2.8.6 Biological Treatment
2.8.6.1 Algal uptake
Nutrient uptake by microalgae from organic waste is another potential technique of nutrient
recycling from manure. This a sustainable and environmentally friendly technique where
nutrient assimilation into algal biomass give rise to high quality fertilizers. Manure digestate is
typically a favorable medium to cultivate microalgae for the production of biofertilizers
because it has less contamination compared to raw manure and has comparatively high N and
P concentrations. Similarly, this technique can also be used for nutrient extraction from the
liquid fraction of digestate. In the recent past, several studies have demonstrated the potential
of dry algal biomass, generated from the treatment of anaerobically digested manure, as a
probable fill-in for commercial fertilizers (Mulbry et al, 2005; Veronesi et al, 2015; Uggetti et
al, 2014).
2.8.6.2 Composting
Composting is defined as the biological degradation process of heterogeneous solid organic
materials under controlled moist, self-heating, and aerobic conditions to obtain a stable material
that can be used as organic fertilizer (Lobo and Dorta, 2019). The cycle involves decomposing
organic material into a humus-like substance which could act as a nutrient source supporting
plant growth (Lal, 2013). Composting includes the following three components: human
18
control, aerobic conditions, and internal biological heat production. For an effective working,
it requires the counterbalance of four essential counterparts:
• Carbon — The microbial oxidation of carbon produces the heat. The compounds with
high carbon content tend to be brown and dry.
• Nitrogen — for growing and replicating more carbon oxidizing species. The high
nitrogen products, including fruit and vegetables, appear to be green (or colorful) and
wet.
• Oxygen — for oxidizing the carbon, the decomposition process.
• Water — to maintain the activity of microorganisms without inhibiting aerobic
conditions.
The composting is mostly preferred with an optimal C:N ratio of around 25:1. Rapid
composting is encouraged by having a C/N ratio of approximately 30 or less (Lal, 2003). Above
30, the substrate is nitrogen starved, below 15 it is likely to outgas a portion of nitrogen as
ammonia.
Composting is used as an important recycling tool for local-generated livestock waste and
offers an environmentally friendly alternative method for organic waste disposal as it
contributes to organic waste stabilization and usage. Many studies indicate that the application
of mature compost to agronomic soils improves production because of its characteristics such
as high plant nutrient content and retention of moisture. In a study performed by Huang et al
(2004) reported that, at the initial C/N of 30, the co-composting of pig manure with sawdust
provided a maturity for the compost after 49 days. With manual turning, the stable compost
produced could be used for organic farming or as a soil amendment. However, treatment at a
low initial C/N of 15 significantly influenced behaviours of many important parameters such
as high dissolved organic carbon (DOC) and soluble NH4+ during the co-composting.
Moreover, the resulting compost's high electrical conductivity values must be reduced to levels
that would not impose an inhibition on plant development.
2.8.6.3 Anaerobic Digestion
Anaerobic digestion of animal manure is an alternative way to treat large volumes of organic
waste and its related issues in feeding lots and limited feeding operations (Ileleji, Martin and
Jones, 2015). There are majorly four steps involved in the process of anaerobic digestion
(figure 1):
19
• Hydrolysis - Biopolymers are decomposed to monomeric building blocks or other
dissolvable basic products. Fats decompose to fatty acids, carbohydrates as for example
polysaccharides are transformed in monosaccharides or oligosaccharides and the
proteins in pectin respectively (Shrivastava et al, 2019).
• Acidogenesis - simple monomers are converted into fatty and carbonic acids, as for
example butyric, propionic and acetic acid, then in lower alcohols - ethanol.
• Acetogenesis – A biological reaction where the lower fatty and carbonic acids as well
as the lower alcohols are converted in acetic acid.
• Methanogenesis – A biological reaction where the acetic acids are converted into
methane (Shrivastava et al, 2019).
Figure 1. Cycle for biogas generation and utilization (Shrivastava et al, 2019).
1. Digestate
Increasing numbers of anaerobic digestion plants in Europe have resulted in increased nutrient-
rich digestate production with great potential as fertilizer for arable land. Anaerobic digestion
of animal manure prior to being used as a fertilizer is usually considered favourable, since the
digestate generated has greater proportions of mineralized, plant-available nutrients than
untreated manure (Insam et al, 2015). Other environmental benefits such as increase in soil
carbon and reduction in atmospheric carbon levels, soil erosion (runoff) and nitrate leaching
20
further makes it an attractive option (LPELC, 2020). The digestate nutrient composition varies
with the substrate processed by the biogas plant and may contain compounds stimulating or
inhibiting soil microbial activity (Risberg et al, 2017). The composition of the digestate
depends on the origin of the ingoing substrate and on the management digestion cycle. Factors
like animal form (omnivore, ruminant, etc.), sex, species, age, and diet, as well as geographic
and environmental conditions strictly changes the composition of digestate. According to the
study done by Arthurson (2009), the proportion of ammonium (NH4+) is generally higher in
digestate than in the organic substrate going into the anaerobic digestion (AD) process. Another
study performed by Risberg et al (2017) displayed higher ammonium levels and lower organic
carbon levels in digestates as compared with pig slurry and cattle manure. In addition, digestate
usually induced increased potential for ammonium oxidation, while pig slurry and cattle
manure caused substantially more respiration. This trend indicates that for heavy soils with a
high level of clay and carbon, the digestate may be better alternative, whereas for lighter sandy
soils with less organic carbon the slurry and cattle manure are more efficient.
2. Biogas
Biogas is a mixture of methane, carbon-dioxide, sometimes nitrogen, hydrogen, hydrogen-
sulphide, ammonia, and other remainder-gases, which are produced by micro-organisms in
anaerobic environment from organic materials. The biogas mainly constitutes of methane
corresponding to around 45 – 70%, followed by CO2 between 35 – 50%. In a study done by
Nagy and Wopera (2012) at Hungary, the anaerobic digestion was carried out in a batch reactor
with continuous mixer at a thermophilic temperature of 54°C. For a hydraulic loading of
100,000 m3 pig slurry/yr, the estimated biogas production was about 1,024 m3/day. The
methane content of the produced biogas was normally 60%, which is proper for the work of
gas engines. With the gas engines cogeneration can be achieved. Through the cogeneration on
the one hand heat can be produced and on the other hand electricity can be generated. If this
biogas is used to release heat by burning, a corresponding energy of 22,022 MJ/day will be
obtained. The electrical equivalence of this heat will be 6,117 kWh/day (Nagy and Wopera,
2012). Moreover, for a higher biogas yield, the co-digestion (involving two or more type of
organic matter) is mostly preferred to maintain the C/N ratio in the feedstock. In another study
performed by Vasmara et al (2015), wheat straw was pre-treated with lignocellulosic fungi and
then is co-digested with pig slurry. The co-digestion in this case helped to reduce the maximum
methane yield time from 35 to 21 days with an average increase of 37% in biogas production.
21
Methodology
The meta-analysis of research studies was carried out according to the guidelines suggested by
the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA)
statement (www.prismastatement.org). Moreover, the principles of random effects model were
employed for this meta-analysis.
3.1 Data and literature sources
The studies were collected from various online databases such as Web of Science, Journal
Storage (JSTOR), ScienceDirect and Google Scholar on the bases of relevance to the concerned
topic. The approach for ferreting out the relevant studies from these databases was based on
the subject headings such as resource recovery, manure management, etc. and the
corresponding key words. To obtain more topic-oriented results, additional filters were
involved in the methodology. These filters contained search terms such as (1) manure, (2)
valorization and (3) nutrients. Furthermore, the manual selection of studies has also been done,
however this did not lead to inclusion of any further studies.
3.2 Study selection
The selection of the articles/studies from the initial database for further assessment first
proceeded via elimination of duplicates. For this purpose, studies were entered in a web
application named Kopernio, which facilitates in the blinded screening. After removing the
duplicates from the data, the remaining articles were first assessed based on the eligibility of
titles and abstracts of these studies. This further helped in labelling the articles as “included”
or “excluded”. Later on, the following conditions were selected and applied as a criterion to
find out the appropriate studies for a meta-analysis.
a. The study had to refer to pig manure.
b. The study must report the initial and final concentrations of nutrients or a
combination of either one of the above two values and the recovery efficiency.
c. The language of study could be one of the following: English, Dutch, French,
German, or Spanish.
The research studies that did not meet the aforementioned inclusion criteria, were excluded
from this study. The exclusion criteria adopted, for labelling a study as ineligible, comprised
of the following points.
22
a. Manure Type: Any other source of manure (such as cattle, poultry) were not
considered
b. Studies reporting anaerobic digestion for biogas generation were excluded (as the
primary focus of the study was nutrient recovery).
c. The studies dealing with piggery wastewater were not included.
d. Research articles available in only Japanese or Chinese languages (i.e. no
translation available) were omitted.
e. Studies reporting only recovery/valorization efficiency were eliminated.
f. The studies for which full text could not be obtained from any source or the studies
with irrelevant abstract were discarded.
3.3 Data extraction
The data extraction was started from the shortlisted papers for which a Microsoft Excel data
sheet file was created for recording the results. The extracted data contained following
information about the studies: (1) recovered nutrients - nitrogen, phosphorous, organic carbon
or potassium, (2) technology implemented, (3) scale of implementation: lab scale, pilot scale
and full scale, (4) final concentration of nutrients, (5) flow/volume of test, (6) nutrient recovery
efficiency, (7) location of study, (8) duration of study and (9) authors names and DOI of study.
3.4 Data analysis
The dataset was sorted by nutrient extracted and filtered by valorization technique used. Using
this, a database of six main treatment technologies were identified for inclusion: hydrothermal
carbonization (HTC), ammonia stripping, pyrolysis, Crystallization, Biological processes and
Separation techniques. For each valorization mechanism, the reported recovery efficiency (%
recovery) was recorded. When percentage recovery was not directly given in the study, they
were calculated from the influent and effluent concentrations where provided.
3.5 Strategy for data assessment
3.5.1 Qualitative assessment
The data mined from the eligible studies will be described in a narrative style. This will
summarize the characteristics of the studies in terms of year wise trend in technological shift,
country wise technological preference and nutrient wise distribution of studies. A 95%
confidence interval is a range of values that you can be 95% certain contains the true mean of
the population.
23
3.5.2 Quantitative assessment
The evaluation of data will further be conducted in a statistical meta-analysis using Review
Manager (RevMan) computer program version 5.4 (The Cochrane Collaboration, 2020). The
meta-analysis will only be performed when three or more studies that had data points for
recovery of phosphorus and/or nitrogen for a particular technology of interest. For a particular
technology, the initial and valorized product among the studies were compared with the help
of forest plots. In this method, the differences in means between experimental (represents
valorized product concentration) and control groups (initial concentration) will be divided by
pooled standard deviation (SD) of the two groups to convert all outcome measures on to a
standardized scale with a unit of SD incorporating a random effects modelling approach. The
random effects model accounts for the intra-study and inter-study variability. The 95%
confidence intervals were considered to ensure the certainty that range of values contains the
95% values of the true mean of the entire dataset. Additionally, various units (such as mg/L,
dg/L, etc) were used in order to plot the graphs in the limits set up by RevMan (-1000 to 1000).
Furthermore, the data for REs were evaluated on box and whisker plots to summarizes the set
of data measured on an interval scale, which facilitates an explanatory data analysis. The graph
represents an overall shape of the distribution, the central value, and its variability. The value
is considered to be “satisfactory” when the condensed box is obtained for a relatively high
number of studies. For the economics, data on capital, operational and maintenance cost was
collected for each technology and evaluated. For some of the technologies, the data on value
of final product is also compiled.
3.5.3 Heterogeneity assessment
Inevitably, the studies delved out for the meta-analysis will differ from each other due to factors
including the diversity in slurry composition, and geographical distribution. The variability
among the studies is termed as heterogeneity and manifests the extent to which the results of
these studies are consistent (Cochrane, 2020). The evaluation of heterogeneity between studies’
valorization effects was determined with the help of probability (p) and percentage of variance
(I2) values. A low p value indicates that the observed variation in the estimates of effect is not
due to chance alone. However, a significant p value does not always indicate the absence of
heterogeneity because of few numbers of comparisons or small sample size contribute to false
results. Therefore, an additional measure I2 was used to assess heterogeneity. I2 describes the
percentage of total variation across the studies and is calculated by taking the difference
24
between Cochran's homogeneity test statistic (Q) and degrees of freedom (df). A value of 75
or more will be considered as an indication of heterogeneity (Deeks, Higgins and Altman 2008;
Borenstein et al, 2010).
3.6 Risk-of-Bias assessment
The quality of every study in the dataset was estimated using the Revised Cochrane risk-of-
bias tool for randomized trials, which majorly uses the 5 domains: 1) randomization process;
2) deviations from the intended interventions; 3) missing outcome data; 4) measurement of the
outcome; and 5) selection of the reported result. Each study has been categorized for the risk-
of-bias, divided into the sections of “low risk” (green), “some concern” (yellow) and “high
risk” (red). However, the overall risk for a particular study depends upon the overall effect of
all domains contributing equally for the final risk determination (Cochrane, 2020). For the
concerned meta-analysis, the 4 factors were used for the risk determination: 1) randomization
process; 2) missing outcome data 3) measurement of the outcome; and 4) selection of the
reported result. The overall judgement for the risk is defined as follows 1) If all the domains
are categorized as low risk then the complete study will be defined “low risk-of-bias”; 2) the
overall risk will be assigned as “some concerns” if the result in any one of the domains was
assigned “some concerns” 3) the overall risk will be high if the result in any of the domains
will be assigned as “high risk-of-bias” or if the results of multiple domains were assigned
“some concerns” (Cochrane, 2020).
25
Results and discussion
4.1 Overview of the data collection
A total of 52 studies published between 2002 and 2020 were selected. Prior to the initial
screening, the raw database consisted of 3337 articles. Out of these, 1457 studies were
identified as duplicate sources among the various databases. Further screening (explained in
the Figure 2) led to a final database consisting of records of 52 studies that reported the possible
valorization percentages of nitrogen and phosphorous by the application of various
technologies. A complete list of all the studies containing the details of the extracted data from
these studies is given in Appendix 1.
The shortlisted research studies were sorted in 3 phases.
• Phase 1: Dataset (n = 52) was sorted according to the scale of a study. It was observed
that the about 88% of the studies were performed on the lab/batch scale and only 6
studies (combined) were done for pilot- and full- scale respectively.
• Phase 2: In this phase, the categorization of the data was based on the type of nutrients
extracted or removed in the study. The studies reporting phosphorous recovery were 43
while 33 were carried out to determine nitrogen recovery.
• Phase 3: The scrutinization was done based on the type of technology used for the
treatment purpose. A comprehensive search in this phase divided all the nutrient
recovery technologies in six major treatment processes – hydrothermal carbonization,
pyrolysis, struvite precipitation, biological processes, separation techniques and
ammonia stripping (Table 5).
During the scrutinization of data, it was observed that some of the studies mentioned the use
of more than one treatment technique for the nutrient recovery process (number of studies - 7).
Adding to this, some studies also considered the use of different manure fractions to access the
nutrient recovery process (number of studies – 4).
26
Figure 2. Data screening and selection steps for systematic review
Iden
tifi
cati
on
Sc
reen
ing
Elig
ibili
ty
Incl
ud
ed
Records identified through database searching (n = 3,325)
Web of Science (n = 1,072)
JSTOR (n = 1,096)
Science Direct (n = 1,157)
Additional records identified through
other sources (n = 12)
Records identified for screening
(n = 3,337)
Records after duplicates removed
(n = 1880)
Records excluded (n = 1,457)
Full-text articles excluded
(n = 225) Reasons:
• Irrelevant abstract
(n = 157)
• Review papers (n = 23)
• Language (n = 5)
Full-text articles assessed for eligibility
(n = 317)
Studies included in risk of bias assessment
(n = 52)
Studies included in meta-analysis
(n = 52)
27
4.2 Data distribution
An overview distribution of the final dataset (Table 5) based on the number of studies for
various recovery technologies is shown. Other details such as RE, location, year, etc. has been
provided in Annex 1.
Table 5. Treatment processes diversification in the selected dataset
Treatment technology Number of studies*
Hydrothermal Carbonization 9
Ammonia Stripping 7
Pyrolysis 10
Crystallization 12
Separation 5
Biological 9
Total studies 52
*See annex 1 for further details of studies
4.2.1 Year wise distribution of studies
The studies were first categorized according to publication year in classes of 3-year periods
(Figure 3).
Figure 3. Distribution of concerned dataset across last two decades
0
2
4
6
8
10
12
14
16
18
2018 - 20202015 - 20172012 - 20142009 - 20112006 - 20082000 - 2005
Nu
mb
er o
f st
ud
ies
Years
Hydrothermal Carbonization Ammonia Stripping Pyrolysis Crystallization Separation Biological
28
Moreover, the data has been further subdivided into the employment of technology for each
range of years. This will help in gaining an insight of the range of technology used for various
years.
The number of studies on nutrient recovery over the span of years increased exponentially from
2000-2020 (Figure 3). Furthermore, a higher focus has been shifted towards the varied range
of technologies over the time period. Precisely, crystallization and ammonia stripping has
shown a growth of 53% and 50% over the last 5 years. Additionally, the development of novel
separation technologies (membrane distillation, electrodialysis reversal) also gained attention,
contributing to around 16% of the studies observed over the last 5 years. However, biological
methods for nutrient recovery showed a constant trend, contributing to ~23% of total studies
done in the last 3 years.
This exponential increase in studies over the last two decades could be explained by the
following points:
• The recent increase in environmental, economic, geopolitical and social concerns on
the use of nutrients for the short- and long-term in the field of agriculture. These factors
further put pressure on the need to reassess the way how plants and crops access their
required nutrients.
• The industrial, sanitation and green revolutions have altered human use of available
nutrients, shifting from close-looped nutrient management systems to unsustainable
linear paths (Ashley, Cordell and Mavinic, 2012). This has led to a global
environmental challenge of nutrient pollution and scarcity.
• The use of nutrients as a ‘strategic’ commodity is now in trend at the marketplace,
creating polarization of powers and the autocracy in the global trade.
• The focus of the recent governmental policies on the subject of “resource recovery” and
“waste valorization” has further intensified the research.
4.2.2 Country wise distribution of studies
The dataset is distributed based on the number of studies performed in the various geographical
location for the valorization of pig manure (Figure 4). Europe and China dominate the current
research for the nutrient’s recovery, contributing to around 53% and 29% of the total studies
respectively. In Europe, Denmark, Spain, and Belgium are the leading researchers adding to
21% of the total studies. Additionally, the other minor part of the studies is shared in between
29
USA, Japan, Taiwan and Vietnam, whose combined studies results in around 18% of the total
studies in the dataset.
Figure 4. Country wise distribution of studies
Furthermore, the use of crystallization and pyrolysis techniques were majorly focused for
nutrient recovery, especially in Europe. The use of struvite recovery alone results in around
20% and 22% of the studies performed in Europe and China. Interestingly, even though China
shares a large percentage in total studies, only a single study has been considered establishing
pyrolysis for the nutrient recovery at the database.
The data interpretation suggests that the number of studies is directly proportional to the
amount of pigs per head in different countries (China - 310 million pigs, market share of nearly
50%; EU - 148 million pigs) (Shahbandeh, 2020). Furthermore, USA, Japan and Vietnam also
follow the same trend.
On the contrary, studies for pyrolysis were not the part of the dataset for China. The most
plausible explanation is the implementation of the China’s national biochar programme, which
was signed and ratified in 2015, but the initial works began at late 2017 (Biochar International,
2020). This could further explain the smaller number of studies coming from China in the
sector of biochar.
4.2.3 Nutrient wise distribution of studies
The studied data were processed based on the recovery efficiencies for the nutrients. For this,
the studies were subdivided for the individual RE of each nutrient.
0
5
10
15
20
25
30
China Europe Others USA
Nu
mb
er o
f st
ud
ies
Hydrothermal Carbonization Ammonia Stripping Pyrolysis Crystallization Separation Biological
30
4.2.3.1 Nitrogen (N)
The technological distribution for different studies concerned with the RE for nitrogen was
plotted. The hydrothermal carbonization shows an interquartile range between 23% and 56%,
with a mean removal efficiency of 42% for all the studies. Furthermore, the whiskers
correspond with the value of 12% and 67%. In the case of ammonia stripping (mean – 83%)
and crystallization (mean – 84%), the whiskers show a value of 98-55% and 97-56%, with an
interquartile range of 96-68% and 96-67%. Moreover, the upper and the lower quartile values
for separation were recorded to be 78% and 42%, with a mean value of 64% over the set of 8
data points.
Figure 5. Comparison of RE various valorization technologies for nitrogen (x = mean, --- = median and dot =
datapoints)
From the above data, the use of ammonia stripping and crystallization appears to show
successful recovery efficiency for N. This could be the reason behind the exponential increase
in ammonia stripping and crystallization across the dataset. Ammonia stripping is a mechanical
procedure and creates no backwash or regeneration (EPA, 2020). However, a drawback of this
technology is that it is highly temperature dependent and energy requirements could be a
burden. This issue could be resolved by the use of solar heating of the wastewater before
entering the ammonia stripper (Melgaço, Meers and Mota, 2020). Overall, modified ammonia
stripping is interesting alternative for pig slurry processing, especially for the recovery of N.
31
4.2.3.2 Phosphorous (P)
The data for the RE of phosphorous across the 55 data points was plotted (Figure 6). The
crystallization technology had the data points (21), which corresponds to 39% of the total points
selected for this study. Additionally, the whiskers for the crystallization (mean – 80%)
corresponds to 98-40% with an interquartile range of 93% to 69%. On the other hand, the
hydrothermal carbonization shows a same whisker and interquartile ranges (between 95 to 60
percent) due to the inadequate number of data points for phosphorous recovery (5 points).
However, the most varied range of values has been shown by the separation technology (mean
– 48%), with an interquartile range of 84% to 13% and whiskers in 90-10% range.
Figure 6. Comparison of RE various valorization technologies for phosphorous (x = mean, --- = median and dot
= datapoints)
The crystallization and pyrolysis have come forward as the best technology for the valorization
of P. In the studies for crystallization, the recovery of P via struvite precipitation (crystallization
in Figure 6) showed the most successful results. However, Kozik et al (2013) reported that the
presence of organic impurities may affect the final size and shape of struvite crystals).
Furthermore, to reduce the cost of struvite production, the use of magnesium compounds like
MgCO3 and Mg(OH)2 is required, however those reagents decrease the purity of the struvite
(Huang et al, 2012). However, when used as a fertilizer, it prevents toxification by regulating
leaching of minerals into the soil, making it fit as a valorized product.
32
4.2.3.3 Potassium (K) and Organic Carbon (OC)
The data for potassium and organic carbon was very limited as only 13 data points were
available. Thus, a detailed RE graph was not prepared. For both nutrients, the hydrothermal
carbonization has shown appreciable results. In case of potassium, an average RE of 37% was
obtained for HTC and 16% for OC.
4.3 Risk-of-Bias
The risk of bias has been evaluated for the study (Figure 7) based on four parameters. Nearly
84% of the studies show “low risk”, 14% with “some concerns” and merely 2% shows “high
risk”.
Figure 7. Risk-of-bias assessment for the dataset
Most of the medium and high-risk studies concerns with the irregularity in reporting of the
results or error in measuring the final outcome. This estimate has been performed by comparing
among the values of particular technology in the dataset. If the concerned value is “too high”
or “too low” in comparison to the overall mean, the study will be placed under “risk” (See
annex 2 for detailed Risk-of-Bias assessment).
4.4 Quantitative analysis of studies
4.4.1 Ammonia Stripping
Due to the limited data availability on other nutrients, only recovery of nitrogen is considered
in the data analysis. However, 3 data points were found across the studies for phosphorous
0 10 20 30 40 50 60 70 80 90 100
Randomization process
Mising outcome data
Measurement of the outcome
Selection of the reported result
Overall Bias
Low risk Some concerns High risk
33
recovery with an average RE of 95%. Seven studies with 9 data points were available about
nutrient recovery via ammonia stripping (Figure 8).
Figure 8. Trend of valorization against initial product for nitrogen recovery across studies (values in dg/L)
The effect was found from 7 studies with a mean difference of 25 dg/L (95% CI: 10, 40) and
an overall effect of Z = 3.3% (p = 0.0008). This value of MD shows a significant inclination
towards the valorized product in comparison with initial (raw) product. This is due to ability to
form chemical building blocks (generally ammonium sulfate) which is suitable for production
of fertilizers and other chemical products (Brienza et al, 2020). The value of I2 corresponds to
maximum heterogeneity. The significantly higher values of MD reported by the studies of
Huang et al (2019) and Ippersiel et al (2012) intensifies heterogeneity. This is due to influence
of process variables (temperature, pH, scale, air-to-water ratio) resulting in varied SD.
Excluding these values, an I2 of 85% will be obtained.
4.4.2 Pyrolysis
Data about pyrolysis were collected from a total of 10 studies across 19 data points. Moreover,
a variety of biochar synthesized from a temperature ranging between 350oC to 850oC was taken
into account. The recovery for phosphorous is only considered for data analysis as insufficient
data points available in case of nitrogen recovery (only 1 data point for N). For phosphorous,
6 data studies across 12 data points were analyzed on RevMan (Figure 9). Furthermore, an
average RE of 45-47% was obtained for potassium across 5 data points.
A random effect with MD of 19 mg/g (95% CI: 13, 25) and an overall effect of Z = 6.3 (p <
0.00001) were determined. In comparison with the initial product, valorized product has shown
more favourability. This is because organic P in biomass proceed through compositional
transformations during process, in which breakdown of phytate (phytic acid bound to mineral)
occurs followed by the reoccurrence of inorganic metal-P consortiums (Sun et al, 2018).
34
Figure 9. Trend of valorization against initial product for phosphorous recovery across pyrolysis (values in
mg/g)
However, unlike ammonia stripping, the resulting heterogeneity in this case is not because of
variability in published data. If the specific case of Uchimiya and Hiradate (2014) (4 data
points) is considered for heterogeneity assessment, an overall I2 = 97% is obtained. Even
though the actual reason of this is unknown, differences in valorization temperatures, gas flows
and particle heating time could result in a significant effect on the I2 value.
4.4.3 Crystallization
The valorization of pig manure via crystallization contributes to maximum number of studies
in the dataset (n = 12). Furthermore, the studies correspond to 29 data points (23 for
phosphorous (Figure 11) and 6 for nitrogen (Figure 10) which are around 25% of all data points
considered in the entire meta-analysis. Additionally, 2 datapoints have been removed
considering the “high risk” in risk-of-bias studies.
Figure 10. Trend of valorization against initial product for nitrogen recovery across crystallization (values in
mg/kg)
For nitrogen recovery, a MD of 295 mg/kg (95% CI: 155, 435) is obtained with an overall
effect of Z = 4.1 (p < 0.0001). Even though the results favor the valorized product to be more
feasible (Figure 9), the overall reliability on the data is less as the dataset only considers 3
publications. This could also be one of the reasons of high heterogeneity across the studies. On
the other hand, recovery of N in process is significant as reaction dynamics for struvite
precipitation also requires NH3 to be present.
35
Figure 11. Trend of valorization against initial product for phosphorous recovery across crystallization (values
in mg/g).
For the phosphorous recovery via crystallization, a total of 21 data points across 10 papers were
observed. An average MD of 400 mg/kg (95% CI: 380, 420) is obtained with an overall effect
of Z = 39 (p < 0.00001) (Figure 11). As an interpretation, the use of precipitation using oxides
and sulphates of Al, Ca and Mg is found to be particularly relevant. However, the software is
only designed for considering the statistical values (input by user) and no co-relation has been
designed for considering intangibles factors (such as environmental effects, feasibility, capital
costs, etc.) while comparing the overall difference. Furthermore, a heterogeneity resulting due
to variation of factors such as molar ratio of Mg:NH4:P, pH and aeration rate value across
database.
4.4.4 Hydrothermal Carbonization
The use of hydrothermal carbonization for valorization was evaluated across 9 studies with 19
data points (8 for phosphorous, 6 for nitrogen, 3 for potassium and 2 for organic carbon). For
P, average MD of 0.22 g/kg (95% CI: 0.15, 0.28) is obtained with an overall effect of Z = 6 (p
< 0.00001) (Figure 12). This value shows slight favourability of valorized product over initial
product. Furthermore, the heterogeneity of the database could be reduced to 90% if the two
highest values corresponding to Song et al (2019) and Wang et al (2020) are not considered.
The variation in database is a result of initial synthesis temperature for the production of
hydrochars (ranging between 150oC – 350oC).
36
Figure 12. Trend of valorization against initial product for nitrogen recovery across hydrothermal carbonization
(values in g/kg)
The phosphorous recovery indicates an overall MD of 3.6 g/kg (95% CI: 2.8, 4.5) is obtained
with an overall effect of Z = 8.8 (p < 0.00001) (Figure 13). This is due to the ability of
phosphorus being contained within the solid hydrochars which could be later leached out using
acid extraction (Heilmann et al, 2014). Even though only a slight inclination towards valorized
product is shown by the study (which is limited to nutrients recovery), the hydrochars could be
used for a variety of applications ranging from production of biofuel to use as an adsorbent
(Libra et al, 2011). However, in the case of Qiao et al (2011), the inverse in the favorability
could be observed which an average mean corresponding to -7.9 g/kg. This is because of
disruption of cells due to treatment, releasing phosphorous from the biomass waste into the
supernatant liquid.
Figure 13. Trend of valorization against initial product for phosphorous recovery across hydrothermal
carbonization (values in g/kg)
4.4.5 Separation
The study mentioned under the separation process combines the data in quick wash process,
distillation, and dialysis for efficient recovery of phosphorous and nitrogen. A total of 5 studies
consisting of 14 data points (7 for nitrogen and 7 for phosphorous).
In case of nitrogen (Figure 14), an average MD of 28 mg/dL (95% CI: -84, 28) is obtained with
an overall effect of Z = 0.9 (p = 0.3). The overall comparison listed initial product as a better
37
option over valorized product due to the quick wash process, which leaves most of the nitrogen
in the washed manure solids (LPELC 2019). However, the data studies also focus on two more
technologies, distillation and dialysis, which gives a positive MD strengthening valorized
product. Furthermore, if the consideration of intangible elements (socio-economic aspects) is
taken, the use of vacuum membrane distillation (VMD) was used without pH adjustment and
proved successful for nitrogen recovery, overall favouring the valorized product (Shi et al,
2020).
Figure 14. Trend of valorization against initial product for nitrogen recovery across separation processes (values
in mg/dL)
For phosphorous (Figure 15), an average MD of 6.2 mg/L (95% CI: -30.7, 18.2) is obtained
with an overall effect of Z = 0.50 (p = 0.62). The heterogeneity could further be reduced
significantly by excluding the study performed by Shi et al (2018). The technologies such as
quick wash process have shown a significant recovery of 90% of phosphorous, however the
co-recovery of nitrogen was not effectively analyzed (Szoegi, Vanotti and Hunt, 2015). The
phosphorous recovery could be significantly increased, if membrane processes concentrates
phosphate which could be coupled with other processes like crystallization (Xie et al, 2014).
Figure 15. Trend of valorization against initial product for phosphorous recovery across separation processes
(values in mg/L)
4.4.6 Biological
For the biological processes, the combination of studies done under composting, anaerobic
digestion (using digestate as a nutrient source), nutrients uptake by algae and others are
38
evaluated. In total, a database consisting of 9 studies with 21 data points (8 for nitrogen and 9
for phosphorous).
Figure 16. Trend of valorization against initial product for nitrogen recovery across biological processes (values
in mg/L)
For the nitrogen recovery, the analysis has shown a significant focus towards the use of
valorized product. The average MD of 5.2 mg/L (95% CI: 1.9, 8.5) is obtained with a
heterogeneity of I² = 100% (p < 0.00001) (Figure 16). Furthermore, the overall effect Z has a
value of 3.1 (p < 0.002). It is important to note that the number of studies done on nutrient
recovery from algal uptake were significantly low. A possible explanation of this could be the
inefficiency of algal species in the selective recovery of nutrients from pig slurry. This is due
to dependency of alage on factors like contamination, inconsistent slurry components, and
unstable biomass production.
Figure 17. Trend of valorization against initial product for phosphorous recovery across biological processes
(values in mg/L)
An average MD of 1.7 mg/L (95% CI: -2.5, -0.9) is obtained with a heterogeneity of I² = 100%
(p < 0.00001) (Figure 17). Furthermore, the overall effect Z has a value of 4.2 (p < 0.0001).
The analysis of data suggests that the use of biological methods for phosphorous recovery has
not shown significant results across the studies. However, for process of composting, a slight
inclination towards the valorized product is seen (Raza et al, 2019; Zhang and He, 2005) due
to formation of phosphorus pentoxide (P2O5). This results in an increase of P content in
compost (Hanrinth and Polprasert, 2016).
39
4.5 Economics
The feasibility of a proposed solution for a nutrient recovery goes hand in hand with the
economical assessment and cost benefit achieved by it. In this section, a brief overview on the
market demand of the fertilizers as well as the economic assessment of the proposed technology
will be discussed.
4.5.1 Economic evaluation of fertilizers
The value of global market for the consumption of phosphate rock was marked at 24.4 billion
US dollars and is expected to continue growing at a cumulative average growth rate of 7.1%
from 2019 to 2025 (GVR, 2019). The use of phosphate-based chemicals in production of
detergents, pesticides, metal coatings, toothpaste, matches, and water softeners is one of the
reasons of this growth (especially in underdeveloped and developing countries). However, the
agricultural industry drives the rock’s market, surging over 4% from 1.2% in last decade (GMI,
2019). The expected increase is a result of two major factors:
• The rise in usage of fertilizers due to increasing food production. It is expected that
nearly 68% of the world’s population will live in urban areas by 2050. The total world
fertilizer market is estimated at 200 billion US$ (20 – 25 billion €/year for European
Union) (UNDESA, 2020). That of phosphate fertilizers is around 50-70 billion
US$/year. This particular factor also puts external pressure on demand for processed
food, hence propelling the growth of phosphate rock market (UNDESA, 2020).
• Phosphate rock is also used as a preservative in food industry (Indexmundi, 2020) for
maintaining taste and increasing shelf life of processed food. Its growth is further
expected to rise exponentially in upcoming decade.
Furthermore, the addition of phosphate in animal feed also contributes significantly to
increasing market demand. The revenue of animal feed segment is expected to grow by 8.5%
in between 2020 to 2025 (The World Bank, 2020). In feed, it is mainly used in forms of
monocalcium phosphate and calcium phosphate. However, use of phytate as an alternative for
feeds could further reduce the pressure on market demand for phosphorous rock.
The growth of phosphate market is noted to be highest in regions of Asia-Pacific. Increasing
awareness about product among the farmers, growing demand for harvesting and rising
agriculture in countries such as India and China, whose major part of gross domestic product
depends upon agriculture (13% for India) is also a significant factor to this increase.
40
Figure 18. Trend of market price (global) for fertilizers over the last 20 years (The World Bank, 2020).
The fertilizer prices overall showed a rather constant trend throughout the span of 20 years
(Figure 18), except for a sudden spike in 2007-2009. In October 2007, fertilizers prices rose
rapidly making an all-time high within a period of 10 months. Prices were driven essentially
by a supply imbalance and rapidly increasing demand, especially in Asia. At a point of time,
available supply could not fulfil the required demand of fertilizers, especially in China and
India. Furthermore, use of fertilizers to produce biofuels in Brazil, Europe and US also
contributed to this factor (IDFC, 2008). Increased livestock production created more demand
for grain and thus for fertilizers. Grain reserves became historically low and prices rose sharply
(IDFC, 2008). Another factor was China's imposition of high tariffs on fertilizer exports and
devaluation of the U.S. dollar in 2007 and 2008 (The World Bank, 2008). Energy prices also
increased, affecting overall cost of production of ammonia (IDFC, 2008).
Following the rapid increase, a sharp decline was also noticed in late 2008. This was due to the
collapse of the global credit market, trade recession, and slowdown in world economic growth
which led to a fall in demand of fertilizers and accumulation of stocks (IDFC, 2008). However,
the price of potash continued to be relatively high due to its shortage and difficulties in
transporting (IDFC, 2008).
0
100
200
300
400
500
600
700
800
Jul-
00
Jul-
01
Jul-
02
Jul-
03
Jul-
04
Jul-
05
Jul-
06
Jul-
07
Jul-
08
Jul-
09
Jul-
10
Jul-
11
Jul-
12
Jul-
13
Jul-
14
Jul-
15
Jul-
16
Jul-
17
Jul-
18
Jul-
19
Jul-
20
Pri
ces
(EU
R/M
T)
Years
Urea triple superphosphate (TSP)
Rock Phosphate Potassium Chloride
diammonium phosphate (DAP)
41
4.5.2 Economic assessment of available technologies
• Ammonia Stripping: From study done by Errico et al (2018), the total capital
investment is about 4.87 million EUR (total bare module cost of about 1.95 million
EUR) treating 30,000 kg/h of digestate. Furthermore, the cost of chemicals and energy
were found out to be less than 1 million EUR. Having the average recovery efficiency
of 97% and current ammonium sulphate price of 462 EUR/MT, the overall benefit of
1.4 EUR per m3 of digestate is obtained (Errico et al, 2018). In another study, Hildago
et al (2002) suggested 1927 EUR/kg-raw manure treatment cost by using ammonia
stripping.
• Pyrolysis: The total capital cost for setting up a pyrolysis plant for biochar production
from manure was estimated to be 90,000 EUR for a daily inflow of 230 kg/h (Li et al,
2016). Furthermore, the yearly operation and maintenance costs corresponds to around
60,000 EUR/year. Considering the market price of biochar at 50 EUR/MT, the yearly
profit of 24,000 EUR could be achieved (Li et al, 2016).
• Struvite Precipitation: According to the study performed by Shu et al (2006), a total
profit of ranging from -8000 EUR to $90000 EUR/yr (the negative value indicated a
loss) for an average inflow of 50000 m3/d. Assuming overall capital and operation and
maintenance costs are calculated to be 2 million EUR, the payback period will be less
than 5 years. However, in another study done by Yetilmezsoy et al (2017), the average
cost for recovering struvite was 1753 EUR/kg.
• Hydrothermal Carbonization: The cost of setting up an hydrothermal carbonization
plant for production of biofuel for 110 MW coal power plant was estimated to be around
10 million EUR with an average operation and maintenance costs (excluding raw
materials) 6 million EUR/year MT (Saba, McGaughy and Reza, 2019). The breakdown
selling price of the fuel obtained from this source ranges between 100 to 113 EUR/MT
(Saba, McGaughy and Reza, 2019).
42
Table 6. Economic comparison for various valorization technologies
Ammonia
Stripping
Pyrolysis Struvite
Precipitation
Hydrothermal
Carbonization
Capital Costs 4-5 million EUR 1–15 million
EUR
1-1.5 million EUR 10 million EUR
Operational
Costs (per year)
1 million EUR 1-8 million
EUR
1 million EUR 5-8 million EUR
Profit (per year) 1.5-1.7 million
EUR
1-5 million
EUR
50000 – 1 million
EUR
1-3 million EUR
Payback Period 5-10 years 5-12 years 2-5 years 10-12 years
Recovered
Products
Ammonia N, P, K,
biofuels
N, P, K Biofuel, Carbon
The economics of a particular technology depends on various factors such as scale,
transportation costs, availability of raw materials, price of raw material, choice of reactor,
energy input requirement and the requirement of separation processes to retrieve products.
Hence, it is not possible to accurately predict cost effectiveness of any process without a
detailed techno-economic analysis comparing all process on a homogenized scale.
However, a brief comparison in between the technologies (Table 6) predicts pyrolysis and
struvite precipitation as most promising valorization mechanisms. This is due to their
comparative low capital and maintenance costs, high profit percentage and smaller payback
periods. Furthermore, the availability of multiple nutrients from both the processes adds to the
benefit. However, in some of the cases of pyrolysis, capital cost could rise as high as 12 million
EUR and overall cost of production (per kg biochar) is significantly high. However, these
processes are coupled with the production of biofuel making overall product economical.
For standalone recovery of nitrogen, ammonia stripping proves to be one of the most efficient
methods. Furthermore, initial capital cost is relatively inexpensive considering the treatment
scale. However, operational and maintenance cost could be significantly high as it is an energy
intensive process. However, these costs could be further reduced if the influent is preheated by
using the waste heat (of system) or renewable energy source. Additionally, ammonia stripping
43
could also be coupled up with technologies like crystallization for the recovery of other
nutrients, hence increasing the cost benefits.
4.6 Overall techno-economic comparison
Presently, only crystallization, ammonia stripping, pyrolysis, and separation techniques (such
as membrane distillation) have been applied at full-scale for nutrient recovery from pig manure.
While the investment costs of ammonia stripping are relatively low, its operational
expenditures are much higher than crystallization. The main operational costs for
crystallization are related to dosing of chemicals – such as calcium and magnesium hydroxides,
while main costs for stripping are air requirements and energy. Optimization of these
parameters is therefore of high interest.
The valorization by using pyrolysis seems as the promising technology, because of potential
benefits of soil carbon sequestration, heavy metal immobilization, improvement in soil quality,
increased crop yields, mitigation of nutrient leaching, and organic contaminant remediation.
However, it can be questioned under ecological assessment whether pyrolysis of a sustainable
treatment option is (due to involvement of combustion process) and if this should be
encouraged or not. Furthermore, techniques such as composting is relatively simple, but the
overall cost of this treatment is still significant as large surface areas are required, making its
potential implementation very region-specific. Further research to improve the economic and
technical feasibility of this technology is recommended.
Lastly from a technical point of view, further calibration in all technologies is required to
minimize operational and maintenance costs, specifically for chemicals and energy, in order to
produce high-quality bio-based fertilizers. Furthermore, struvite precipitation, ammonia
stripping and pyrolysis came forward as best available and most established technologies for
nutrient recovery in terms of fertilizer marketing potential, technical performance, and overall
economics.
44
Conclusions
A meta-analysis and short economic evaluation were conducted for different valorization
mechanisms which have stated raw pig manure as a limiting product for fulfilling the nutrients
requirements as a fertilizer. All valorization mechanisms showed appreciable results for N and
P recovery with average REs of 79% and 85%. Recent studies (year 2015-2020) are mainly
focused towards crystallization (15%), ammonia stripping (15%) and pyrolysis (15%) along
with increasing trend of hydrothermal carbonization (25%). Furthermore, the recent studies
were led by the parts of Europe (Denmark, Spain and Belgium; 55% of total studies) and from
the parts of Chinese subcontinent (28% of total studies). Only 7 studies have demonstrated the
performance at pilot or full scale. Moreover, most technologies have reported to obtain
remarkable recovery efficiencies for standalone N or P, however, only crystallization has
shown >90% RE for both at the same time. Furthermore, technologies such as ammonia
stripping and pyrolysis show best results for standalone recovery (>96%). The data analysis
done by RevMan showed an overall effect in the range of 0.5 – 32 for all the cases, confirming
the statistical significance of the database. Additionally, values of RevMan shown significant
inclination towards the valorized product in comparison with initial (raw) product.
Furthermore, the relative probability was noted to be <0.05 for all the technologies (except
separation), hence confirming the significance that the dataset contains the experimental values
and the values are not merely obtained by chance. Additionally, the economic aspect was also
evaluated, in which pyrolysis and crystallization has come forward as the most promising
techniques with the payback period of nearly 5-7 years with an initial capital and operation and
maintenance costs ranging between 3 – 5 million EUR. Overall assessment categorizes struvite
precipitation, ammonia stripping and pyrolysis came forward as best available and most
established technologies for nutrient recovery in techno-economic aspects. However, further
calibration in all technologies is recommended to minimize operation and maintenance costs
along with promoting the use of multiple valorization techniques (in combination) to enhance
the overall RE.
45
References
Achat, D.L., Sperandio, M., Daumer, M.L., Santellani, A.C., Prud'Homme, L., Akhtar, M. and
Morel, C. (2014) ‘Plant-availability of phosphorus recycled from pig manures and dairy
effluents as assessed by isotopic labeling techniques’, Geoderma, 232, pp.24-33.
Ackerman, J.N., Cicek, N. and Oleszkiewicz, J. (2012) ‘Anaerobic fermentation of pig manure to
increase phosphorus removal by struvite precipitation’, Biological Engineering
Transactions, 5(4), pp.177-189.
Akinbowale, O.L., Peng, H., Grant, P. and Barton, M.D. (2007) ‘Antibiotic and heavy metal
resistance in motile aeromonads and pseudomonads from rainbow trout (Oncorhynchus
mykiss) farms in Australia’, International Journal of Antimicrobial Agents, 30(2), pp.177-182.
Al‐Kanani, T., Akochi, E., Mackenzie, A.F., Alli, I. and Barrington, S. (1992) ‘Organic and
inorganic amendments to reduce ammonia losses from liquid hog manure’, Journal of
Environmental Quality, 21(4), pp.709-715.
Amery, F. and Schoumans, O.F. (2014) ‘Agricultural phosphorus legislation in Europe’, Institute
for Agricultural and Fisheries Research (ILVO), Alterra Wageningen UR.
Anon. (2011) ‘Decreet van 22 december 2006 houdende de bescherming van water tegen de
verontreiniging door nitraten uit agrarische bronnen’ Available at:
https://codex.vlaanderen.be/PrintDocument.ashx?id=1015329&datum=&geannoteerd=false&
print=false. (Accessed: 16 August 2020)
Arthurson, V. (2009) ‘Closing the global energy and nutrient cycles through application of biogas
residue to agricultural land–potential benefits and drawback’, Energies, 2(2), pp.226-242.
Ashley, K.I., Mavinic, D.S. and Koch, F.A. (2009) ’International Conference on Nutrient
Recovery from Wastewater Streams’, International Conference on Nutrient Recovery from
Wastewater Streams (April 30, 2009: Vancouver, BC). IWA Publishing.
Azevedo, J. and Stout, P.R. (1974) ‘Farm animal manures: An overview of their role in the
agricultural environment’, California Agricultural Experiment Station and Extension Service,
Division of Agricultural Sciences, University of California, 44.
Azuara, M., Kersten, S.R. and Kootstra, A.M.J. (2013) ‘Recycling phosphorus by fast pyrolysis of
pig manure: concentration and extraction of phosphorus combined with formation of value-
added pyrolysis products’, Biomass and Bioenergy, 49, pp.171-180.
Bass, L., Liebert, C.A., Lee, M.D., Summers, A.O., White, D.G., Thayer, S.G. and Maurer, J.J.
(1999) ‘Incidence and characterization of integrons, genetic elements mediating multiple-drug
46
resistance, in avian Escherichia coli.’, Antimicrobial Agents and Chemotherapy, 43(12),
pp.2925-2929.
Beauchamp, E.G. (1983) ‘Response of corn to nitrogen in preplant and side dress applications of
liquid dairy cattle manure’, Canadian Journal of Soil Science, 63(2), pp.377-386.
Bhamidimarri, S.R. and Pandey, S.P. (1996) ‘Aerobic thermophilic composting of piggery solid
wastes’, Water Science and Technology, 33(8), pp.89-94.
Biochar for Sustainable Soils (2020) ‘China - Biochar for Sustainable Soils’, Available at:
https://biochar.international/the-biochar-for-sustainable-soils-b4ss-project/china/. (Accessed:
16 August 2020).
Borenstein, M., Hedges, L.V., Higgins, J.P.T. and Rothstein, H.R. (2010) ‘A basic introduction to
fixed-effect and random-effects models for meta-analysis’, Research Synthesis Methods, 1(2),
pp.97–111.
Bridgwater, A.V. and Peacocke, G.V.C. (2000) ‘Fast pyrolysis processes for biomass’, Renewable
and Sustainable Energy Reviews, 4, pp.1‐73.
Bridgwater, A.V., Meier, D. and Radlein, D. (1999) ‘An overview of fast pyrolysis of biomass’,
Organic Geochemistry, 30, pp.1479‐1493.
Brienza, C., Sigurnjak, I., Michels, E., & Meers, E. (2020) ‘Ammonia Stripping and Scrubbing
for Mineral Nitrogen Recovery’, Biorefinery of Inorganics, pp.95–106.
Brumm, M.C. and Sutton, A.L. (1979) ‘Effect of copper in swine diets on fresh waste composition
and anaerobic decomposition’, Journal of Animal Science, 49(1), pp.20-25.
Buelna, G., Dubé, R. and Turgeon, N. (2008) ‘Pig manure treatment by organic bed
biofiltration’, Desalination, 231(1-3), pp.297-304.
Burns, R.T. and Moody, L.B. (2002) ‘Phosphorus recovery from animal manures using optimized
struvite precipitation’, Proceedings of Coagulants and Flocculants: Global Market and
Technical Opportunities for Water Treatment Chemicals (Chicago, Illinois: May 22-24, 2002).
The University of Tennessee.
Burns, R.T., Moody, L.B., Celen, I. and Buchanan, J.R. (2003) ‘Optimization of phosphorus
precipitation from swine manure slurries to enhance recovery’, Water Science and
Technology, 48(1), pp.139-146.
Camargo-Valero, M. A., De Clercq, L., Delvigne, F., Haumont, A., Lebuf, V., Meers, E., Michels,
E., Raesfeld, U., Ramirez-Sosa, D. R., Ross, A. B., Schoumans, O., Snauwaert, E., Tarayre,
C., Tarayre, N., Vandaele, E., Velthof, G., Williams, P. T. and Tech, G. A. (2015) ‘Techniques
47
for nutrient recovery from manure and slurry’, Biorefine (Europe: May 13, 2015).
https://doi.org/10.13140/RG.2.1.2190.7602.
Cang, L., Wang, Y.J., Zhou, D.M. and Dong, Y.H. (2004) ‘Heavy metals pollution in poultry and
livestock feeds and manures under intensive farming in Jiangsu Province, China’, Journal of
Environmental Sciences, 16(3), pp.371-374.
Caraco, N.F. (1995) ‘Influence of human populations on phosphorus transfers to aquatic systems:
a regional scale study using large rivers’, Scope-Scientific Committee On Problems Of The
Environment International Council Of Scientific Unions, 54, pp.235-244.
Cattaneo, M., Finzi, A., Guido, V., Riva, E. and Provolo, G. (2019) ‘Effect of ammonia stripping
and use of additives on separation of solids, phosphorus, copper and zinc from liquid fractions
of animal slurries’, Science of the Total Environment, 672, pp.30-39.
Cerrillo, M., Palatsi, J., Comas, J., Vicens, J. and Bonmatí, A. (2015) ‘Struvite precipitation as a
technology to be integrated in a manure anaerobic digestion treatment plant–removal
efficiency, crystal characterization and agricultural assessment’, Journal of Chemical
Technology & Biotechnology, 90(6), pp.1135-1143.
Chen, Y. X., Huang, X. D., Han, Z. Y., Huang, X., Hu, B., Shi, D. Z. and Wu, W. X. (2010) ‘Effects
of bamboo charcoal and bamboo vinegar on nitrogen conservation and heavy metals
immobility during pig manure composting’, Chemosphere, 78(9), pp.1177-1181.
Chen, Y.X., Huang, X.D., Han, Z.Y., Huang, X., Hu, B., Shi, D.Z. and Wu, W.X. (2010) ‘Effects
of bamboo charcoal and bamboo vinegar on nitrogen conservation and heavy metals
immobility during pig manure composting’, Chemosphere, 78(9), pp.1177-1181.
Chowdhury, R.B., Moore, G.A., Weatherley, A.J. and Arora, M. (2014) ‘A review of recent
substance flow analyses of phosphorus to identify priority management areas at different
geographical scales’, Resources, Conservation and Recycling, 83, pp.213-228.
Christel, W., Bruun, S., Magid, J. and Jensen, L.S. (2014) ‘Phosphorus availability from the solid
fraction of pig slurry is altered by composting or thermal treatment’, Bioresource
Technology, 169, pp.543-551.
Christel, W., Bruun, S., Magid, J., Kwapinski, W. and Jensen, L.S. (2016) ‘Pig slurry acidification,
separation technology and thermal conversion affect phosphorus availability in soil amended
with the derived solid fractions, chars or ashes’, Plant and Soil, 401(1-2), pp.93-107.
Christel, W., Zhu, K., Hoefer, C., Kreuzeder, A., Santner, J., Bruun, S., Magid, J. and Jensen, L.S.
(2016) ‘Spatiotemporal dynamics of phosphorus release, oxygen consumption and greenhouse
48
gas emissions after localised soil amendment with organic fertilisers’, Science of the Total
Environment, 554, pp.119-129.
Commodity Markets. (2020) The World Bank. Available at:
https://www.worldbank.org/en/research/commodity-markets (Accessed: 10 July 2020).
Conti, F., Toor, S.S., Pedersen, T.H., Seehar, T.H., Nielsen, A.H. and Rosendahl, L.A. (2020)
‘Valorization of animal and human wastes through hydrothermal liquefaction for biocrude
production and simultaneous recovery of nutrients’, Energy Conversion and
Management, 216, pp.112925.
Council Directive 91/676/EEC of 12 December 1991 concerning the protection of waters against
pollution caused by nitrates from agricultural sources. Council of the European Union.
Daumer, M.L., Santellani, A.C., Capdevielle, A. and Diara, A. (2013) ‘Phosphorus recycling as
struvite from pig manure. Influence of process parameters’, In RAMIRAN 2013. 15th
International Conference, (Versailles, France : 3-5 June. 2013) Proceedings. Institut National
de la Recherche Agronomique (INRA).
De Ridder, M., De Jong, S., Polchar, J. and Lingemann, S. (2012) ‘Risks and opportunities in the
global phosphate rock market: Robust strategies in times of uncertainty’, The Hague Centre
for Strategic Studies, Hague, The Netherlands .
Deeks, J.J., Higgins, J.P. and Altman, D.G. (2008) ‘Analysing data andundertaking metaanalyses’
in Deeks JJ, Higgins JP, Altman DG. (ed.) Cochrane Handbook for Systematic Reviews of
Interventions: Cochrane Book Series. Chichester (UK): John Wiley & Sons, pp.244–649.
Desmidt, E., Ghyselbrecht, K., Monballiu, A., Rabaey, K., Verstraete, W. and Meesschaert, B.D.
(2013) ‘Factors influencing urease driven struvite precipitation’, Separation and Purification
Technology, 110, pp.150-157.
Dickey, E.C. and Vanderholm, D.H. (1975) ‘Water Quality and Management Characteristics of
Feedlot Runoff Holding Ponds’, Presented at the 1975 Winter Meeting in, American Society of
Agricultural Engineers, Chicago, Illinois December 15-18, pp. 6.
Ehmann, A., Bach, I.M., Laopeamthong, S., Bilbao, J. and Lewandowski, I. (2017) ‘Can phosphate
salts recovered from manure replace conventional phosphate fertilizer?’, Agriculture, 7(1),
pp.1.
Ekpo, U., Ross, A.B., Camargo-Valero, M.A. and Fletcher, L.A. (2016) ‘Influence of pH on
hydrothermal treatment of swine manure: Impact on extraction of nitrogen and phosphorus in
process water’, Bioresource Technology, 214, pp.637-644.
49
EPA, (2000) ‘Wastewater technology fact sheet — Ammonia stripping’.
https://www3.epa.gov/npdes/pubs/ammonia_stripping.pdf
Errico, M., Sotoft, L.F., Nielsen, A.K. and Norddahl, B. (2018) ‘Treatment costs of ammonia
recovery from biogas digestate by air stripping analyzed by process simulation’, Clean
Technologies and Environmental Policy, 20(7), pp.1479-1489.
European Commission. (2018) ‘Valorization of the digestate from pig manure as new fertilizers
with an organic/mineral base and gradual release’, Life Mix Fertilizer, ID: LIFE12
ENV/ES/000689.
European Commission. (2019) ‘Use of Phosphorus and its resource availability’, Natural Resources
- Environment - European Commission. Available at:
https://ec.europa.eu/environment/natres/phosphorus.htm (Accessed: 10 July 2020).
European Environment Agency (2020) ‘Nitrate Directive’, Available at:
https://www.eea.europa.eu/archived/archived-content-water-topic/water-
pollution/prevention-strategies/nitrate-
directive#:~:text=In%201991%2C%20the%20EU%20introduced,nitrate%20vulnerable%20z
ones%20(NVZ's). [Date Accessed - 16 August 2020].
Evans, S.D., Goodrich, P.R., Munter, R.C. and Smith, R.E., 1977. Effects of solid and liquid beef
manure and liquid hog manure on soil characteristics and on growth, yield, and composition of
corn. Journal of Environmental Quality, 6(4), pp.361-368.
Gascó, G., Paz-Ferreiro, J., Álvarez, M.L., Saa, A. and Méndez, A. (2018) ‘Biochars and
hydrochars prepared by pyrolysis and hydrothermal carbonisation of pig manure’, Waste
Management, 79, pp.395-403.
Gellings, C.W. and Parmenter, K.E. (2016) ‘Energy efficiency in fertilizer production and use’,
Efficient Use and Conservation of Energy; Gellings, CW, Ed.; Encyclopedia of Life Support
Systems, pp.123-136.
Global Market Insights (GMI). (2019) ‘Phosphate Market Size, Industry Analysis Report, Regional
Outlook, Application Development Potential, Price Trends, Competitive Market Share &
Forecast, 2020 – 2026’, Bulk and Specialty Chemicals. Available at:
https://www.gminsights.com/industry-analysis/phosphate-market (Accessed: 10 August
2020).
Grand View Research (GVR). (2019) ‘Phosphate Rock Market Size, Share & Trends Analysis
Report By Application (Animal Feed, Fertilizers), By Region (North America, Europe, Asia
Pacific, CSA, MEA), Vendor Landscape, And Segment Forecasts, 2019 – 2025’, Market
50
Analysis Report. Available at: https://www.grandviewresearch.com/industry-
analysis/phosphate-rock-market (Accessed: 10 August 2020).
Guštin, S. and Marinšek-Logar, R. (2011) ‘Effect of pH, temperature and air flow rate on the
continuous ammonia stripping of the anaerobic digestion effluent’, Process Safety and
Environmental Protection, 89 (1), pp.61-66.
Harford, T. (2017) ‘How fertiliser helped feed the world’, BBC News. Available at:
https://www.bbc.com/news/business-38305504 (Accessed: 10 July 2020).
Heilmann, S.M., Molde, J.S., Timler, J.G., Wood, B.M., Mikula, A.L., Vozhdayev, G.V.,
Colosky, E.C., Spokas, K.A. and Valentas, K.J. (2014) ‘Phosphorus reclamation through
hydrothermal carbonization of animal manures’, Environmental science &
technology, 48(17), pp.10323-10329.
Hidalgo, D., Corona, F., Martín-Marroquín, J.M., del Álamo, J. and Aguado, A. (2016) ‘Resource
recovery from anaerobic digestate: struvite crystallisation versus ammonia
stripping’, Desalination and Water Treatment, 57(6), pp.2626-2632.
Hjorth, M., Christensen, K. V., Christensen, M. L., Sommer, S. G. (2010) ‘Solid–liquid separation
of animal slurry in theory and practice. A review’, Agronomy for Sustainable Development,
30(1), pp.153–180.
Hölzel, C.S., Müller, C., Harms, K.S., Mikolajewski, S., Schäfer, S., Schwaiger, K. and Bauer, J.
(2012) ‘Heavy metals in liquid pig manure in light of bacterial antimicrobial
resistance’, Environmental Research, 113, pp.21-27.
Huang, H., He, L., Zhang, Z., Lei, Z., Liu, R. and Zheng, W. (2019) ‘Enhanced biogasification from
ammonia-rich swine manure pretreated by ammonia fermentation and air
stripping’, International Biodeterioration & Biodegradation, 140, pp.84-89.
Huang, H., Xiao, D., Liu, J., Hou, L. and Ding, L. (2015) ‘Recovery and removal of nutrients from
swine wastewater by using a novel integrated reactor for struvite decomposition and
recycling’, Scientific Reports, 5, pp.10183.
Huang, W., Zhao, Z., Yuan, T., Huang, W., Lei, Z. and Zhang, Z. (2017) ‘Low-temperature
hydrothermal pretreatment followed by dry anaerobic digestion: A sustainable strategy for
manure waste management regarding energy recovery and nutrients availability’, Waste
Management, 70, pp.255-262.
IDFC (2008) ‘World fertilizer prices drop dramatically after soaring to all-time high‘, EurekAlert.
Available at: https://www.eurekalert.org/pub_releases/2008-12/i-wfp121608.php. (Accessed:
16 August 2020)
51
Ileleji, K. E., Martin, C. and Jones, D. (2015) ‘Basics of Energy Production through Anaerobic
Digestion of Livestock Manure’, Bioenergy – Biomass to biofuels. Academic Press, pp. 287-
295.
IndexMundi, (2020) ‘Diammonium phosphate (DAP) fertilizer price over last year’, Available at:
https://www.indexmundi.com/commodities/?commodity=urea. (Accessed: 16 August 2020)
Insam, H., Gómez-Brandón, M. and Ascher, J. (2015) ‘Manure-based biogas fermentation
residues–Friend or foe of soil fertility?’, Soil Biology and Biochemistry, 84, pp.1-14.
Ippersiel, D., Mondor, M., Lamarche, F., Tremblay, F., Dubreuil, J. and Masse, L. (2012) ‘Nitrogen
potential recovery and concentration of ammonia from swine manure using electrodialysis
coupled with air stripping’, Journal of environmental Management, 95, pp.165-169.
Jin, Y., Liang, X., He, M., Liu, Y., Tian, G. and Shi, J. (2016) ‘Manure biochar influence upon soil
properties, phosphorus distribution and phosphatase activities: a microcosm incubation
study’, Chemosphere, 142, pp.128-135.
Kebede-Westhead, E., Pizarro, C. and Mulbry, W.W. (2006) ‘Treatment of swine manure effluent
using freshwater algae: production, nutrient recovery, and elemental composition of algal
biomass at four effluent loading rates’, Journal of Applied Phycology, 18(1), pp.41-46.
Kornegay, E.T., Hedges, J.D., Martens, D.C. and Kramer, C.Y., 1976. Effect on soil and plant
mineral levels following application of manures of different copper contents. Plant and
Soil, 45(1), pp.151-162.
Kozik, A., Hutnik, N., Piotrowski, K., Mazienczuk, A. and Matynia, A. (2013) ‘Precipitation and
Crystallization of Struvite from Synthetic Wastewater under Stoichiometric Conditions’,
Advances in Chemical Engineering and Science, 3, pp.20–26.
Kruk, D. J., Elektorowicz, M. and Oleszkiewicz, J. A. (2014) ‘Struvite precipitation and phosphorus
removal using magnesium sacrificial anode’, Chemosphere, 101, pp.28–33.
Külling, D.R., Menzi, H., Kröber, T.F., Neftel, A., Sutter, F., Lischer, P. and Kreuzer, M. (2001)
‘Emissions of ammonia, nitrous oxide and methane from different types of dairy manure
during storage as affected by dietary protein content’, The Journal of Agricultural
Science, 137(2), pp.235-250.
Lal, R. (2013) ‘Food security in a changing climate’, Ecohydrology & Hydrobiology, 13(1), pp.8-
21.
Larson, B.G. (1991) ‘Saskatchewan pork industry manure management recommendations’,
Saskatchewan Pork Producers' Marketing Board, Saskatoon, SK, Canada.
52
Laureni, M., Palatsi, J., Llovera, M. and Bonmatí, A. (2013) ‘Influence of pig slurry characteristics
on ammonia stripping efficiencies and quality of the recovered ammonium‐sulfate
solution’, Journal of Chemical Technology & Biotechnology, 88(9), pp.1654-1662.
Li, H., Zhao, X., Zhang, T. and Kruse, A. (2019) ‘Hydrothermal Process for Extracting Phosphate
from Animal Manure’, Phosphorus Recovery and Recycling. Singapore: Springer, pp.377-389.
Li, J., Dai, J., Liu, G., Zhang, H., Gao, Z., Fu, J., He, Y. and Huang, Y. (2016) ‘Biochar from
microwave pyrolysis of biomass: A review’, Biomass and Bioenergy, 94, pp.228-244.
Li, X., Guo, J., Dong, R., Ahring, B.K. and Zhang, W. (2016) ‘Properties of plant nutrient:
comparison of two nutrient recovery techniques using liquid fraction of digestate from
anaerobic digester treating pig manure’, Science of the Total Environment, 544, pp.774-781.
Libra, J.A., Ro, K.S., Kammann, C., Funke, A., Berge, N.D., Neubauer, Y., Titirici, M.M.,
Fühner, C., Bens, O., Kern, J. and Emmerich, K.H. (2011) ‘Hydrothermal carbonization of
biomass residuals: a comparative review of the chemistry, processes and applications of wet
and dry pyrolysis’, Biofuels, 2(1), pp.71-106.
Liu, L., Pang, C., Wu, S. and Dong, R. (2015) ‘Optimization and evaluation of an air-recirculated
stripping for ammonia removal from the anaerobic digestate of pig manure’, Process Safety
and Environmental Protection, 94, pp.350-357.
Liu, R., Xing, L., Zhou, G. and Zhang, W. (2017) ‘What is meat in China?’, Animal Frontiers, 7(4),
pp.53-56.
Liu, Y.G., Zhou, M., Zeng, G.M., Wang, X., Li, X., Fan, T. and Xu, W.H. (2008) ‘Bioleaching of
heavy metals from mine tailings by indigenous sulfur-oxidizing bacteria: effects of substrate
concentration’, Bioresource Technology, 99(10), pp.4124-4129.
Lobo, M.G. and Dorta, E. (2019) ‘Utilization and Management of Horticultural Waste’, Postharvest
Technology of Perishable Horticultural Commodities, Woodhead Publishing, pp.639-666.
LPELC. (2020) ‘Extraction and Recovery of Phosphorus from Pig Manure Using the Quick Wash
Process’, Livestock and Poultry Environmental Learning Community. Available at:
https://lpelc.org/extraction-and-recovery-of-phosphorus-from-pig-manure-using-the-quick-
wash-process/ (Accessed: 10 July 2020).
Luján-Facundo, M.J., Iborra-Clar, M.I., Mendoza-Roca, J.A. and Also-Jesús, M. (2019)
‘Alternatives for the management of pig slurry: Phosphorous recovery and biogas
generation’, Journal of Water Process Engineering, 30, pp.100473.
53
Ma, L., Yuan, S., Ji, F., Wang, W. and Hu, Z.H. (2018) ‘Ammonia and phosphorous precipitation
through struvite crystallization from swine wastewater with high suspended solid’,
Desalination and Water Treatment, 116, pp.258-266.
MacLeod, M., Gerber, P., Mottet, A., Tempio, G., Falcucci, A., Opio, C., Vellinga, T., Henderson,
B. and Steinfeld, H. (2013) ‘Greenhouse gas emissions from pig and chicken supply chains –
A global life cycle assessment’, Food and Agriculture Organization of the United Nations
(FAO), Rome. Available at: http://www.fao.org/3/i3460e/i3460e.pdf (Accessed: 10 July 2020).
Madison, F., Kelling, K., Massie, L. and Good, L.W. (1995) ‘Guidelines for applying manure to
cropland and pasture in Wisconsin’, University of Wisconsin Cooperative Extension
Publications, Madison, WI.
Maggen, J., Carleer, R., Yperman, J., De Vocht, A., Schreurs, S., Reggers, G. and Thijsen, E. (2017)
‘Biochar Derived from the Dry, Solid Fraction of Pig Manure as Potential Fertilizer for Poor
and Contaminated Soils’, Sustainable Agriculture Research, 6, pp.167-184.
Marcato, C.E., Pinelli, E., Pouech, P., Winterton, P. and Guiresse, M. (2008) ‘Particle size and
metal distributions in anaerobically digested pig slurry’, Bioresource Technology, 99(7),
pp.2340-2348.
Marchetti, R., Castelli, F., Orsi, A., Sghedoni, L. and Bochicchio, D. (2012) ‘Biochar from swine
manure solids: influence on carbon sequestration and Olsen phosphorus and mineral nitrogen
dynamics in soil with and without digestate incorporation’, Italian Journal of Agronomy,
pp.189-195.
Martin, C., De la Noüe, J. and Picard, G. (1985) ‘Intensive cultivation of freshwater microalgae on
aerated pig manure’, Biomass, 7(4), pp.245-259.
Martinez-Almela, J. and Barrera, J.M. (2005) ‘SELCO-Ecopurin® pig slurry treatment system’,
Bioresource Technology, 96(2), pp.223-228.
McCarthy, G., Lawlor, P.G., Gutierrez, M. and Gardiner, G.E. (2013) ‘Assessing the biosafety risks
of pig manure for use as a feedstock for composting’, Science of the Total Environment, 463,
pp.712-719.
Melgaço, L.A., Meers, E. and Mota, C.R. (2020) ‘Ammonia recovery from food waste digestate
using solar heat-assisted stripping-absorption’, Waste Management, 113, pp.244-250.
Minnesota Pollution Control Agency (MPCA) (2020) ‘Land Application Of Manure’, Available
at: https://www.pca.state.mn.us/water/land-application-manure. (Accessed: 16 August 2020).
54
Mohedano, R.A., Velho, V.F., Costa, R.H.R., Hofmann, S.M. and Belli Filho, P. (2012) ‘Nutrient
recovery from swine waste and protein biomass production using duckweed ponds (Landoltia
punctata): southern Brazil’, Water Science and Technology, 65(11), pp.2042-2048.
Mulbry, W., Westhead, E.K., Pizarro, E. and Sikora, L. (2005) ‘Recycling of manure nutrients: use
of algal biomass from dairy manure treatment as a slow release fertilizer’, Bioresource
Technology, 96, pp.451-458.
Mulbry, W., Westhead, E.K., Pizarro, E. and Sikora, L. (2005) ‘Recycling of manure nutrients: use
of algal biomass from dairy manure treatment as a slow release fertilizer’, Bioresource
Technology, 96, pp.451-458.
Nagy, G.Á.B.O.R. and Wopera, A. (2012) ‘Biogas production from pig slurry-feasibility and
challenges’, Materials Science and Engineering, 37, pp.65-75.
Nasiru, A., Ibrahim, M.H. and Ismail, N. (2014) ‘Nitrogen losses in ruminant manure management
and use of cattle manure vermicast to improve forage quality’, International Journal of
Recycling of Organic Waste in Agriculture, 3(2), pp.57.
Oliveira, I., Blöhse, D. and Ramke, H. G. (2013) ‘Hydrothermal carbonization of agricultural
residues’, Bioresource Technology, 142, pp.138-146.
Ott, C. and Rechberger, H. (2012) ‘The European phosphorus balance’, Resources, Conservation
and Recycling, 60, pp.159-172.
Perera, P.A., Wei-Xiang, W.U., Ying-Xu, C.H.E.N. and Zhi-Ying, H.A.N. (2009) ‘Struvite
recovery from swine waste biogas digester effluent through a stainless steel device under
constant pH conditions’, Biomedical and Environmental Sciences, 22(3), pp.201-209.
Piveteau, S., Picard, S., Dabert, P. and Daumer, M.L. (2017) ‘Dissolution of particulate phosphorus
in pig slurry through biological acidification: A critical step for maximum phosphorus recovery
as struvite’, Water Research, 124, pp.693-701.
Provolo, G., Manuli, G., Finzi, A., Lucchini, G., Riva, E. and Sacchi, G.A. (2018) ‘Effect of pig
and cattle slurry application on heavy metal composition of maize grown on different
soils’, Sustainability, 10(8), pp.2684.
Qiao, W., Yan, X., Ye, J., Sun, Y., Wang, W. and Zhang, Z. (2011) ‘Evaluation of biogas production
from different biomass wastes with/without hydrothermal pretreatment’, Renewable
Energy, 36(12), pp.3313-3318.
Qureshi, A., Lo, K.V., Liao, P.H. and Mavinic, D.S. (2008) ‘Real-time treatment of dairy manure:
Implications of oxidation reduction potential regimes to nutrient management
strategies’, Bioresource Technology, 99(5), pp.1169-1176.
55
Raza, S.T., Zhu, B., Ali, Z. and Tang, J.L. (2019) ‘Vermicomposting by Eisenia fetida is a
sustainable and eco-friendly technology for better nutrient recovery and organic waste
management in upland areas of China’, Pakistan Journal of Zoology, 51(3), pp.1027.
Reddy, K.S. (2020) ‘Legislation limit for fertilizer usage’, Available at:
https://www.researchgate.net/post/Is_there_some_kind_of_legislation_to_limit_the_quantity
_of_phosphorus_applied_to_the_soil_in_your_country_or_state_We_need_a_better_one_to_
my_state. (Accessed: 16 August 2020).
Renee, C. (2013) ‘Phosphorus: Essential to Life—Are We Running Out?’, State of the Planet.
Available at: https://blogs.ei.columbia.edu/2013/04/01/phosphorus-essential-to-life-are-we-
running-out/ (Accessed: 10 July 2020)
Risberg, K., Cederlund, H., Pell, M., Arthurson, V. and Schnürer, A. (2017) ‘Comparative
characterization of digestate versus pig slurry and cow manure–chemical composition and
effects on soil microbial activity’, Waste management, 61, pp.529-538.
Ritchie, H. and Roser, M. (2019) ‘Meat and Dairy Production’, Our World in Data. Available at:
https://ourworldindata.org/meat-production (Accessed: 10 August 2020).
Román, S., Nabais, J. M. V., Laginhas, C., Ledesma, B. and González, J. F. (2012) ‘Hydrothermal
carbonization as an effective way of densifying the energy content of biomass’, Fuel
Processing Technology, 103, pp.78-83.
Saba, A., McGaughy, K. and Reza, M.T. (2019) ‘Techno-economic assessment of Co-hydrothermal
carbonization of a coal-miscanthus blend’, Energies, 12(4), pp.630.
Sáez, J.A., Clemente, R., Bustamante, M.Á., Yañez, D. and Bernal, M.P. (2017) ‘Evaluation of the
slurry management strategy and the integration of the composting technology in a pig farm–
Agronomical and environmental implications’, Journal of Environmental Management, 192,
pp.57-67.
Schoumans, O.F., Bouraoui, F., Kabbe, C., Oenema, O. and van Dijk, K.C. (2015) ‘Phosphorus
management in Europe in a changing world’, Ambio, 44(2), pp.180-192.
Shahbandeh, M. (2020) ‘Number of pigs worldwide 2020, by country’, Statista. Available
at:https://www.statista.com/statistics/263964/number-of-pigs-in-selected
countries/#:~:text=There%20were%20about%20677.6%20million,of%20the%20global%20p
ig%20population (Accessed: 10 August 2020).
Shi, L., Hu, Y., Xie, S., Wu, G., Hu, Z. and Zhan, X. (2018) ‘Recovery of nutrients and volatile
fatty acids from pig manure hydrolysate using two-stage bipolar membrane
electrodialysis’, Chemical Engineering Journal, 334, pp.134-142.
56
Shi, L., Xie, S., Hu, Z., Wu, G., Morrison, L., Croot, P., Hu, H. and Zhan, X. (2019) ‘Nutrient
recovery from pig manure digestate using electrodialysis reversal: Membrane fouling and
feasibility of long-term operation’, Journal of Membrane Science, 573, pp.560-569.
Shi, M., He, Q., Feng, L., Wu, L. and Yan, S. (2020) ‘Techno-economic evaluation of ammonia
recovery from biogas slurry by vacuum membrane distillation without pH adjustment’, Journal
of Cleaner Production, pp.121806.
Shrivastava, V., Mladenović, S., Brestovský, M., and Máček, R. (2019) ‘Analysis of medium- and
large-scale biogas installation in community farms, medium agricultural enterprises and large
installations in food processing industry (TAF/005/2018)’, International Investment Bank,
Moscow.
Shu, L., Schneider, P., Jegatheesan, V. and Johnson, J. (2006) ‘An economic evaluation of
phosphorus recovery as struvite from digester supernatant’, Bioresource Technology, 97(17),
pp.2211-2216.
Song, C., Zheng, H., Shan, S., Wu, S., Wang, H. and Christie, P. (2019) ‘Low-temperature
hydrothermal carbonization of fresh pig manure: Effects of temperature on characteristics of
hydrochars’, Journal of Environmental Engineering, 145(6), pp.04019029.
Stevens, C.J. (2019) ‘Nitrogen in the environment’, Science, 363(6427), pp.578-580.
Sun, D., Hale, L., Kar, G., Soolanayakanahally, R. and Adl, S. (2018) ‘Phosphorus recovery and
reuse by pyrolysis: Applications for agriculture and environment’, Chemosphere, 194,
pp.682-691.
Sutton, A.L., Nelson, D.W., Hoff, J.D. and Mayrose, V.B. (1982) ‘Effects of injection and surface
applications of liquid swine manure on corn yield and soil composition’, Journal of
Environmental Quality, 11(3), pp.468-472.
Sutton, A.L., Nelson, D.W., Mayrose, V.B., Nye, J.C. and Kelly, D.T. (1984) ‘Effects of varying
salt levels in liquid swine manure on soil composition and corn yield’, Journal of
environmental quality, 13(1), pp.49-59.
Sutton, A.L., Vanderholm, D.H. and Melvin, S.W. (1977) ‘Fertilizer value of swine manure’.
Washington State University, Cooperative Extension Service, United States.
Suzuki, K., Tanaka, Y., Kuroda, K., Hanajima, D., Fukumoto, Y., Yasuda, T. and Waki, M. (2007)
‘Removal and recovery of phosphorous from swine wastewater by demonstration
crystallization reactor and struvite accumulation device’, Bioresource Technology, 98(8),
pp.1573-1578.
57
Szoegi, A.A., Vanotti, M.B. and Hunt, P.G. (2015) ‘Phosphorus recovery from pig manure solids
prior to land application’, Journal of Environmental Management, 157, pp.1-7.
Tack, F.M. (2010) ‘Trace elements: general soil chemistry, principles and processes’, Trace
elements in soils, pp.9-37.
Tack, F.M. and Egene, C.E. (2019) ‘Potential of biochar for managing metal contaminated areas,
in synergy with phytomanagement or other management options’, Biochar from biomass and
waste, pp.91-111, Elsevier.
Tansel, B., Lunn, G. and Monje, O. (2018) ‘Struvite formation and decomposition characteristics
for ammonia and phosphorus recovery: A review of magnesium-ammonia-phosphate
interactions’, Chemosphere, 194, pp.504–514.
The World Bank. (2020) ‘Commodity Markets’, The World Bank. Available at:
https://www.worldbank.org/en/research/commodity-markets (Accessed: 10 July 2020).
Tiessen, H., 2008. Phosphorus in the global environment. In The ecophysiology of plant-
phosphorus interactions (pp. 1-7). Springer, Dordrecht.Hjorth, M., Christensen, K. V.,
Christensen, M. L., Sommer, S. G. (2010) ‘Solid–liquid separation of animal slurry in theory
and practice. A review’, Agronomy for Sustainable Development, 30(1), pp.153–180.
Troy, S.M., Lawlor, P.G., O’Flynn, C.J. and Healy, M.G. (2014) ‘The impact of biochar addition
on nutrient leaching and soil properties from tillage soil amended with pig manure’, Water,
Air, & Soil Pollution, 225(3), pp.1900.
Tsai, W. T., Liu, S. C., Chen, H. R., Chang, Y. M. and Tsai, Y. L. (2012) ‘Textural and chemical
properties of swine-manure-derived biochar pertinent to its potential use as a soil amendment’,
Chemosphere, 89(2), pp.198-203.
Uchimiya, M. and Hiradate, S. (2014) ‘Pyrolysis temperature-dependent changes in dissolved
phosphorus speciation of plant and manure biochars’, Journal of Agricultural and Food
Chemistry, 62(8), pp.1802-1809.
Uggetti, E., Sialve, B., Latrille, E. and Steyer, J.P. (2014) ‘Anaerobic digestate as substrate for
microalgae culture: the role of ammonium concentration on the microalgae productivity’,
Bioresource Technology, 152, pp.437-443.
Uggetti, E., Sialve, B., Latrille, E. and Steyer, J.P. (2014) ‘Anaerobic digestate as substrate for
microalgae culture: the role of ammonium concentration on the microalgae productivity’,
Bioresource Technology, 152, pp.437-443.
United Nations Department of Economic and Social Affairs (UNDESA) (2020) ‘World Economic
Situation and Prospects 2020’, United Nations, New York Office. Available at:
58
https://www.un.org/development/desa/dpad/wp-
content/uploads/sites/45/WESP2020_FullReport.pdf. (Accessed: 16 August 2020)
USGS (2020) ‘National Minerals Information Center’, Available at :
https://www.usgs.gov/centers/nmic/phosphate-rock-statistics-and-information. (Accessed: 16
August 2020)
Van Stappen, F., Mathot, M., Decruyenaere, V., Loriers, A., Delcour, A., Planchon, V., Goffart,
J.P. and Stilmant, D. (2016) ‘Consequential environmental life cycle assessment of a farm-
scale biogas plant’, Journal of Environmental Management, 175, pp.20-32.
Vasmara, C., Cianchetta, S., Marchetti, R. and Galletti, S. (2015) ‘Biogas Production from Wheat
Straw Pre-Treated With Ligninolytic Fungi And Co-Digestion With Pig
Slurry’, Environmental Engineering & Management Journal, 14(7).
Velthof, G.L., Lesschen, J.P., Webb, J., Pietrzak, S., Miatkowski, Z., Pinto, M., Kros, J. and
Oenema, O. (2014) ‘The impact of the Nitrates Directive on nitrogen emissions from
agriculture in the EU-27 during 2000–2008’, Science of the Total Environment, 468, pp.1225-
1233.
Veronesi, D., Ida, A., D´Imporzano, D. and Adani, F. (2015) ‘Microalgae Cultivation: Nutrient
Recovery from Digestate for Producing Algae Biomass’, Chemical Engineering Transactions,
43, pp.1201-1206.
Wallace, H.D., McCall, J.T., Bass, B. and Gombs, G.E. (1960) ‘High level copper for growing-
finishing swine’, Journal of Animal Science, 19(4), pp.1153-1163.
Wang, J.X., Chen, S.W., Lai, F.Y., Liu, S.Y., Xiong, J.B., Zhou, C.F. and Huang, H.J. (2020)
‘Microwave-assisted hydrothermal carbonization of pig feces for the production of hydrochar’,
The Journal of Supercritical Fluids, pp.104858.
Wang, L.K., Hung, Y.T. and Shammas, N.K. (2006) ‘Advanced physiochemical treatment
processes’. Handbook of Environmental Engineering. Vol. 4. The Humana Press Inc., Totowa,
NJ, USA.
Wang, M., Lee, E., Zhang, Q. and Ergas, S.J. (2016) ‘Anaerobic co-digestion of swine manure and
microalgae Chlorella sp.: experimental studies and energy analysis’, BioEnergy
Research, 9(4), pp.1204-1215.
Wang, Q., Wang, Z., Awasthi, M.K., Jiang, Y., Li, R., Ren, X., Zhao, J., Shen, F., Wang, M. and
Zhang, Z. (2016) ‘Evaluation of medical stone amendment for the reduction of nitrogen loss
and bioavailability of heavy metals during pig manure composting’, Bioresource
Technology, 220, pp.297-304.
59
Wang, X., Yang, G., Feng, Y., Ren, G. and Han, X. (2012) ‘Optimizing feeding composition and
carbon–nitrogen ratios for improved methane yield during anaerobic co-digestion of dairy,
chicken manure and wheat straw’, Bioresource. Technology, 120, pp.78–83.
Webber, L.R., Lane, T.H. and Nodwell, J.H. (1968) ‘Guidelines to land requirements for disposal
of liquid manure’, Proceedings of Texas Industrial water waste conference 8th, pp. 20-34.
Wei, X., Gao, B., Wang, P., Zhou, H. and Lu, J. (2015) ‘Pollution characteristics and health risk
assessment of heavy metals in street dusts from different functional areas in Beijing,
China’, Ecotoxicology and environmental safety, 112, pp.186-192.
Xie, M., Nghiem, L. D., Price, W. E. & Elimelech, M. (2014) ‘Toward resource recovery from
wastewater: phosphorus extraction from digested sludge using hybrid forward osmosis -
membrane distillation process’, Environmental Science & Technology Letters, 1(2), pp.191-
195.
Yetilmezsoy, K., Ilhan, F., Kocak, E. and Akbin, H.M. (2017) ‘Feasibility of struvite recovery
process for fertilizer industry: A study of financial and economic analysis’, Journal of cleaner
production, 152, pp.88-102.
Zaman, C.Z., Pal, K., Yehye, W.A., Sagadevan, S., Shah, S.T., Adebisi, G.A., Marliana, E.,
Rafique, R.F. and Johan, R.B. (2017) ‘Pyrolysis: A sustainable way to generate energy from
waste’, Pyrolysis. pp.1.
Zeng, W., Wang, D., Luo, Z., Yang, J. and Wu, Z. (2020) ‘Phosphorus recovery from pig farm
biogas slurry by the catalytic ozonation process with MgO as the catalyst and magnesium
source’, Journal of Cleaner Production, pp.122133.
Zhang, P., Sun, H., Yu, L. and Sun, T. (2013) ‘Adsorption and catalytic hydrolysis of carbaryl and
atrazine on pig manure-derived biochars: impact of structural properties of biochars’, Journal
of Hazardous Materials, 244, pp.217-224.
Zhang, T., He, X., Deng, Y., Tsang, D.C., Jiang, R., Becker, G.C. and Kruse, A. (2020) ‘Phosphorus
recovered from digestate by hydrothermal processes with struvite crystallization and its
potential as a fertilizer’, Science of the Total Environment, 698, pp.134240.
Zhang, Y. and He, Y. (2006) ‘Co-composting solid swine manure with pine sawdust as organic
substrate’, Bioresource Technology, 97(16), pp.2024-2031.
Zoccarato, I., Benatti, G., Calvi, S. L. and Bianchini, M. L. (1995) ‘Use of pig manure as fertilizer
with and without supplement feed in pond carp production in Northern Italy’, Aquaculture,
129(1-4), pp.387-390.
60
Annex 1
Ammonia stripping
Technology implemented Scale Type of manure fraction Sample
size
Recovery
efficiency
Duration
of study Year Location Reference
Ammonia stripping and vacuum
evaporation Lab Liquid fraction digestate
1L and 100
ml
95% 10 h 2016 Shunyi, Beijing. Li et al (2016)
Ammonia fermentation and air
stripping Lab Digestate 500 ml 87% 24 h 2019 Tsuchiura(Ibaraki, Japan) Huang et al (2019)
Ammonia stripping Lab
Fresh slurry 55% 225 mins
2012 Catalonia (Spain) Laureni et al (2013) Digested slurry 79%
Partially digested slurry 57%
Air-recirculated stripping Lab Digested pig slurry 3 L 98% 8 h 2015 Rongchang, PR China Liu et al (2015)
Ammonia stripping Lab Raw pig manure 8 L 90% 2012 Quebec, Canada. Ippersiel et al (2012)
Ammonia stripping and struvite Lab Digestate 1 L 91%
3 h 2015 Beijing, China Huang et al (2015) 97%
Ammonia stripping Lab 90% 2015 Spain Hidalgo et al (2016)
Pyrolysis
Technology implemented Scale Type of manure fraction Sample
size
Recovery
efficiency
Duration
of study Year Location Reference
Pyrolysis (700℃) Lab Pig manure 35% 2014 Denmark Christel et al (2014)
Pyrolysis (600℃) Lab Pig manure 93% 2016 Denmark Christel et al (2016) 95%
Pyrolysis (500℃)
Lab Pig manure
78%
2014 USA Uchimiya and Hiradate
(2014)
Pyrolysis (650℃) 85%
Pyrolysis (800℃) 87%
Pyrolysis (350℃) 42%
Pyrolysis (400℃) Lab Pig manure
95% 4h 2015 China Jin et al (2016)
Pyrolysis (350℃) Lab Pig manure 93% 2016 Denmark Christel et al (2016)
Pyrolysis (600℃) Lab Pig digestate 160 mL 56% 2013 Swiss Troy et al (2014)
Fast pyrolysis (500℃)/acid
extraction Lab Biochar 0.2g 90% 120 min 2013 Southern Netherlands Azuara et al (2013)
61
Pyrolysis Lab Pig manure (420℃) 5g 92% 20 min 2012 Italy Marchetti et al (2012)
Pyrolysis (450℃) Lab Pig manure 95% 1 h 2017 Belgium Maggen et al (2017)
Hydrothermal
Technology implemented Scale Type of manure fraction Sample
size
Recovery
efficiency
Duration
of study Year Location Reference
Hydrothermal carbonization Lab Pig manure 600 mL 95%
1h 2016 UK Ekpo et al (2016) 45%
Hydrothermal carbonization Lab Pig manure 20% 2018 Spain Gasco et al (2018)
Hydrothermal carbonization Lab Pig manure
130 mL
2011 China Qiao et al (2011)
Hydrothermal carbonization Lab Pig manure 94% 2018 Germany Li et al (2019)
Hydrothermal carbonization Lab Pig manure digestate 200 mL 95% 2020 China Zhang et al (2020)
Hydrothermal carbonization Lab Pig manure
67%
2017 Japan Huang et al (2017) 15%
Microwave-assisted hydrothermal
carbonization Lab Hydrochar (250℃) 40 ml
33% 30min 2020
Nanchang City,Jiangxi
Province,China Wang et al (2020)
78%
Hydrothermal liquefaction Lab Biocrudes (350℃) 7g 42% 60 min 2020 Aalborg, Denmark Conti et al (2020)
Hydrothermal carbonization Lab Hydrochar (220℃) 75g 12%
1 h 2019 Lin’an City, Zhejiang Song et al (2019) 73%
Struvite recovery
Technology implemented Scale Type of manure fraction Sample
size
Recovery
efficiency
Duration
of study Year Location Reference
Precipitation via Ca(OH)2 and
Al2(SO4)3 Lab
Slurry
500 ml
40-75%
2 min 20
sec 2019 Bergamo, Italy Cattaneo et al (2019)
Digestate 60-75%
Digestate stripped 50-90%
Cattle and pig digestate 65-70%
Cattle and pig digestate
stripped 70-85%
Struvite recovery and anaerobic
digestion Lab Digested pig slurry 600 ml
89% 48 h 2015 Barcelona, Spain Cerrillo et al (2015)
98%
Struvite recovery Lab Raw pig manure 200 mL 69%
4 h 2019 Valencia (Spain) Luján-Facundo et al
(2019) 56%
62
Struvite crystallization Lab
TP = 85% 2018 China Ma et al (2018) TN = 71%
Ammonia stripping and struvite
ppt Lab Digestate 1 L
91% 3 h 2015 Beijing, China Huang et al (2015)
97%
Struvite precipitation Lab Digestate 3L 90% 15 h 2009 Hangzhou, Zhejiang
province. Perera et al (2009)
Struvite precipitation Lab Pig slurry 100 ml 95%
2017 France Piveteau et al (2017) 89%
Struvite precipitation Lab Pig slurry
95%
2013 France Daumer et al (2013)
95%
95%
95%
Struvite precipitation Pilot Pig manure 93% 2002 USA Burns and moody (2002)
Struvite precipitation Pilot Pig manure 90% 2012 USA Ackerman, Cicek and
Oleszkiewicz (2012)
Struvite precipitation Lab Pig manure 400ml 97% 2003 USA Burns et al (2003)
Struvite precipitation Lab Pig manure 65% 2014 France Achat et al (2014)
Separation processes
Technology implemented Scale Type of manure fraction Sample
size
Recovery
efficiency
Duration
of study Year Location Reference
Quick wash process Lab Fresh pig manure 64 g 90% 1 h 2015 Florence Co., SC, USA Szoegi, Vanotti and Hunt
(2015)
Elco-ecopurin® Full
scale Pig slurry
42%
2002
Modena, Italy
Martinez-Almela and
Barrera (2005)
11%
53%
Barcelona, Spain 14%
71%
Murcia, Spain 28%
65%
Goshen, USA 30%
Vacuum membrane distillation Lab Raw biogas slurry 60-360
ml/min 60% 120 min 2020
Ezhou City, Hubei
Province, China Shi et al (2020)
Electrodialysis reversal Lab Digestate 2L 100%
9 h 2019 Galway, Ireland Shi et al (2019) 84%
63
Bipolar membrane electrodialysis
(BMED) system Lab Pig Manure hydrolysate 5L
78% 48 h 2018 Galway, Ireland Shi et al (2018)
75%
Biological methods
Technology implemented Scale Type of manure fraction Sample
size
Recovery
efficiency
Duration
of study Year Location Reference
Vermicompost with pig manure
(VPM) Pilot Crop residue + PM 2g
25% 2 months 2019 Purple Soil, Yanting Raza et al (2019)
90%
Anaerobic digestion Lab Digestate 130 mL 90%
21 days 2016
Wang et al (2016) 89%
Duckweed ponds Full
Scale Digestate 3 m3
84% 134 days 2012 Southern Brazil Mohedaro et al (2012)
86%
Composting (mechanical turning) Full
scale
1 month stored slurry, fresh
slurry 4.8 m3
170 days 2017 Almería,
Spain Saez et al (2017)
Catalytic ozonation ± SBR Lab Digested slurry 1L 90%
4 days 2020 Maogang farm, Guangzhou Zeng et al (2020)
Struvite recovery anaerobic
digestion Lab Digested pig slurry 600 ml
89% 48 h 2015 Barcelona, Spain Cerrillo et al (2015)
98%
Algal accumulation Lab Pig manure
85%
2006 USA
Kebede-Westhead,
Pizarro and Mulbry
(2006) 92%
Composting Lab Pig manure
39%
1996 New Zealand Bhamidimarri and Pandey
(1996) 51%
Composting Lab Pig manure
42%
2005 China Zhang and He (2006) 94%
64
Annex 2
Study ID Randomization
process
Missing outcome
data
Measurement
of the outcome
Selection of the
reported result Overall Bias
Huang et al 2019 Low Low Low Low Low
Li et al 2016 Low Low Low Low Low
Laureni et al (2013) Low Low Low Low Low
Liu et al (2015) Low Low Low Low Low
Ippersiel et al (2012) Low Low Low Low Low
Huang et al (2015) Low Low Low Low Low
Hidalgo et al (2016) Low High High Low High
Christel et al (2014) Low Low Low Low Low
Christel et al (2016) Low Low Low Low Low
Uchimiya and Hiradate (2014) Low Low Low Low Low
Jin et al (2016) Low Some concerns Low Low Some concerns
Troy et al (2014) Low Some concerns Low Low Some concerns
Azuara et al (2013) Low Some concerns Low Some concerns Some concerns
Maggen et al (2017) Low Low Low Low Low
Marchetti et al (2012) Low Some concerns Some concerns Low Some concerns
Cattaneo et al (2019) Low Low Low Low Low
Cerrillo et al (2015) Low Low Low Low Low
Luján-Facundo et al (2019) Low Low Low Low Low
Ma et al (2018) Low High Some concerns Some concerns High
Perera et al (2009) Low Low Low Low Low
65
Piveteau et al (2017) Low Low Low Low Low
Daumer et al (2013) Low Low Low Low Low
Burns and moody (2002) Low Low Low Low Low
Ackerman, Cicek and Oleszkiewicz (2012) Low Low Low Low Low
Burns et al (2003) Low Low Low Low Low
Achat et al (2014) Low Low Some concerns Some concerns Some concerns
Szoegi, Vanotti and Hunt (2015) Low Low Low Low Low
Martinez-Almela and Barrera (2005) Low Low Low Low Low
Shi et al (2020) Low Low Low Low Low
Shi et al (2019) Low Some concerns Some concerns Low Some concerns
Shi et al (2018) Low Low Low Low Low
Raza et al (2019) Low Low Low Low Low
Wang et al (2016) Low Low Low Low Low
Mohedaro et al (2012) Low Some concerns Some concerns Low Some concerns
Saez et al (2017) Low Low Low Low Low
Zeng et al (2020) Low Low Some concerns Low Some concerns
Kebede-Westhead, Pizarro and Mulbry (2006) Low Low Low Low Low
Bhamidimarri and Pandey (1996) Low Low Low Low Low
Zhang and He (2006) Low Low Low Low Low
Ekpo et al (2016) Low Low Low Low Low
Gasco et al (2018) Low Low Low Low Low
Qiao et al (2011) Low Low Low Low Low
Li et al (2019) Low Low Low Low Low
66
Zhang et al (2020) Low Low Low Low Low
Huang et al (2017) Low Low Low Low Low
Wang et al (2020) Low Some concerns Some concerns Low Some concerns
Conti et al (2020) Low Low Low Low Low
Song et al (2019) Low Some concerns Some concerns Low Some concerns
Assessment Details
1. Bias arising from the randomization process:
a. the allocation sequence was random.
b. The allocation sequence was adequately concealed.
c. baseline differences between intervention groups suggest a problem with the randomization process.
2. Bias due to missing outcome data
a. data for this outcome were available for all, or nearly all, participants randomized.
b. (if applicable) there was evidence that the result was not biased by missing outcome data.
c. (if applicable) missingness in the outcome was likely to depend on its true value (e.g. the proportions of missing outcome data, or
reasons for missing outcome data, differ between intervention groups).
3. Bias in measurement of the outcome
a. the method of measuring the outcome was inappropriate.
b. measurement or ascertainment of the outcome could have differed between intervention groups.
c. outcome assessors were aware of the intervention received by study participants.
d. (if applicable) assessment of the outcome was likely to have been influenced by knowledge of intervention received.
67
4. Bias in selection of the reported result
a. the trial was analysed in accordance with a pre-specified plan that was finalized before unblinded outcome data were available for
analysis.
b. the numerical result being assessed is likely to have been selected, on the basis of the results, from multiple outcome
measurements within the outcome domain.
c. the numerical result being assessed is likely to have been selected, on the basis of the results, from multiple analyses of the data.