You are on page 1of 34

Critical Reviews in Environmental Science and

Technology

ISSN: (Print) (Online) Journal homepage: www.tandfonline.com/journals/best20

Sustainable use of biochar for resource recovery


and pharmaceutical removal from human urine: A
critical review

Sayeda Ummeh Masrura, Pavani Dissanayake, Yuqing Sun, Yong Sik Ok,
Daniel C. W. Tsang & Eakalak Khan

To cite this article: Sayeda Ummeh Masrura, Pavani Dissanayake, Yuqing Sun, Yong Sik Ok,
Daniel C. W. Tsang & Eakalak Khan (2021) Sustainable use of biochar for resource recovery and
pharmaceutical removal from human urine: A critical review, Critical Reviews in Environmental
Science and Technology, 51:24, 3016-3048, DOI: 10.1080/10643389.2020.1818497

To link to this article: https://doi.org/10.1080/10643389.2020.1818497

Published online: 12 Sep 2020.

Submit your article to this journal

Article views: 1416

View related articles

Citing articles: 10 View citing articles

Full Terms & Conditions of access and use can be found at


https://www.tandfonline.com/action/journalInformation?journalCode=best20
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY
2021, VOL. 51, NO. 24, 3016–3048
https://doi.org/10.1080/10643389.2020.1818497

Sustainable use of biochar for resource recovery and


pharmaceutical removal from human urine: A
critical review
Sayeda Ummeh Masruraa, Pavani Dissanayakeb, Yuqing Sunc, Yong Sik Okb ,
Daniel C. W. Tsangc , and Eakalak Khana
a
Department of Civil and Environmental Engineering and Construction, University of Nevada, Las
Vegas, Las Vegas, Nevada, USA; bKorea Biochar Research Center & Division of Environmental
Science and Ecological Engineering, Korea University, Seoul, Republic of Korea; cDepartment of Civil
and Environmental Engineering, The Hong Kong Polytechnic University, Kowloon, Hong Kong, China

ABSTRACT
Biochar has recently been used
for recovering nutrients from
waste streams including source-
separated human urine. The
increased consumption of phar-
maceuticals has been a subject of
concern as some of the com-
pounds are not completely
metabolized and consequently
present in human urine. As urine contains both nutrients and pharmaceuticals, biochar
applied for nutrient recovery may adsorb pharmaceuticals causing a concern on the intro-
duction of the contaminants to the environment. This review article discusses the sorption
of nutrients as well as pharmaceuticals by biochar. It reveals that biochars with different
properties can be employed to separately attain nitrogen and phosphorus recovery, and
removal of pharmaceuticals from source-separated urine. Production conditions including
pyrolysis temperature and feedstock source are the vital aspects for delivering biochar
properties that are suitable for different groups of chemical entities (nutrients versus phar-
maceuticals). In addition, pharmaceutical adsorption is more favorable at lower solution pH
whereas nutrient recovery is favorable at higher solution pH. If this concept of using separ-
ate biochars is employed, it will minimize the potential exposure of pharmaceuticals to the
environment and humans and in the process the nutrient-rich biochar can be applied to
the agrarian fields to achieve a closed-loop fertility system.

KEYWORDS Engineered biochar; pharmaceutical adsorption; source-separated urine

1. Introduction
Municipal wastewater should be considered as a valuable resource because
of its high nutrient contents (phosphorus and nitrogen). For sustainable
nutrient management, urine source separation, a scheme involved in

CONTACT Eakalak Khan eakalak.khan@unlv.edu Department of Civil and Environmental Engineering and
Construction, University of Nevada, Las Vegas, Box 454015, 4505 S. Maryland Parkway, Las Vegas, NV 89154-
4015, USA.
ß 2020 Taylor & Francis Group, LLC
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3017

discrete collection and management of urine, is a more auspicious and sus-


tainable practice than traditional wastewater treatment system (Wilsenach
& van Loosdrecht, 2003). On average, urine contributes 45%–50% of total
phosphorus and 75%–80% of total nitrogen by mass in urban wastewater
but accounts for only 1% of the wastewater volume (Larsen & Gujer, 1996;
Wilsenach et al., 2007; Wilsenach & van Loosdrecht, 2003). In many coun-
tries, direct application of human urine is a process for recycling of
nutrients to support agricultural production (Heinonen-Tanski et al., 2007;
Mnkeni et al., 2008; Sridevi et al., 2009). However, with steadily increasing
consumption, availability, and accessibility of pharmaceuticals in daily
products due to population growth, human urine can contain pharmaceuti-
cals, the release of which adversely affects the ecosystems and consequently
hampers its use as a nutrient source for plants.
The presence of pharmaceuticals and their metabolites varies significantly
in fresh human urine. Vree et al. (1978) showed 9.5% of sulfamethoxazole
(SMX) defecated in original form and 52% excreted as metabolite, whereas
60% of trimethoprim (TMP) excreted unchanged. Conventional wastewater
treatment systems are not able to effectively eliminate the pharmaceuticals
and metabolites (de Jesus Gaffney et al., 2017; Garcıa-Galan et al., 2012;
Solanki & Boyer, 2017), which consequently are discharged into rivers,
lakes, and estuaries through treated effluent. As a result, the exposure and
slow degradation of these pharmaceuticals especially antibiotics in the
environment will result in more microbial resistance, which could endanger
human and animal health (de Boer et al., 2018; Hamilton et al., 2020). The
presence of pharmaceuticals in urine needs to be considered prior to the
application of source-separated urine as a nutrient product.
Biochar, a cost-effective carbonized organic matter, is a promising alter-
native to activated carbon due to its cost-effectiveness and energy-efficient
production process from biowaste resources (Ahmad et al., 2014).
Municipal solid wastes (Zornoza et al., 2016), sewage sludge (Li et al.,
2019), animal manures (Cao & Harris, 2010; Zornoza et al., 2016), and
wastes from agricultural production and wood processing (El-Naggar,
Awad, et al., 2018; El-Naggar, Lee, et al., 2018) can be used as raw material
for biochar preparation and soil applications. Bioenergy produced from
converting waste biomass to biochar can be a promising substitute to fossil
energy with less emissions of carbon dioxide (Bolan et al., 2013; Lee et al.,
2017). Many attractive features of biochar including affordability, simple
production process, relatively large surface area, meso-/micro-porosity
(Ahmad et al., 2014; Shaaban et al., 2018), oxygen-rich surface functional-
ity, and high cation exchange capacity (CEC) (Igalavithana, Mandal, et al.,
2017) have helped to increase its usage in many different fields. Adsorption
of contaminants on biochar can be achieved by many mechanisms such as
3018 S. U. MASRURA ET AL.

pore-filling mechanisms, electrostatic interactions, hydrophobicity, parti-


tioning, and hydrogen bonding (Inyang & Dickenson, 2015). These mul-
tiple mechanisms make biochar a versatile adsorbent. Biochar exhibits high
capacities of removing radioactive materials (Jang et al., 2018) and specific
organic contaminants such as antibiotics (Solanki & Boyer, 2017), volatile
organic compounds (Kumar et al., 2020), polychlorinated biphenyls (Xu
et al., 2012), polycyclic aromatic hydrocarbons (Beesley et al., 2010), agro-
chemicals, and aromatic dyes (Qiu et al., 2009) from water and wastewater.
It is also capable of removing inorganic contaminants including metals/
metalloids (Beiyuan et al., 2017; Jeon et al., 2018), phosphate, ammonia,
nitrate (Gai et al., 2014; Takaya, Fletcher, Singh, Anyikude, et al., 2016),
and sulfide (Shang et al., 2013).
Numerous studies have shown the applications of biochar for nutrient
(ammonia and phosphate) recovery from aqueous solutions (Gai et al.,
2014; Taghizadeh-Toosi et al., 2012; Takaya, Fletcher, Singh, Anyikude,
et al., 2016; Yao et al., 2011). While negative surface charge on biochar
facilitates ammonia adsorption, precipitation of metal-phosphate process
plays a more prominent role for phosphate adsorption (Shepherd et al.,
2017; Takaya, Fletcher, Singh, Okwuosa, et al., 2016). Nutrients extraction
from human urine is a sustainable option for waste disposal and an eco-
nomically feasible way to produce soil conditioner/fertilizer. Biochar pro-
duced from waste biomass followed by its application to soils is an effective
way to fight against climate change through carbon sequestration (El-
Naggar et al., 2019; Lehmann et al., 2008). Being a slow-releasing nutrient
agent, biochar has the capability to preserve nutrients and enhance soil
quality (Igalavithana, Mandal, et al., 2017; Vikrant et al., 2018). Biochar can
intensify the biological and physicochemical properties (Igalavithana et al.,
2019; Igalavithana, Lee, et al., 2017), and reduce the bioavailability of
potentially toxic compounds of soil (Chen et al., 2019). Biochar can also
contribute to mitigating greenhouse gases by reducing nitrous oxide and
methane emission from soil (Stewart et al., 2013; Windeatt et al., 2014;
Zhang et al., 2013). The above benefits of biochar have immense import-
ance as the fertility of soils can be improved with the application of nitro-
gen and phosphorus laden biochar.
Several research and review articles have been published addressing the
use of biochar for removal of pharmaceuticals from urine, wastewater, or
aqueous solution (Reguyal & Sarmah, 2018; Solanki & Boyer, 2017). The
principal mechanism underlying the removal of pharmaceuticals is the elec-
tron donor-acceptor (EDA) interactions at slightly acidic pH (Jung et al.,
2013; Peiris et al., 2017). However, to date, studies on the effects of the
presence of pharmaceuticals in urine and wastewater on nutrient recovery
by biochar are lacking. Researchers have overlooked the fact that the
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3019

biochar applied for nutrient recovery from urine can pick up pharmaceuti-
cals. The recovery process reduces the overall pollution (nutrients and
pharmaceuticals) load in the urine stream and eventually natural waters but
utilizing the applied biochar as a soil amendment may lead to unintentional
introduction of the pharmaceuticals to the environment. The overarching
objective of this article is to address this specific scenario. With new
research and developments in biochar-based technologies, there is a possi-
bility to recover nutrients while reducing the risk of introducing pharma-
ceuticals and their metabolites into the environment (Desbiolles et al.,
2018; Li et al., 2020). For this purpose, the selection of specific types of bio-
char based on their sorption properties toward nutrients and pharmaceuti-
cals is essential. If nutrients have more affinities than pharmaceuticals to
biochar, the field application of nutrient-rich biochar can be ensured to
enhance soil productivity with minimal risk of environmental contamin-
ation. Relative affinities of nutrients and pharmaceuticals and their metabo-
lites to biochar are therefore crucial.
Our literature search on Google Scholar, Web of Science, and Elsevier
Science Direct databases was conducted using the keywords “biochar and
nutrients” and “biochar and pharmaceuticals” in the title, abstract, and key-
words. Overall, 116 peer-reviewed journal articles were chosen for this crit-
ical review. The aims of this critical review article are to appraise the
principal mechanisms for separate removal of pharmaceuticals and
nutrients by biochar and to recommend an environmentally sound
approach to recover N and P in urine by biochar for application as a soil
fertilizer with no or limited pharmaceutical contents. In this manner, the
applied biochar, which is rich in N and P, would enhance soil productivity
without contaminating the soil. This issue/approach has not
been discussed.
Several studies evaluated the application of biochar for nutrient recovery
and pharmaceutical removal from wastewater separately (Solanki & Boyer,
2019; Takaya, Fletcher, Singh, Okwuosa, et al., 2016; Trazzi et al., 2016; Xie
et al., 2014); however, none of the studies looked at them together. These
studies described the characteristics and applications of biochar, and inter-
action mechanisms between the contaminants (sorbates) in wastewater and
biochar. Despite significant research and reviews on biochar, there is a
knowledge gap on the application of biochar for separate removal of a mix-
ture of pharmaceuticals and nutrients as found in urine. The idea behind
the recommended approach is to devise two separate biochars with differ-
ent properties and functionalities, one that is selective toward pharma-
ceuticals and the other that mainly adsorbs nutrients. This article
critically evaluates the surface chemistry of biochar and environmental
conditions to elucidate sorption sites and mechanisms for nutrients and
3020 S. U. MASRURA ET AL.

pharmaceuticals. It also covers an overview and implications of advances


in biochar modification processes, and relevant knowledge gaps and
future research directions.

2. Source separated urine


2.1. Nutrient content
Human urine consists of primarily water, and a variety of inorganic salts,
organic compounds including nitrogenous molecules (urea), and other
metabolic waste components. Recently, source-separated urine has gained
attraction as a valuable source of nutrients owing to its high concentrations
of N, K, P, and S (Udert, 2002). In municipal wastewater, human urine
contributes 80%–88% of total nitrogen, 70%–73% of potassium, and
60%–67% of total phosphate (Larsen & Gujer, 1996; Wilsenach et al., 2007)
but is only 1% of the overall wastewater volume (Wilsenach & van
Loosdrecht, 2006). Kirchmann and Pettersson (1995) found that the total
nitrogen concentrations in human urine range from 1.79 to 2.61 g L1, of
which 95% is present as ammonia nitrogen and the remaining were amino
acid-N, nitrite, and nitrate, while the concentration of total phosphorus
varies from 0.20 to 0.21 g L1 in the form of dissolved phosphate.
The pH of the urine solution is generally around 9 due to urea decom-
position during storage (Kirchmann & Pettersson, 1995). The chemical
composition of human urine is influenced by numerous factors including
feeding habits, body size, physical activities, drinking water consumption,
income level, and sociocultural factors (Karak & Bhattacharyya, 2011; Rose
et al., 2015; Vinnerås & J€onsson, 2002). Separate collection of human urine
at the source from the sewerage system and its application as a fertilizer
encourage closed-loop nutrient flow from sanitation to agriculture (Zhang,
Li, et al., 2015).

2.2. Pharmaceutical content


Consumption of pharmaceuticals has continued to increase significantly for
treating various human and animal diseases. To perform the therapeutic
function in the human body, most of the pharmaceuticals are designed to
be persistent. Considerable amounts of these pharmaceuticals are defecated
unchanged or in the form of metabolites in urine which are transported to
the environment via municipal wastewater streams. For example, azithro-
mycin, frequently prescribed for infectious diseases in human, has been
reported in wastewater samples at different concentrations from 15 to 66 ng
L1 (Jones-Lepp et al., 2004). Another study on source-separated urine
detected the presence of SMX, TMP, and diclofenac at 6800, 1280, and
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3021

72 mg L1, respectively (Bischel et al., 2015). On average, 64% (±27%) phar-


maceuticals are excreted via urine and 42% (±28%) of these pharmaceuti-
cals are defecated as metabolites (Lienert et al., 2007).
The major pharmaceutical compounds in human urine are SMX, sulfa-
methazine (SMZ), sulfamerazine, sulfadiazine, TMP, ampicillin, amoxicillin,
tetracycline (TC), azithromycin (Bischel et al., 2015; Desbiolles et al., 2018;
Jung et al., 2013). The metabolites of these compounds commonly detected
in human urine are N4-acetylsulfamethazine for SMZ, N4-acetylsulfamera-
zine for sulfamerazine, N4-acetylsulfadiazine for sulfadiazine, ampicilloic
acid for ampicillin, and amoxicilloic acid for amoxicillin (Fernandez-Torres
et al., 2010). Mack (1992) reported ciprofloxacin and its three metabolites,
sulfociprofloxacin, desethylene ciproftoxacin, and oxo-ciprofloxacin, in
human urine. If liquid urine is applied directly as a fertilizer, the pharma-
ceuticals and its metabolites may accrue in the soil and plants and arouse
environmental and health risks (Zhang, Sun, et al., 2015).

2.3. Difficulties in nutrient recovery from source-separated urine by biochar


The principal source of nutrients in municipal wastewater is human urine.
Apart from being a valuable resource, human urine contains metals/metal-
loids, pathogenic organisms, and pharmaceuticals (Ahmed et al., 2017;
Lienert et al., 2007) which can negatively affect the environment and
human health. Urine collection, handling, and storage if required, need
additional investment. In urban areas, due to space constraints, the storage
of large volumes of urine is difficult. Poor urine storage facilities will cause
odor problems. Health risks to workers dealing with urine storage and
treatment as well as those involved in the field application of urine treated
biochar are also a matter of concern (Bischel et al., 2015).
In source-separated urine, ammonium could be recovered efficiently by
adsorption yielding nutrient-enriched biochar (Bai et al., 2018; Tarpeh
et al., 2017). The principal nitrogen components in urine are urea and
ammonium. The recovery of urea is however difficult and possibly
unnecessary due to its rapid decomposition into ammonium and ammonia
gas during storage (Zhang, Li, et al., 2015). The World Health
Organization (WHO) recommended that applying source-separated urine
directly in agriculture after storing for 6 months at 20  C or longer could
be pathogenically safe (WHO, 2006). However, long-term storage of urine
may cause an odor problem and release of recoverable nutrients through
volatilization of ammonia (Zhang, Li, et al., 2015). Due to negatively
charged surface area, raw biochars without engineering design/modification
hardly adsorb phosphate (Trazzi et al., 2016). The phosphate concentration
of human urine is strongly influenced by precipitation process.
3022 S. U. MASRURA ET AL.

Consequently, the combination of biochar and struvite precipitation can


recover over 99% of phosphate from human urine (Zheng et al., 2018).
Based on the previous studies reviewed, it is clear that source-separated
human urine has a fertilization value but the pharmaceuticals present need
to be removed for environmentally sound application of the urine as a soil
amendment. Application of urine treated biochar not only positively
affected the growth of plants immediately but also contributed to the plant
N uptake and had the potential to serve as transient storage of available N
for the plant (Taghizadeh-Toosi et al., 2012). Urine source separation and
consequent agricultural application would reduce the waste load to waste-
water treatment plants.

3. Application of biochar for nutrient recovery


Biochar is a carbon rich by-product of the thermochemical decomposition
of biomass at temperatures of 300–900  C in an oxygen-limited condition,
which is termed as pyrolysis (Ahmad et al., 2014; Igalavithana, Mandal,
et al., 2017). Among different methods for pyrolysis differing in residence
time, heating rate and temperature (fast pyrolysis, intermediate pyrolysis,
slow pyrolysis, and gasification), slow pyrolysis generate a higher quantity
of biochar and less bio-oil compared to other methods (Ahmad et al., 2014;
Al-Wabel et al., 2018). Biochar yield primarily varies with the raw material
used and pyrolysis conditions including heating rate and temperature
(Ahmad et al., 2014; Al-Wabel et al., 2018; Igalavithana, Mandal,
et al., 2017).

3.1. Desirable characteristics of biochar


Feedstocks and pyrolysis conditions can influence different biochar proper-
ties such as surface area and molecular structure of biochar, and conse-
quently affect the cation and anion exchange capacities for upholding
nutrients (Ahmad et al., 2014; Gai et al., 2014; Sun et al., 2014). Biochar
primarily contains carbon, hydrogen, oxygen, and nitrogen, along with
mineral elements and nutrients depending on the raw biomass used for its
production (Yuan et al., 2019). Nutrient contents are significantly higher in
the biochar prepared from animal manure than wood biomass due to the
presence of more organic compounds (Chen et al., 2018; Zornoza et al.,
2016). Table 1 summarizes previous studies on the composition and pri-
mary characteristics of biochar for nutrients recovery prepared at different
pyrolysis conditions.
The pore size of biochar mainly depends on the feedstock type and typ-
ically varies from nano (<0.9 nm) to micro (<2 nm) to macro pores
Table 1. Elemental composition of pristine biochars used for nutrients recovery from urine and wastewater stream.
Pyrolysis Elemental composition of biochar before application
temperature Adsorbate
Nutrient Feedstock ( C) media Solution pH Chemical agent C (%) H (%) O (%) N (%) Ash content (%) References
Ammonium Oak wood 400–450 Wastewater 7.0 70.9 3.6 12.9 0.4 20.8 Takaya,
600–650 79.2 2.0 3.5 0.3 13.4 Fletcher, Singh,
Greenhouse waste 400–450 63.0 1.2 7.5 0.9 17 Anyikude,
600–650 59.0 2.9 9.6 1.2 27.0 et al. (2016)
Corn straw 400 Aqueous 56.1 4.3 22.0 2.4 14.0 Gai et al. (2014)
500 solution 58.0 2.7 21.5 2.3 17.0
600 58.6 2.0 18.7 2.0 18.0
700 59.5 1.5 16.6 1.6 18.0
Oak sawdust 300 Aqueous LaCl3 50.2 5.8 41.6 0.2 0.9 Wang
400 solution 69.4 4.3 22.4 0.4 2.0 et al. (2015)
500 76.5 3.4 16.6 0.4 2.9
600 80.4 3.1 12.2 0.4 3.6
Pine sawdust 550 Aqueous 3.0–10.0 78 2.3 10.2 0.6 Yang
Wheat straw 550 solution 87 2.6 8.9 1.3 et al. (2018)
Fecal sludge 400–800 Urine 6.0–8.0 84.4 2.4 0.8 3.1 Bai et al. (2018)
Corncob 200 Aqueous 7.0 51.2 5.7 42.4 0.6 Cai et al. (2016)
Pomelo peel solution 52.6 5.1 40.8 1.2
Banana stalk 52.5 4.5 41.0 1.8
Nitrate Corn straw 400 Aqueous 56.1 4.3 22.0 2.4 14.0 Gai et al. (2014)
500 solution 58.0 2.7 21.5 2.3 17.0
600 58.6 2.0 18.7 2.0 18.0
700 59.5 1.6 16.6 1.6 18.0
Oak sawdust 300 Aqueous LaCl3 50.2 5.8 41.6 0.2 0.9 Wang
400 solution 69.4 4.3 22.4 0.4 2.0 et al. (2015)
500 76.5 3.4 16.6 0.4 2.9
600 80.4 3.1 12.2 0.4 3.6
Urea Corn cob 300 Human urine 67.9 4.5 21.9 0.7 5.0 Zhang, Li,
et al. (2015)
Phosphate Oak wood 450 Wastewater 7.0 KOH 65.7 2.7 31 0.6 11.7 Takaya,
650 H2O2 76.5 1.4 21.3 0.8 14.3 Fletcher, Singh,
Greenhouse waste 400 MgCl2.6H2O 59 2.9 36.6 1.2 27 Okwuosa,
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY

et al. (2016)
Oak sawdust 300 Aqueous LaCl3 50.2 5.8 41.6 0.2 0.9 Wang et al.
400 solution 69.4 4.3 22.4 0.4 2.0 (2015)
(continued)
3023
Table 1. Continued.
3024

Pyrolysis Elemental composition of biochar before application


temperature Adsorbate
Nutrient Feedstock ( C) media Solution pH Chemical agent C (%) H (%) O (%) N (%) Ash content (%) References
500 76.5 3.4 16.6 0.4 2.9
600 80.4 3.1 12.2 0.4 3.6
Orange peel 250 Wastewater FeCl3 and FeCl2 56.5 5.1 1.7 3.2 Chen et al.
700 67 1.5 2.1 14.9 (2011)
Wood waste 600 Human urine 6.0–11.0 MgCl2.6H2O 73.3 3.4 13.7 1.8 Xu et al. (2019)
Pine sawdust 300 Aqueous 7.0 62.7 4.1 27.1 0.3 2.7 Lou et al.
550 solution 78.0 2.3 10.2 0.6 6.4 (2016)
S. U. MASRURA ET AL.

Phosphorus Sesame straw 300 Aqueous ZnCl2 58.1 5.2 33.4 2.4 Park et al.
400 solution 61.7 4.7 31.2 2.5 (2015)
500 64.2 4.2 30.2 2.7
600 72.6 2.1 21.7 2.9
Miscanthus x giganteus 700 Aqueous 7.0 90.4 1.7 7.5 0.5 14.9 Trazzi et al.
Sugarcane bagasse 700 solution (2016)
86.5 1.9 11.1 0.5 12.5
Wheat straw 500–550 Aqueous 3.0–11.0 86.9 2.6 8.9 1.3 31.8 Dugdug et al.
Hardwood 500–550 solution 89.2 2.7 7.9 0.2 35.8 (2018)
Willow wood 500–560 86.7 2.2 10.3 0.8 37.7
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3025

(>50 nm) (Li et al., 2017). Biochars produced from different types of wood
and bamboo have meso/macroporous structures while those produced from
husks exhibit microporous structures (Joseph et al., 2007). The removal of
volatile materials from biochar at high pyrolysis temperatures results in the
development of micropores (Ahmad et al., 2012) and thereby improved
adsorption capacity (Sun et al., 2014). Generally, biochar produced at lower
temperatures has a higher yield than the biochar produced at higher tem-
peratures as organic matter decomposition rate increases with temperature
(Sun et al., 2014). Biochar pyrolyzed at high temperatures results in more
specific surface area and aromaticity (Ahmad et al., 2012) but less H and O
components (Gai et al., 2014). For example, biochar pyrolyzed at 600  C
showed 30 times greater surface areas than the biochar prepared at 450  C
(Sun et al., 2014). Larger surface areas indicate more porous structures
within biochar to adsorb chemical compounds.
Takaya, Fletcher, Singh, Anyikude, et al. (2016) inspected the effect of
feedstocks on the physicochemical properties of biochar such as surface
functionality, pH, CEC, and mineral contents. Manure biochar has higher
ash contents because of the presence of minerals (calcite and quartz) facili-
tating phosphate adsorption (Cao & Harris, 2010). Recent studies explored
different engineering approaches to alter biochar surface by metal oxides to
increase the adsorption capacity for phosphate from human urine (Park
et al., 2015; Xu et al., 2019; Zheng et al., 2018). Among different activation
agents, biochar surface modified with MgO resulted in better adsorption
capacity for phosphate (Xu et al., 2018, 2019; Zheng et al., 2018). Previous
analyses have reported that phosphate adsorption capacity of biochar
increases with production temperature up to 500  C (Takaya, Fletcher,
Singh, Anyikude, et al., 2016; Wang et al., 2015) as pores in the biochar are
blocked with further increase in the pyrolysis temperature (Jung et al.,
2016). However, a different study reported that phosphate adsorption cap-
acity of biochar was hardly affected by pyrolysis temperature (Lou et al.,
2016). Phosphorus sorption capacity of biochar is controlled by the initial
phosphate concentration more than the type of feedstock and pyrolysis
conditions. The reactive adsorption sites on biochar surface filled better at
higher concentration gradients (Dugdug et al., 2018; Takaya, Fletcher,
Singh, Anyikude, et al., 2016; Trazzi et al., 2016).
Biochar usually carries negative surface charge, which boosts the ability
to adsorb and hold cations (NH4þ) (Gai et al., 2014; Zheng et al., 2018).
Some studies reported that NH4þ adsorption was not influenced by biochar
surface area (Cai et al., 2016; Gai et al., 2014; Takaya, Fletcher, Singh,
Anyikude, et al., 2016). Ammonium adsorption by biochar is characterized
by chemical bonding and electrostatic interaction of ammonium with the
surface functional group (Yang et al., 2018). Biochars pyrolyzed at lower
3026 S. U. MASRURA ET AL.

temperatures show better adsorption capacity for ammonium because of an


increase in negatively charged functional groups (Gai et al., 2014; Takaya,
Fletcher, Singh, Anyikude, et al., 2016). Ammonium adsorption reaction
rate accelerated with smaller particle sizes of biochar (<2 mm) due to large
specific surface area (Bai et al., 2018).
Pyrolysis temperature and type of feedstock are the main factors for con-
trolling the pH of biochar (Ahmad et al., 2014). Generally, pH of biochar
changes from acidic to alkaline with an increasing trend with pyrolysis
temperature (Ahmad et al., 2014; Igalavithana, Mandal, et al., 2017).
Electrical conductivity (EC) of biochar is related to the presence of water-
soluble ions. EC value increases significantly with higher pyrolysis tempera-
ture because of less volatile materials (Gai et al., 2014; Igalavithana,
Mandal, et al., 2017). However, the effects of pH and EC of biochar on
nutrient recovery from human urine have not been studied.
Recently, the application of modified biochar for nutrient recovery has
gained much attention as surface modification can increase the surface area
and electron transfer capacity (Fang et al., 2020) leading to improved
adsorption capacity and kinetics (Huang et al., 2020). Adsorption mechanism
of modified biochar predominantly involved electrostatic interaction between
biochar and the sorbates including nutrients (Fang et al., 2020; Huang et al.,
2020; Jiang et al., 2019). Among different modification methods of biochar,
steam activation showed greater heavy metal removal potential compared to
pristine biochar due to increased surface area (Kwak et al., 2019; Wang
et al., 2020). However, Lou et al. (2016) stated that steam activation of bio-
char has no effect on its adsorption capacity of phosphate.

3.2. Recovery of N
Urea, a major nitrogen component in human urine, rapidly undergoes
decomposition during storage to ammonia. As a result, urea recovery by
biochar has not been widely studied. For low urea concentrations in human
urine (<4000 mg L1), biochar prepared at low temperature manifested
greater urea adsorption capacity than that prepared at high temperature
because of more C ¼ O and/or C-H on the surface that could act as poten-
tial sites for nutrient interaction (Gai et al., 2014; Zhang, Li, et al., 2015).
Biochar prepared at high pyrolysis temperatures had low polarity result-
ing in less NH4þ adsorption capacity (Gai et al., 2014). Oxygen-containing
functional groups such as C ¼ O, COOH, and  COC  contributed sub-
stantially to NH4þ adsorption because of hydrogen bonds and electrostatic
interaction between NH4þ and biochar (Cai et al., 2016). The sorption cap-
acity of NH4þ-N decreased after washing biochar with deionized water and
acid as the process washed off ash content and some inorganic fractions
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3027

(Gai et al., 2014). Nitrogen recovery efficiency by biochar increased with


solution pH from 7 to 12. At high pH, the zeta potential of biochar
decreased leading to more adsorption of positively charged ions (Yang
et al., 2018; Zheng et al., 2018). Adsorption capacity generally increases
with adsorption time, however process slow down at the end (Bai et al.,
2018). Corncob biochars modified with HNO3 and NaOH improved
ammonium adsorption capacity due to active carboxylic, lactonic and acidic
groups for adsorbing NH4þ-N (Vu et al., 2017).

3.3. Recovery of P
Surface functionality of biochar surface may not influence phosphate adsorp-
tion due to negatively charged surface (Takaya, Fletcher, Singh, Anyikude,
et al., 2016; Yao et al., 2011). The adsorption of P on biochar was affected
by the concentration of phosphate in solution, pyrolysis temperature, and
adsorption time. Higher phosphate concentrations in the solution, increased
pyrolysis temperature (up to 500  C), and longer residence time resulted in
the highest adsorption capacity (Takaya, Fletcher, Singh, Anyikude, et al.,
2016; Trazzi et al., 2016). The main forms of phosphate in urine are
HPO42 and H2PO4 at a pH range of 3–7 (Trazzi et al., 2016; Yang et al.,
2019). At pH above 7, OH strongly competes with PO43 in the solution
for active sites, leading toward lower phosphate adsorption capacity (Dugdug
et al., 2018; Jung et al., 2015; Trazzi et al., 2016; Yang et al., 2019).
Chen et al. (2011) studied the adsorption of phosphate by magnetic and
nonmagnetic biochars. The results displayed that the sorption efficacy of mag-
netic biochar was considerably greater than the companion biochar pyrolyzed
at a similar temperature, indicating the positive impact of the presence of iron
oxides for better adsorption of phosphate (Chen et al., 2011; Peng et al.,
2019). Dolomite-modified biochar formed lamellar structures via decompos-
ition of dolomite into magnesium and calcium oxides to offer binding sites
for phosphate at lower solution pH (Li et al., 2019). Biochar activated with
ZnCl2 improved phosphorus adsorption capacity by flaring the pores and pro-
ducing more positive sites on biochar surface (Park et al., 2015).

3.4. Simultaneous recovery of N and P


Struvite (MgNH4PO4.6H2O), a slow-releasing fertilizer can be generated
from urine due to the presence of NH4þ and phosphate (Wei et al., 2018).
A combination of biochar with struvite precipitation significantly improved
recovery of N and P from urine around 40%–50% and 99%, respectively.
Struvite precipitation in white crystal forms attached to biochar surface
enhances the specific surface area of biochar, thus improving nutrient
3028 S. U. MASRURA ET AL.

recovery (Zheng et al., 2018). Surface modification of biochars with MgO


and subsequent release of Mg2þ into the solution produced Mg–P precipi-
tates by reacting with the phosphate compounds present in the solution
(Chimenos et al., 2003; Xu et al., 2019). The interactions between MgO
and P formed Mg3(PO4)2, Mg(H2PO4)2, or MgHPO4 precipitates (Cui
et al., 2016; Li et al., 2016; Vikrant et al., 2018; M. Zheng et al., 2018).
Thus, Mg-biochar struvite precipitation is the principal mechanism for
high removal capacities of phosphate and ammonium (Xu et al., 2018).
Lanthanum modified biochar showed better ammonium adsorption cap-
acity due to acidic functional groups (carboxyl C ¼ O and phenolic-OH)
and improved phosphate adsorption capacity due to the formation of
La2O3 (Wang et al., 2015).
Nutrient adsorption properties of biochar are controlled by several fac-
tors, for example, biomass type, biochar pyrolysis temperature, and the pH
and chemistry of urine. Modified biochar shows better adsorption capacity
than pristine biochar and among the biochar modification methods; MgO
seems to have the best recovery of NH4þ and PO43 together in the form
of struvite precipitation. While oxygen-containing functional groups are
responsible for NH4þ adsorption, PO43 adsorption is mostly governed by
initial phosphate concentration and subsequent surface precipitation.
However, both NH4þ and PO43 adsorption is favorable at a slightly higher
pH (7) and for biochar pyrolyzed at low temperatures having greater sur-
face area and micropores.

4. Application of biochar for removal of pharmaceuticals


During the past several decades, consumer’s demand for pharmaceuticals
has grown tremendously. As a result, there are numerous pharmaceuticals
found in wastewater. Biochar application has extended beyond the recovery
of nutrients to the adsorption of pharmaceuticals in wastewater. Table 2
compiles the studies on biochar application for pharmaceutical adsorption
from different wastewater streams.

4.1. Desirable characteristics of biochar for pharmaceuticals extraction


According to Fourier transform infrared spectroscopy (FTIR) results, inter-
actions between biochar and pharmaceuticals will occur through p-p EDA
interactions and hydrogen bond due to carbonyl, hydroxyl and aromatic
compounds on the surface of biochar (Sun et al., 2018). Biochars pyrolyzed
at higher temperatures show better adsorption capacity of pharmaceuticals
than those produced at lower temperatures due to low volatile chemical
contents (Liu et al., 2017; Peiris et al., 2017; Rajapaksha, Vithanage, Lim,
Table 2. Biochars utilization for pharmaceutical adsorption from urine and wastewater stream.
Pyrolysis
Pharmaceuticals Feedstock temperature ( C) Adsorbate media Solution pH Chemical agent References
Carbamazepine Pine chips 300 Aqueous solution 3.5 Jung et al. (2013)
Bamboo >315 Synthetic and 6.0 and 9.0 Solanki and Boyer (2017)
Softwood pine 550 real urine
Coconut shell 400–500
Northern 400–500
hardwood

Diclofenac Pine chips 300 Aqueous solution 3.5 Jung et al. (2013)
Bamboo >315 Synthetic and 6.0 and 9.0 Solanki and
Softwood pine 550 real urine Boyer (2017)
Coconut shell 400–500
Northern 400–500
hardwood

Ibuprofen Pine chips 300 Aqueous solution 3.5 Jung et al. (2013)
Bamboo >315 Synthetic and 6.0 and 9.0 Solanki and Boyer (2017)
Softwood pine 550 real urine
Coconut shell 400–500
Northern 400–500
hardwood

Naproxen Bamboo >315 Synthetic and 6.0 and 9.0 Solanki and Boyer (2017)
Softwood pine 550 real urine
Coconut shell 400–500
Northern 400–500
hardwood
Bamboo >315 Synthetic and Solanki and Boyer (2019)
Softwood 550 real urine
Sulfamethoxazole Pine 650 Aqueous solution 4.0–9.0 FeCl2 Reguyal et al. (2017)
sawdust
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY

biochar
Pine chips 300 Aqueous solution 3.5 Jung et al. (2013)
Bamboo 550 Aqueous solution 3.0–9.0 CuZnFe2O4 Heo et al. (2019)
Giant reed 300–600 Aqueous solution 1.0–6.0 Zheng et al. (2013)
3029

Tea waste 300 and 700 Water 3.0–9.0 Rajapaksha, Vithanage, Zhang, et al. (2014)
(continued)
Table 2. Continued.
3030

Pyrolysis
Pharmaceuticals Feedstock temperature ( C) Adsorbate media Solution pH Chemical agent References
Sulfamethazine Wheat and 30 and 600 Aqueous solution 1.5–10.2 Jia et al. (2018)
maize straw
Burcucumber 700 Aqueous solution 3.0–9.0 Rajapaksha et al. (2015)
plant
Tea waste
S. U. MASRURA ET AL.

Tetracycline Rice husk 450 Wastewater 2.0 CH3OH Jing et al. (2014)
Cow manure 300–700 Aqueous solution 3–10 Zhang et al. (2019)
Rice straw 700 Aqueous solution 5.0–9.0 H3PO4 Chen et al. (2018)
Swine manure
Bamboo 700 Deionized water 5.0–7.0 SiO2 Zhao et al. (2019)
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3031

et al., 2014; Rajapaksha, Vithanage, Zhang, et al., 2014; Zheng et al., 2013).
For example, SMX being a strong p-acceptor due to N-heteroaromatic
rings and amino functional groups interacts with high temperature biochar
which is a p-donor due to less carboxyl functional groups and high content
of graphitic carbon (Zheng et al., 2013). Similar p-p interactions were
observed during biochar adsorption of TC (Peiris et al., 2017) and
naproxen (Tomul et al., 2020). A study on microalgae derived biochar
showed that the presence of Ca3(PO4)2, CaCO3, and CaNaPO4 may affect
TC adsorption through the metal complexation process (Choi et al., 2020).
As manure-based biochar contains higher ash content and surface oxygen
content, it should be less effective for the adsorption of pharmaceuticals.
Jung et al. (2013) compared the adsorption capacity of four pharmaceuti-
cals (carbamazepine, SMX, ibuprofen, diclofenac) on biochar generated
under oxygen-free (N-biochar) and oxygenated (O-biochar) conditions. N-
biochar contained better polarity moieties content but less aromaticity than
that of O-biochar. While high aromaticity contributed to adsorption,
increased pore volume and surface area of N-biochar led to greater sorp-
tion for pharmaceuticals.
The adsorption capacity of pharmaceuticals can be enhanced by chemical
activation of biochar surface as a result of enhanced surface areas, pore
structures, and interactions with specific surface functional groups. For
example, a surface modification with acid or alkaline substances increased
the availability of oxygen containing functional groups and resulted in
42.92% increase in amoxicillin adsorption (Li et al., 2017). Thermal treat-
ment by using air/nitrogen mixture promoted the mesoporosity on the sur-
face of biochar leading to improved TC adsorption by 5.5–9.2 folds (Zhu et
al., 2018). Steam activated biochar removed 98% more SMZ than non-acti-
vated biochar owing to improved porous structure with larger pore diame-
ters (Rajapaksha et al., 2016).

4.2. Removal of pharmaceuticals


Biochar can remove up to 100% of certain pharmaceutical groups from
human urine (Ahmed et al., 2015). If biochar is selective toward the phar-
maceuticals only, the remedied urine can be applied as a pharmaceutical-
free nutrient product to the soil. A major drawback of this concept is the
disposal or management of pharmaceutical laden biochar. The pharmaceut-
ical loaded biochar must be regenerated, incinerated, or disposed of at a
secure landfill.
The key driving forces for pharmaceuticals adsorption to biochar are van
der Waals force, electrostatic interaction, and hydrogen bonding which are
prevalent at low solution pH (Rajapaksha, Vithanage, Zhang, et al., 2014;
3032 S. U. MASRURA ET AL.

Solanki & Boyer, 2019; Zhang et al., 2019). On the contrary, nutrient
adsorption tends to be more prevalent at higher solution pH. A potential
process for SMZ sorption on biochars at low pH can be described by p-p
EDA interactions between the electron-rich graphene surfaces and proto-
nated amino groups on the aromatic ring (Rajapaksha, Vithanage, Zhang,
et al., 2014; Teixido et al., 2011). Electrostatic interactions and charge dif-
ferential between biochar and pharmaceuticals stimulated the removal of
negatively charged pharmaceuticals, for example, naproxen, ibuprofen, and
diclofenac (Solanki & Boyer, 2017).
The adsorption efficiency of pharmaceuticals decreases with increasing
adsorbate concentration. In contrast, elevating biochar dose will bring
about a better adsorption efficiency, but the treatment cost will increase
(Teixido et al., 2011). The adsorption capacity of biochar for pharmaceuti-
cals enhanced with adsorbent dosage due to a greater number of adsorption
sites and larger surface areas (Shang et al., 2016; Solanki & Boyer, 2017;
Zhang et al., 2019). The contact time between biochar and pharmaceuticals
needs to be chosen in a way that maximum removal can be achieved at
minimum contact time. The longer contact time provided better adsorption
capacity (Solanki & Boyer, 2019) and maximum uptake occurred in the
first 24 h (Teixido et al., 2011). For instance, biochar prepared from soft-
wood delivered the highest sorption capacity for naproxen and paracetamol
with the longest contact time studied (5 days) (Solanki & Boyer, 2019).
Adsorption of the antibiotic SMZ on biochar is a function of adsorbate
pH, competing organic compounds, and inorganic background ions
(Teixido et al., 2011). In general, the maximum sorption efficiency of anti-
biotics was achieved at lower pH values. The p-p EDA interaction con-
trolled the sorption capacity at low pH as SMZ and biochar both were
positively charged. Biochar surface became negatively charged at lower pH,
and the adsorption capacity of SMZ improved due to cation-p bonding
and electrostatic attractive force (Jia et al., 2018).
At pH >6.0, negative charge-assisted hydrogen bond (CAHB) dominated
the adsorption as the SMX and biochar both had negative surface charge
(Li et al., 2014). However, Shang et al.(J. G. Shang et al., 2016) showed that
biochars pyrolyzed at 800  C had maximum adsorption of ciprofloxacin at
pH 7, while the adsorption capacity reduced with the change of pH from 7
to 10. The removal of ciprofloxacin was attributed to the formation of
hydrogen bonding and extents of ionization of ciprofloxacin at different
pH (Li et al., 2014). In a different study, the adsorption of SMX on mag-
netic pine sawdust biochars (MPSB) was affected negatively with the
increase in pH. At higher pH, the negative species present in SMX was
more dominant and had less affinity to MPSB (Reguyal et al., 2017).
Additionally, the presence of humic acid could create obstruction for SMZ
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3033

to adsorb on biochar surface by blocking pores and increasing competition


for adsorption sites (Jia et al., 2018).

4.3. Biochar surface modification for removal of pharmaceuticals


Several articles have reported that surface modifications of biochar could
improve the adsorption capacity by changing the surface chemistry of bio-
char (Jing et al., 2014; Reguyal et al., 2017). Chen et al. (2018) studied the
adsorption capability of TC on H3PO4 modified biochar. The modification
increased the adsorption capacity of TC for manure-based biochar due to
more pore volume and -COOH and -OH groups. Similarly methanol modi-
fied rice husk biochars showed a major increase in adsorption efficiency of
TC compared to unmodified biochar and the increase is attributed to the
enhancement in O containing functional groups (Jing et al., 2014).
Sun et al. (2018) investigated the removal of sulfonamides (SAs) in syn-
thetic urine matrix by H2O2 and biochars. The removal of SAs from aque-
ous solution increased with the increase in biochar doses. The addition of
biochar facilitates the generation of hydroxyl radicals that can degrade the
pharmaceuticals because of its high oxidation potential and low selectivity.
Reguyal and Sarmah (Reguyal & Sarmah, 2018) confirmed that the removal
of SMX using MPSB from aqueous solution is a function of pH as adsorp-
tion capacity decreased at higher solution pH. Similar results observed on
biochars modified by magnetic CuZnFe2O4 composite and the principal
mechanisms for adsorption was CAHB, hydrophobicity, and p–p EDA
interactions (Heo et al., 2019). However, Reguyal et al. (2017) showed that
Fe3O4 formation on the surface of MPSB lower SMX adsorption capability.
A study on silica-biochar composites showed that silica addition
increased the TC adsorption yield, average pore size and total pore volume
of the biochar composites but decreased their surface areas. The silica add-
ition also improved the adsorption capacity of biochars for TC via pore-fill-
ing effect and improved p-p EDA interaction (Zhao et al., 2019). Another
study on NaOH-activated alfalfa derived biochars showed effective adsorp-
tion of TC in water owing to high surface area, high hydrophobicity and
pore volume (Jang & Kan, 2019).
Having higher carbon contents, biochars pyrolyzed at high temperatures
deliver better pharmaceutical adsorption. The solution pH (5) can affect
biochar surface properties and prompt the adsorption process through
hydrogen bond and p-p EDA interactions. The low solution pH is abso-
lutely necessary for effective pharmaceutical adsorption even for biochars
with improved hydrophobicity and p–p EDA interactions through surface
modifications. As described above, biochar has been studied only for cer-
tain groups of pharmaceuticals. In reality, human urine contains several
3034 S. U. MASRURA ET AL.

pharmaceutical compounds depending on the consumption and metabol-


ism, and further studies to cover a wider range of environmentally relevant
pharmaceuticals should be conducted.

5. Future research perspectives


Biochar can serve as an adsorbent for both nutrients and pharmaceuticals
from human urine. Using biochar for nutrient recovery from human urine
and applying it on land could result in the release of pharmaceuticals and/
or their metabolites into the environment through desorption. On a posi-
tive note, this practice is beneficial because contaminants (drugs and/or
metabolites) get removed at the source before they are diluted by other
wastewater streams. Although this process reduces the overall pollution
load in the urine stream, it is not desirable for the application of biochar as
a soil conditioner for the reason given above. Biochars can remove more
than 90% of pharmaceuticals with 20% co-removal of nitrogen and phos-
phate contents present in urine (Solanki & Boyer, 2017). However, limited
studies have considered the capability of biochar to remove both nutrients
and pharmaceuticals at the same time. The following subsections touch on
an approach to avoid the unintentional discharge of pharmaceuticals into
the environment through urine treated biochar and the research gaps
toward the application.

5.1. Application of two separate biochars for selective recovery


Two separate biochars with different characteristics can be applied for sep-
arate nutrient and pharmaceutical extractions in sequence. As illustrated in
Figure 1, pharmaceutical adsorption on biochar is highly pH-dependent
and more favorable at lower solution pH values (<5). The N and P recov-
ery increased gradually with the pH of urine. Biochars pyrolyzed at higher
temperatures were more favorable for pharmaceutical adsorption as the
surface was rich in aromatic rings assisting p-p EDA interactions (Peiris
et al., 2017). Biochars pyrolyzed at lower temperatures offered better
adsorption capacity of NH4þ and phosphate (Figure 2).
Two separate biochars can be put together in series in a filter set to
achieve both N and P recovery, and removal of pharmaceuticals from
source-separated urine at different pH values. In the first filter aimed for
recovery of nutrients, biochar pyrolyzed at low temperatures (<500  C)
having solution pH above 7 can be chosen. In the second filter for adsorp-
tion of pharmaceuticals, the pH of the urine solution needs to be reduced
below 5 and high-temperature biochar is a preferable option due to higher
aromaticity. The key advantage of this process is pH of the urine solution
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3035

Figure 1. Effect of pH on adsorption of ammonium using corn cob biochar (Vu et al., 2017),
phosphate using wheat straw biochar (Dugdug et al., 2018) and sulfamethazine removal using
bur cucumber biochar (Rajapaksha et al., 2016).

Figure 2. Effect of pyrolysis temperature on adsorption of ammonium using Pine sawdust bio-
char (Yang et al., 2018), phosphate using Pine sawdust biochar (Lou et al., 2016) and tetracyc-
line removal using Cow manure biochar (Zhang et al., 2019).

needs to be adjusted once as the pH of urine is generally above 8


(Kirchmann & Pettersson, 1995; Udert et al., 2006; Xu et al., 2018). As dis-
cussed earlier, biochar may pick up a small portion of the pharmaceuticals
3036 S. U. MASRURA ET AL.

Figure 3. Schematic diagram of the process for recovery of nutrients and removal of
pharmaceuticals.

along with nutrients at the first setting, and may be emitted to the environ-
ment during the application of nutrient-rich biochar to the field. Figure 3
displays the schematic representation of this process.
If the filter setting is placed in a way that biochar adsorbs pharmaceuti-
cals first and then another biochar is employed for nutrient recovery, the
problem of environmental release would be substantially less. However, pH
would need to be adjusted twice; first below 5 for removal of pharmaceuti-
cals and then above 7 for nutrient recovery. In that case, biochar removes
most of the pharmaceuticals in the first filter and only low levels of them
remain in the urine stream. The second filter, designed for adsorption of
nutrients, may adsorb the remaining pharmaceuticals along with nutrients,
thereby the risk of soil contamination would be less.
These concepts of using two separate biochars in sequence if applied to source-
separated urine will yield nutrient-rich biochar that will not cause the environ-
mental concern of pharmaceuticals release. In addition, the contaminants (phar-
maceuticals and metabolites) in the urine stream get removed separately at the
source before they are diluted into the wastewater stream. These outcomes are the
best among those delivered by all the different schemes discussed above.
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3037

5.2. Limitations and challenges for application of biochar on human urine


In the last few years, research on biochar has been highlighted for nutrient
removal from wastewater and usage as a soil conditioner to enhance agri-
cultural soil quality and nutrient availability. Studies on nutrient extraction
from urine by biochar have been limited and are highly recommended.
More investigations on not only the excreted pharmaceuticals but also the
metabolites present in urine are needed. In general, metabolites show less
toxicity and bioactivity than the parent pharmaceuticals. However, codeine,
a commonly used pain killer during the postpartum period, produces
metabolite morphine that is more active than the parent drug (Madadi
et al., 2007). Available information on the excreted metabolites in human
urine formed during drug metabolism in human beings is scarce (Zhang,
Sun, et al., 2015). Although this review mostly focuses on the removal of
pharmaceuticals, attention needs to be given to the recognition of human
metabolites of pharmaceuticals in human urine before the application of
biochar for nutrient extraction. However, little attention has been given to
the identification and formation of metabolites of pharmaceuticals
in human.
As discussed in this review, future work should consider the extraction
of nutrients and pharmaceuticals and/or metabolites separately using two
different biochars in sequence. Although the physicochemical properties of
biochar are reliant mostly on the type of feedstock, future studies should
emphasis on the identification of biomass and engineering design for the
production of biochar that shows a higher affinity toward pharmaceuticals
than nutrients or vice versa. Future work should emphasize on formulating
functionalized biochar with better specificity and selectivity for pharma-
ceuticals and nutrients. In addition to the two-stage adsorption process,
future research could involve the removal of pharmaceuticals from urine
first by different processes such as liquid-liquid extraction or biodegrad-
ation followed by nutrient recovery from pharmaceutical-free urine by bio-
char. Ionic liquid can be a potential extraction agent for pharmaceuticals
removal. Also, the surface of biochar can be modified partially to adsorb
nutrients and the non-modified part will attract pharmaceuticals. In that
case, the pharmaceuticals need to be selectively extracted before the land
application of nutrient-rich biochar. Therefore, more research should be
conducted to unravel the relationships between surface modification of bio-
char and nutrients and pharmaceuticals adsorption.
Pharmaceutical laden biochar can be either regenerated for reuse or dis-
posed in a secure landfill. The desorption of adsorbed pharmaceuticals dur-
ing the regeneration may cause secondary pollution and be a disadvantage
for the practical application of biochar as an adsorbent. Thermal regener-
ation process consumes high energy, but the pharmaceuticals will be
3038 S. U. MASRURA ET AL.

mineralized to carbon dioxide. Chemical regeneration of biochar may pro-


duce concentrate/brine which needs further management. On the other
hand, the disposal of exhausted biochar in a secure landfill is not a sustain-
able practice. The reuse/regeneration and safe disposal of pharmaceuticals
laden biochar should be a matter of concern.
This review addresses the use of human urine for closed-loop nutrient
recycling. Further evaluation should include the potential use of animal
urine as it could contain different pharmaceutical metabolites (Vree et al.,
1995). It should be noted that the disposal of animal urine is a matter of
concern due to its tremendous quantity. The effect of the presence of dif-
ferent pathogenic microorganisms in human urine on the recovery of
nutrients needs to be evaluated. Bacteria and pathogens become inactive if
urine is stored for six months. Consequently, potential space constraints
should be considered especially in urban areas. Efficient methods for urine
processing should be established to mitigate occupational health threats to
the people involved in urine treatment and field application of urine
treated biochar, and to reduce the risks associated with urine management
such as urine spills and overflow.
Application of urine treated biochar has exhibited strong potential for
improving soil condition and crop yield. Several important factors need to
be further evaluated such as interactions among soil, biochar, plants, and
nutrient leaching. Potential effects of consumption of biochar fertilized
foods on human health need to be looked at carefully. The application of
urine treated biochar as a sustainable agriculture product requires a new
and holistic understanding of the environmental fate of nutrients and other
constituents in urine particularly desorption behavior and mechanisms.

6. Conclusions
Biochar, a promising and environmentally friendly adsorptive material, can
serve as recovery and treatment media for nutrients and pharmaceuticals,
respectively, from source-separated urine. Application of nutrient-rich bio-
char to low fertility soil can contribute to the habilitation of soil and crop
productivity. This review highlights that the types of feedstock, pyrolysis
conditions, biochar properties, and pH values are the principal factors
influencing biochar adsorption capacities of nutrients and pharmaceuticals.
Using biochar for recovery and delivery of nutrients from urine could
transfer pharmaceuticals to agricultural fields. As emphasized in this
review, separate extraction of nutrients and pharmaceuticals using two dif-
ferent biochars can be placed in a series to eliminate the problem of intro-
ducing pharmaceuticals into the environment. For the proposed in-series
extraction process, low temperature (from 300 to 500  C) biochar is
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3039

effective for nutrient adsorption at solution pH >7 while high temperature


(from 500 to 950  C) biochar is superior for pharmaceutical adsorption at
solution pH <5. Designing suitable biochars with better selectivity and
affinity toward nutrients and pharmaceuticals requires further research
efforts. Proper management of pharmaceuticals-loaded biochar is worth
future research. This article provides new insights on the extraction of
nutrients from source-separated urine by biochar and application of the
nutrient-rich biochar in an environmentally sound manner without the
unintentional release of emerging contaminants to the environment.

ORCID
Yong Sik Ok http://orcid.org/0000-0003-3401-0912
Daniel C. W. Tsang http://orcid.org/0000-0002-6850-733X
Eakalak Khan http://orcid.org/0000-0002-6729-2170

References
Ahmad, M., Lee, S. S., Dou, X., Mohan, D., Sung, J. K., Yang, J. E., & Ok, Y. S. (2012).
Effects of pyrolysis temperature on soybean stover- and peanut shell-derived biochar
properties and TCE adsorption in water. Bioresource Technology, 118, 536–544. https://
doi.org/10.1016/j.biortech.2012.05.042
Ahmad, M., Rajapaksha, A. U., Lim, J. E., Zhang, M., Bolan, N., Mohan, D., Vithanage, M.,
Lee, S. S., & Ok, Y. S. (2014). Biochar as a sorbent for contaminant management in soil and
water: A review. Chemosphere, 99, 19–33. https://doi.org/10.1016/j.chemosphere.2013.10.071
Ahmed, M. B., Zhou, J. L., Ngo, H. H., & Guo, W. (2015). Adsorptive removal of antibiot-
ics from water and wastewater: Progress and challenges. Science of the Total
Environment, 532, 112–126. https://doi.org/10.1016/j.scitotenv.2015.05.130
Ahmed, W., Hamilton, K. A., Vieritz, A., Powell, D., Goonetilleke, A., Hamilton, M. T., &
Gardner, T. (2017). Microbial risk from source-separated urine used as liquid fertilizer
in sub-tropical Australia. Microbial Risk Analysis, 5, 53–64. https://doi.org/10.1016/j.
mran.2016.11.005
Al-Wabel, M. I., Hussain, Q., Usman, A. R. A., Ahmad, M., Abduljabbar, A., Sallam, A. S.,
& Ok, Y. S. (2018). Impact of biochar properties on soil conditions and agricultural sus-
tainability: A review. Land Degradation & Development, 29(7), 2124–2161. https://doi.
org/10.1002/ldr.2829
Bai, X., Li, Z., Zhang, Y., Ni, J., Wang, X., & Zhou, X. (2018). Recovery of ammonium in
urine by biochar derived from faecal sludge and its application as soil conditioner.
Waste and Biomass Valorization, 9(9), 1619–1628. https://doi.org/10.1007/s12649-017-
9906-0
Beesley, L., Moreno-Jimenez, E., & Gomez-Eyles, J. L. (2010). Effects of biochar and green-
waste compost amendments on mobility, bioavailability and toxicity of inorganic and
organic contaminants in a multi-element polluted soil. Environmental Pollution, 158(6),
2282–2287. https://doi.org/10.1016/j.envpol.2010.02.003
Beiyuan, J., Awad, Y. M., Beckers, F., Tsang, D. C. W., Ok, Y. S., & Rinklebe, J. (2017).
Mobility and phytoavailability of As and Pb in a contaminated soil using pine sawdust
3040 S. U. MASRURA ET AL.

biochar under systematic change of redox conditions. Chemosphere, 178, 110–118.


https://doi.org/10.1016/j.chemosphere.2017.03.022

Bischel, H. N., Ozel Duygan, B. D., Strande, L., McArdell, C. S., Udert, K. M., & Kohn, T.
(2015). Pathogens and pharmaceuticals in source-separated urine in eThekwini, South
Africa. Water Research, 85, 57–65. https://doi.org/10.1016/j.watres.2015.08.022
Bolan, N. S., Thangarajan, R., Seshadri, B., Jena, U., Das, K. C., Wang, H., & Naidu, R.
(2013). Landfills as a biorefinery to produce biomass and capture biogas. Bioresource
Technology, 135, 578–587. https://doi.org/10.1016/j.biortech.2012.08.135
Cai, Y., Qi, H., Liu, Y., & He, X. (2016). Sorption/Desorption Behavior and Mechanism of
NH4(þ) by Biochar as a Nitrogen Fertilizer Sustained-Release Material. Journal of
Agricultural and Food Chemistry, 64(24), 4958–4964. https://doi.org/10.1021/acs.jafc.
6b00109
Cao, X., & Harris, W. (2010). Properties of dairy-manure-derived biochar pertinent to its
potential use in remediation. Bioresource Technology, 101(14), 5222–5228. https://doi.org/
10.1016/j.biortech.2010.02.052
Chen, B., Chen, Z., & Lv, S. (2011). A novel magnetic biochar efficiently sorbs organic pol-
lutants and phosphate. Bioresource Technology, 102(2), 716–723. https://doi.org/10.1016/j.
biortech.2010.08.067
Chen, H., Yang, X., Gielen, G., Mandal, S., Xu, S., Guo, J., Shaheen, S. M., Rinklebe, J.,
Che, L., & Wang, H. (2019). Effect of biochars on the bioavailability of cadmium and di-
(2-ethylhexyl) phthalate to Brassica chinensis L. in contaminated soils. Science of the
Total Environment, 678, 43–52. https://doi.org/10.1016/j.scitotenv.2019.04.417
Chen, T., Luo, L., Deng, S., Shi, G., Zhang, S., Zhang, Y., Deng, O., Wang, L., Zhang, J., &
Wei, L. (2018). Sorption of tetracycline on H3PO4 modified biochar derived from rice
straw and swine manure. Bioresource Technology, 267, 431–437. https://doi.org/10.1016/j.
biortech.2018.07.074
Chimenos, J. M., Fernandez, A. I., Villalba, G., Segarra, M., Urruticoechea, A., Artaza, B.,
& Espiell, F. (2003). Removal of ammonium and phosphates from wastewater resulting
from the process of cochineal extraction using MgO-containing by-product. Water
Research, 37(7), 1601–1607. https://doi.org/10.1016/S0043-1354(02)00526-2
Choi, Y. K., Choi, T. R., Gurav, R., Bhatia, S. K., Park, Y. L., Kim, H. J., Kan, E., & Yang,
Y. H. (2020). Adsorption behavior of tetracycline onto Spirulina sp. (microalgae)-derived
biochars produced at different temperatures. The Science of the Total Environment, 710,
136282. https://doi.org/10.1016/j.scitotenv.2019.136282
Cui, X., Dai, X., Khan, K. Y., Li, T., Yang, X., & He, Z. (2016). Removal of phosphate from
aqueous solution using magnesium-alginate/chitosan modified biochar microspheres
derived from Thalia dealbata. Bioresource Technology, 218, 1123–1132. https://doi.org/10.
1016/j.biortech.2016.07.072
de Boer, M. A., Hammerton, M., & Slootweg, J. C. (2018). Uptake of pharmaceuticals by
sorbent-amended struvite fertilisers recovered from human urine and their bioaccumula-
tion in tomato fruit. Water Research, 133, 19–26. https://doi.org/10.1016/j.watres.2018.01.
017
de Jesus Gaffney, V., Cardoso, V. V., Cardoso, E., Teixeira, A. P., Martins, J., Benoliel,
M. J., & Almeida, C. M. M. (2017). Occurrence and behaviour of pharmaceutical com-
pounds in a Portuguese wastewater treatment plant: Removal efficiency through conven-
tional treatment processes. Environmental Science and Pollution Research, 24(17),
14717–14734. https://doi.org/10.1007/s11356-017-9012-7
Desbiolles, F., Malleret, L., Tiliacos, C., Wong-Wah-Chung, P., & Laffont-Schwob, I.
(2018). Occurrence and ecotoxicological assessment of pharmaceuticals: Is there a risk
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3041

for the Mediterranean aquatic environment? The Science of the Total Environment, 639,
1334–1348. https://doi.org/10.1016/j.scitotenv.2018.04.351
Dugdug, A. A., Chang, S. X., Ok, Y. S., Rajapaksha, A. U., & Anyia, A. (2018). Phosphorus
sorption capacity of biochars varies with biochar type and salinity level. Environmental
Science and Pollution Research International, 25(26), 25799–25812. https://doi.org/10.
1007/s11356-018-1368-9
El-Naggar, A., Awad, Y. M., Tang, X. Y., Liu, C., Niazi, N. K., Jien, S. H., Tsang, D. C. W.,
Song, H., Ok, Y. S., & Lee, S. S. (2018). Biochar influences soil carbon pools and facili-
tates interactions with soil: A field investigation. Land Degradation & Development,
29(7), 2162–2171. https://doi.org/10.1002/ldr.2896
El-Naggar, A., Lee, S. S., Awad, Y. M., Yang, X., Ryu, C., Rizwan, M., Rinklebe, J., Tsang,
D. C. W., & Ok, Y. S. (2018). Influence of soil properties and feedstocks on biochar
potential for carbon mineralization and improvement of infertile soils. Geoderma, 332,
100–108. https://doi.org/10.1016/j.geoderma.2018.06.017
El-Naggar, A., Lee, S. S., Rinklebe, J., Farooq, M., Song, H., Sarmah, A. K., Zimmerman,
A. R., Ahmad, M., Shaheen, S. M., & Ok, Y. S. (2019). Biochar application to low fertility
soils: A review of current status, and future prospects. Geoderma, 337, 536–554. https://
doi.org/10.1016/j.geoderma.2018.09.034
Fang, Z., Gao, Y., Bolan, N., Shaheen, S. M., Xu, S., Wu, X., Xu, X., Hu, H., Lin, J., Zhang,
F., Li, J., Rinklebe, J., & Wang, H. (2020). Conversion of biological solid waste to gra-
phene-containing biochar for water remediation: A critical review. Chemical Engineering
Journal, 390, 124611. https://doi.org/10.1016/j.cej.2020.124611
Fernandez-Torres, R., Consentino, M. O., Lopez, M. A. B., & Mochon, M. C. (2010).
Simultaneous determination of 11 antibiotics and their main metabolites from four dif-
ferent groups by reversed-phase high-performance liquid chromatography-diode array-
fluorescence (HPLC-DAD-FLD) in human urine samples. Talanta, 81(3), 871–880.
https://doi.org/10.1016/j.talanta.2010.01.031
Gai, X., Wang, H., Liu, J., Zhai, L., Liu, S., Ren, T., & Liu, H. (2014). Effects of feedstock
and pyrolysis temperature on biochar adsorption of ammonium and nitrate. PLoS One,
9(12), e113888. https://doi.org/10.1371/journal.pone.0113888
Garcıa-Galan, M. J., Gonzalez Blanco, S., L opez Roldan, R., Dıaz-Cruz, S., & Barcel
o, D.
(2012). Ecotoxicity evaluation and removal of sulfonamides and their acetylated metabo-
lites during conventional wastewater treatment. The Science of the Total Environment,
437, 403–412. https://doi.org/10.1016/j.scitotenv.2012.08.038
Hamilton, K. A., Ahmed, W., Rauh, E., Rock, C., McLain, J., & Muenich, R. L. (2020).
Comparing microbial risks from multiple sustainable waste streams applied for agricul-
tural use: Biosolids, manure, and diverted urine. Current Opinion in Environmental
Science & Health, 14, 37–50. https://doi.org/10.1016/j.coesh.2020.01.003
Heinonen-Tanski, H., Sj€ oblom, A., Fabritius, H., & Karinen, P. (2007). Pure human urine
is a good fertiliser for cucumbers. Bioresource Technology, 98(1), 214–217. https://doi.
org/10.1016/j.biortech.2005.11.024
Heo, J., Yoon, Y., Lee, G., Kim, Y., Han, J., & Park, C. M. (2019). Enhanced adsorption of
bisphenol A and sulfamethoxazole by a novel magnetic CuZnFe2O4-biochar composite.
Bioresource Technology, 281, 179–187. https://doi.org/10.1016/j.biortech.2019.02.091
Huang, Y., Lee, X., Grattieri, M., Yuan, M., Cai, R., Macazo, F. C., & Minteer, S. D. (2020).
Modified biochar for phosphate adsorption in environmentally relevant conditions.
Chemical Engineering Journal, 380, 122375. https://doi.org/10.1016/j.cej.2019.122375
Igalavithana, A. D., Kim, K. H., Jung, J. M., Heo, H. S., Kwon, E. E., Tack, F. M. G.,
Tsang, D. C. W., Jeon, Y. J., & Ok, Y. S. (2019). Effect of biochars pyrolyzed in N2 and
3042 S. U. MASRURA ET AL.

CO2, and feedstock on microbial community in metal(loid)s contaminated soils.


Environment International, 126, 791–801. https://doi.org/10.1016/j.envint.2019.02.061
Igalavithana, A. D., Lee, S. E., Lee, Y. H., Tsang, D. C. W., Rinklebe, J., Kwon, E. E., & Ok,
Y. S. (2017). Heavy metal immobilization and microbial community abundance by vege-
table waste and pine cone biochar of agricultural soils. Chemosphere, 174, 593–603.
https://doi.org/10.1016/j.chemosphere.2017.01.148
Igalavithana, A. D., Mandal, S., Niazi, N. K., Vithanage, M., Parikh, S. J., Mukome,
F. N. D., Rizwan, M., Oleszczuk, P., Al-Wabel, M., Bolan, N., Tsang, D. C. W., Kim,
K. H., & Ok, Y. S. (2017). Advances and future directions of biochar characterization
methods and applications. Critical Reviews in Environmental Science and Technology,
47(23), 2275–2330. https://doi.org/10.1080/10643389.2017.1421844
Inyang, M., & Dickenson, E. (2015). The potential role of biochar in the removal of organic
and microbial contaminants from potable and reuse water: A review. Chemosphere, 134,
232–240. https://doi.org/10.1016/j.chemosphere.2015.03.072
Jang, H. M., & Kan, E. (2019). Engineered biochar from agricultural waste for removal of
tetracycline in water. Bioresource Technology, 284, 437–447. https://doi.org/10.1016/j.bio-
rtech.2019.03.131
Jang, J., Miran, W., Divine, S. D., Nawaz, M., Shahzad, A., Woo, S. H., & Lee, D. S. (2018).
Rice straw-based biochar beads for the removal of radioactive strontium from aqueous
solution. The Science of the Total Environment, 615, 698–707. https://doi.org/10.1016/j.
scitotenv.2017.10.023
Jeon, E. K., Ryu, S., Park, S. W., Wang, L., Tsang, D. C. W., & Baek, K. (2018). Enhanced
adsorption of arsenic onto alum sludge modified by calcination. Journal of Cleaner
Production, 176, 54–62. https://doi.org/10.1016/j.jclepro.2017.12.153
Jia, M., Wang, F., Bian, Y., Stedtfeld, R. D., Liu, G., Yu, J., & Jiang, X. (2018). Sorption of
sulfamethazine to biochars as affected by dissolved organic matters of different origin.
Bioresource Technology, 248(Pt B), 36–43. https://doi.org/10.1016/j.biortech.2017.08.082
Jiang, Y. H., Li, A. Y., Deng, H., Ye, C. H., Wu, Y. Q., Linmu, Y. D., & Hang, H. L.
(2019). Characteristics of nitrogen and phosphorus adsorption by Mg-loaded biochar
from different feedstocks. Bioresource Technology, 276, 183–189. https://doi.org/10.1016/j.
biortech.2018.12.079
Jing, X. R., Wang, Y. Y., Liu, W. J., Wang, Y. K., & Jiang, H. (2014). Enhanced adsorption
performance of tetracycline in aqueous solutions by methanol-modified biochar.
Chemical Engineering Journal, 248, 168–174. https://doi.org/10.1016/j.cej.2014.03.006
Jones-Lepp, T. L., Alvarez, D. A., Petty, J. D., & Huckins, J. N. (2004). Polar organic chem-
ical integrative sampling and liquid chromatography-electrospray/ion-trap mass spec-
trometry for assessing selected prescription and illicit drugs in treated sewage effluents.
Archives of Environmental Contamination and Toxicology, 47(4), 427–439. https://doi.
org/10.1007/s00244-004-3146-6
Joseph, S. D., Downie, A., Munroe, P., Crosky, A., Lehmann, J. (2007). Biochar for carbon
sequestration, reduction of greenhouse gas emissions and enhancement of soil fertility: A
review of the materials science. Proceedings of the Australian Combustion Symposium,
pp. 130–133.
Jung, C., Park, J., Lim, K. H., Park, S., Heo, J., Her, N., Oh, J., Yun, S., & Yoon, Y. (2013).
Adsorption of selected endocrine disrupting compounds and pharmaceuticals on acti-
vated biochars. Journal of Hazardous Materials, 263, 702–710. https://doi.org/10.1016/j.
jhazmat.2013.10.033
Jung, K. W., Hwang, M. J., Ahn, K. H., & Ok, Y. S. (2015). Kinetic study on phosphate
removal from aqueous solution by biochar derived from peanut shell as renewable
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3043

adsorptive media. International Journal of Environmental Science and Technology, 12(10),


3363–3372. https://doi.org/10.1007/s13762-015-0766-5
Jung, K. W., Kim, K., Jeong, T. U., & Ahn, K. H. (2016). Influence of pyrolysis temperature
on characteristics and phosphate adsorption capability of biochar derived from waste-
marine macroalgae (Undaria pinnatifida roots). Bioresource Technology, 200, 1024–1028.
https://doi.org/10.1016/j.biortech.2015.10.016
Karak, T., & Bhattacharyya, P. (2011). Human urine as a source of alternative natural fertil-
izer in agriculture: A flight of fancy or an achievable reality. Resources, Conservation and
Recycling, 55(4), 400–408. https://doi.org/10.1016/j.resconrec.2010.12.008
Kirchmann, H., & Pettersson, S. (1995). Human urine - Chemical composition and fertilizer
use efficiency. Fertilizer Research, 40(2), 149–154. https://doi.org/10.1007/BF00750100
Kumar, A., Singh, E., Khapre, A., Bordoloi, N., & Kumar, S. (2020). Sorption of volatile
organic compounds on non-activated biochar. Bioresource Technology, 297, 122469.
https://doi.org/10.1016/j.biortech.2019.122469
Kwak, J. H., Islam, M. S., Wang, S., Messele, S. A., Naeth, M. A., El-Din, M. G., & Chang,
S. X. (2019). Biochar properties and lead(II) adsorption capacity depend on feedstock
type, pyrolysis temperature, and steam activation. Chemosphere, 231, 393–404. https://
doi.org/10.1016/j.chemosphere.2019.05.128
Larsen, T. A., & Gujer, W. (1996). Separate management of anthropogenic nutrient solu-
tions (human urine). Water Science and Technology, 34(3–4), 87–94. https://doi.org/10.
2166/wst.1996.0420
Lee, J., Yang, X., Cho, S. H., Kim, J. K., Lee, S. S., Tsang, D. C. W., Ok, Y. S., & Kwon,
E. E. (2017). Pyrolysis process of agricultural waste using CO2 for waste management,
energy recovery, and biochar fabrication. Applied Energy, 185, 214–222. https://doi.org/
10.1016/j.apenergy.2016.10.092
Lehmann, J., Skjemstad, J., Sohi, S., Carter, J., Barson, M., Falloon, P., Coleman, K.,
Woodbury, P., & Krull, E. (2008). Australian climate-carbon cycle feedback reduced by
soil black carbon. Nature Geoscience, 1(12), 832–835. https://doi.org/10.1038/ngeo358
Li, H., Zhang, D., Han, X., & Xing, B. (2014). Adsorption of antibiotic ciprofloxacin on
carbon nanotubes: PH dependence and thermodynamics. Chemosphere, 95, 150–155.
https://doi.org/10.1016/j.chemosphere.2013.08.053
Li, H., Dong, X., da Silva, E. B., de Oliveira, L. M., Chen, Y., & Ma, L. Q. (2017).
Mechanisms of metal sorption by biochars: Biochar characteristics and modifications.
Chemosphere, 178, 466–478. https://doi.org/10.1016/j.chemosphere.2017.03.072
Li, J., Li, B., Huang, H., Lv, X., Zhao, N., Guo, G., & Zhang, D. (2019). Removal of phos-
phate from aqueous solution by dolomite-modified biochar derived from urban dewa-
tered sewage sludge. The Science of the Total Environment, 687, 460–469. https://doi.org/
10.1016/j.scitotenv.2019.05.400
Li, R., Wang, J. J., Zhou, B., Awasthi, M. K., Ali, A., Zhang, Z., Lahori, A. H., & Mahar, A.
(2016). Recovery of phosphate from aqueous solution by magnesium oxide decorated
magnetic biochar and its potential as phosphate-based fertilizer substitute. Bioresource
Technology, 215, 209–214. https://doi.org/10.1016/j.biortech.2016.02.125
Li, Y., Zhang, L., Ding, J., & Liu, X. (2020). Prioritization of pharmaceuticals in water
environment in China based on environmental criteria and risk analysis of top-priority
pharmaceuticals. Journal of Environmental Management, 253, 109732. https://doi.org/10.
1016/j.jenvman.2019.109732
Lienert, J., B€urki, T., & Escher, B. I. (2007). Reducing micropollutants with source control:
Substance flow analysis of 212 pharmaceuticals in faeces and urine. Water Science and
Technology, 56(5), 87–96. https://doi.org/10.2166/wst.2007.560
3044 S. U. MASRURA ET AL.

Liu, Z., Han, Y., Jing, M., & Chen, J. (2017). Sorption and transport of sulfonamides in
soils amended with wheat straw-derived biochar: Effects of water pH, coexistence copper
ion, and dissolved organic matter. Journal of Soils and Sediments, 17(3), 771–779. https://
doi.org/10.1007/s11368-015-1319-8
Lou, K., Rajapaksha, A. U., Ok, Y. S., & Chang, S. X. (2016). Pyrolysis temperature and
steam activation effects on sorption of phosphate on pine sawdust biochars in aqueous
solutions. Chemical Speciation & Bioavailability, 28(1–4), 42–50. https://doi.org/10.1080/
09542299.2016.1165080
Mack, G. (1992). Improved high-performance liquid chromatographic determination of
ciprofloxacin and its metabolites in human specimens. Journal of Chromatography B:
Biomedical Sciences and Applications, 582(1–2), 263–267. https://doi.org/10.1016/0378-
4347(92)80331-J
Madadi, P., Koren, G., Cairns, J., Chitayat, D., Gaedigk, A., Leeder, J. S., Teitelbaum, R.,
Karaskov, T., & Aleksa, K. (2007). Safety of codeine during breastfeeding: Fatal morphine
poisoning in the breastfed neonate of a mother prescribed codeine. Canadian Family
Physician Medecin de Famille Canadien, 53(1), 33–35.
Mnkeni, P. N. S., Kutu, F. R., Muchaonyerwa, P., & Austin, L. M. (2008). Evaluation of
human urine as a source of nutrients for selected vegetables and maize under tunnel
house conditions in the Eastern Cape, South Africa. Waste Management & Research,
26(2), 132–139. https://doi.org/10.1177/0734242X07079179
Park, J. H., Ok, Y. S., Kim, S. H., Cho, J. S., Heo, J. S., Delaune, R. D., & Seo, D. C. (2015).
Evaluation of phosphorus adsorption capacity of sesame straw biochar on aqueous solu-
tion: Influence of activation methods and pyrolysis temperatures. Environmental
Geochemistry and Health, 37(6), 969–983. https://doi.org/10.1007/s10653-015-9709-9
Peiris, C., Gunatilake, S. R., Mlsna, T. E., Mohan, D., & Vithanage, M. (2017). Biochar based
removal of antibiotic sulfonamides and tetracyclines in aquatic environments: A critical
review. Bioresource Technology, 246, 150–159. https://doi.org/10.1016/j.biortech.2017.07.150
Peng, Y., Sun, Y., Sun, R., Zhou, Y., Tsang, D. C. W., & Chen, Q. (2019). Optimizing the
synthesis of Fe/Al (Hydr)oxides-Biochars to maximize phosphate removal via response
surface model. Journal of Cleaner Production, 237, 117770. https://doi.org/10.1016/j.jcle-
pro.2019.117770
Qiu, Y., Zheng, Z., Zhou, Z., & Sheng, G. D. (2009). Effectiveness and mechanisms of dye
adsorption on a straw-based biochar. Bioresource Technology, 100(21), 5348–5351.
https://doi.org/10.1016/j.biortech.2009.05.054
Rajapaksha, A. U., Vithanage, M., Ahmad, M., Seo, D. C., Cho, J. S., Lee, S. E., Lee, S. S.,
& Ok, Y. S. (2015). Enhanced sulfamethazine removal by steam-activated invasive plant-
derived biochar. Journal of Hazardous Materials, 290, 43–50. https://doi.org/10.1016/j.
jhazmat.2015.02.046
Rajapaksha, A. U., Vithanage, M., Lee, S. S., Seo, D. C., Tsang, D. C. W., & Ok, Y. S.
(2016). Steam activation of biochars facilitates kinetics and pH-resilience of sulfametha-
zine sorption. Journal of Soils and Sediments, 16(3), 889–895. https://doi.org/10.1007/
s11368-015-1325-x
Rajapaksha, A. U., Vithanage, M., Lim, J. E., Ahmed, M. B. M., Zhang, M., Lee, S. S., &
Ok, Y. S. (2014). Invasive plant-derived biochar inhibits sulfamethazine uptake by lettuce
in soil. Chemosphere, 111, 500–504. https://doi.org/10.1016/j.chemosphere.2014.04.040
Rajapaksha, A. U., Vithanage, M., Zhang, M., Ahmad, M., Mohan, D., Chang, S. X., & Ok,
Y. S. (2014). Pyrolysis condition affected sulfamethazine sorption by tea waste biochars.
Bioresource Technology, 166, 303–308. https://doi.org/10.1016/j.biortech.2014.05.029
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3045

Reguyal, F., & Sarmah, A. K. (2018). Adsorption of sulfamethoxazole by magnetic biochar:


Effects of pH, ionic strength, natural organic matter and 17a-ethinylestradiol. The
Science of the Total Environment, 628-629, 722–730. https://doi.org/10.1016/j.scitotenv.
2018.01.323
Reguyal, F., Sarmah, A. K., & Gao, W. (2017). Synthesis of magnetic biochar from pine
sawdust via oxidative hydrolysis of FeCl2 for the removal sulfamethoxazole from aqueous
solution. Journal of Hazardous Materials, 321, 868–878. https://doi.org/10.1016/j.jhazmat.
2016.10.006
Rose, C., Parker, A., Jefferson, B., & Cartmell, E. (2015). The characterization of feces and
urine: A review of the literature to inform advanced treatment technology. Critical
Reviews in Environmental Science and Technology, 45(17), 1827–1879. https://doi.org/10.
1080/10643389.2014.1000761
Shaaban, M., Van Zwieten, L., Bashir, S., Younas, A., N un~ez-Delgado, A., Chhajro, M. A.,
Kubar, K. A., Ali, U., Rana, M. S., Mehmood, M. A., & Hu, R. (2018). A concise review
of biochar application to agricultural soils to improve soil conditions and fight pollution.
Journal of Environmental Management, 228, 429–440. https://doi.org/10.1016/j.jenvman.
2018.09.006
Shang, G., Shen, G., Liu, L., Chen, Q., & Xu, Z. (2013). Kinetics and mechanisms of hydro-
gen sulfide adsorption by biochars. Bioresource Technology, 133, 495–499. https://doi.org/
10.1016/j.biortech.2013.01.114
Shang, J. G., Kong, X. R., He, L. L., Li, W. H., & Liao, Q. J. H. (2016). Low-cost biochar
derived from herbal residue: Characterization and application for ciprofloxacin adsorp-
tion. International Journal of Environmental Science and Technology, 13(10), 2449–2458.
https://doi.org/10.1007/s13762-016-1075-3
Shepherd, J. G., Joseph, S., Sohi, S. P., & Heal, K. V. (2017). Biochar and enhanced phos-
phate capture: Mapping mechanisms to functional properties. Chemosphere, 179, 57–74.
https://doi.org/10.1016/j.chemosphere.2017.02.123
Solanki, A., & Boyer, T. H. (2017). Pharmaceutical removal in synthetic human urine using
biochar. Environmental Science: Water Research & Technology, 3(3), 553–565. https://doi.
org/10.1039/C6EW00224B
Solanki, A., & Boyer, T. H. (2019). Physical-chemical interactions between pharmaceuticals
and biochar in synthetic and real urine. Chemosphere, 218, 818–826. https://doi.org/10.
1016/j.chemosphere.2018.11.179
Sridevi, G., Srinivasamurthy, C. A., Bhaskar, S., & Viswanath, S. (2009). Evaluation of
source separated human urine (ALW) as a source of nutrients for banana cultivation.
ARPN Journal of Agricultural and Biological Science, 4(5), 44–48.
Stewart, C. E., Zheng, J., Botte, J., & Cotrufo, M. F. (2013). Co-generated fast pyrolysis bio-
char mitigates green-house gas emissions and increases carbon sequestration in temper-
ate soils. GCB Bioenergy, 5(2), 153–164. https://doi.org/10.1111/gcbb.12001
Sun, P., Li, Y., Meng, T., Zhang, R., Song, M., & Ren, J. (2018). Removal of sulfonamide
antibiotics and human metabolite by biochar and biochar/H2O2 in synthetic urine.
Water Research, 147, 91–100. https://doi.org/10.1016/j.watres.2018.09.051
Sun, Y., Gao, B., Yao, Y., Fang, J., Zhang, M., Zhou, Y., Chen, H., & Yang, L. (2014).
Effects of feedstock type, production method, and pyrolysis temperature on biochar and
hydrochar properties. Chemical Engineering Journal, 240, 574–578. https://doi.org/10.
1016/j.cej.2013.10.081
Taghizadeh-Toosi, A., Clough, T. J., Sherlock, R. R., & Condron, L. M. (2012). A wood
based low-temperature biochar captures NH3-N generated from ruminant urine-N,
3046 S. U. MASRURA ET AL.

retaining its bioavailability. Plant and Soil, 353(1–2), 73–84. https://doi.org/10.1007/


s11104-011-1010-9
Takaya, C. A., Fletcher, L. A., Singh, S., Anyikude, K. U., & Ross, A. B. (2016a). Phosphate
and ammonium sorption capacity of biochar and hydrochar from different wastes.
Chemosphere, 145, 518–527. https://doi.org/10.1016/j.chemosphere.2015.11.052
Takaya, C. A., Fletcher, L. A., Singh, S., Okwuosa, U. C., & Ross, A. B. (2016b). Recovery
of phosphate with chemically modified biochars. Journal of Environmental Chemical
Engineering, 4(1), 1156–1165. https://doi.org/10.1016/j.jece.2016.01.011
Tarpeh, W. A., Udert, K. M., & Nelson, K. L. (2017). Comparing ion exchange adsorbents
for nitrogen recovery from source-separated urine. Environmental Science & Technology,
51(4), 2373–2381. https://doi.org/10.1021/acs.est.6b05816
Teixid
o, M., Pignatello, J. J., Beltran, J. L., Granados, M., & Peccia, J. (2011). Speciation of
the ionizable antibiotic sulfamethazine on black carbon (Biochar). Environmental Science
& Technology, 45(23), 10020–10027. https://doi.org/10.1021/es202487h
Tomul, F., Arslan, Y., Kabak, B., Trak, D., Kend€ uzler, E., Lima, E. C., & Tran, H. N. (2020).
Peanut shells-derived biochars prepared from different carbonization processes: Comparison
of characterization and mechanism of naproxen adsorption in water. The Science of the Total
Environment, 726, 137828. https://doi.org/10.1016/j.scitotenv.2020.137828
Trazzi, P. A., Leahy, J. J., Hayes, M. H. B., & Kwapinski, W. (2016). Adsorption and
desorption of phosphate on biochars. Journal of Environmental Chemical Engineering,
4(1), 37–46. https://doi.org/10.1016/j.jece.2015.11.005
Udert, K. M. (2002). The fate of nitrogen and phosphorus in source-separated urine.
[Doctoral dissertation]. https://doi.org/10.3929/ETHZ-A-004541820
Udert, K. M., Larsen, T. A., & Gujer, W. (2006). Fate of major compounds in source-sepa-
rated urine. Water Science and Technology, 54(11–12), 413–420. https://doi.org/10.2166/
wst.2006.921
Vikrant, K., Kim, K. H., Ok, Y. S., Tsang, D. C. W., Tsang, Y. F., Giri, B. S., & Singh, R. S.
(2018). Engineered/designer biochar for the removal of phosphate in water and waste-
water. The Science of the Total Environment, 616-617, 1242–1260. https://doi.org/10.
1016/j.scitotenv.2017.10.193
Vinnerås, B., & J€onsson, H. (2002). The performance and potential of faecal separation and
urine diversion to recycle plant nutrients in household wastewater. Bioresource
Technology, 84(3), 275–282. https://doi.org/10.1016/S0960-8524(02)00054-8
Vree, T. B., Hekster, Y. A., Baars, A. M., Damsma, J. E., & Van Der Kleijn, E. (1978).
Determination of trimethoprim and sulfamethoxazole (co-trimoxazole) in body fluids of
man by means of high-performance liquid chromatography. Journal of Chromatography
B: Biomedical Sciences and Applications, 146(1), 103–112. https://doi.org/10.1016/S0378-
4347(00)81294-3
Vree, T. B., van de Ven, E. S., Verwey-van Wissen, C. P. W. G. M., Baars, A. M., Swolfs,
A., van Galen, P. M., & Amatdjais-Groenen, H. (1995). Isolation, identification and
determination of sulfadiazine and its hydroxy metabolites and conjugates from man and
Rhesus monkey by high-performance liquid chromatography. Journal of Chromatography
B: Biomedical Sciences and Applications, 670(1), 111–123. https://doi.org/10.1016/0378-
4347(95)00163-D
Vu, T. M., Trinh, V. T., Doan, D. P., Van, H. T., Nguyen, T. V., Vigneswaran, S., & Ngo,
H. H. (2017). Removing ammonium from water using modified corncob-biochar. The
Science of the Total Environment, 579, 612–619. https://doi.org/10.1016/j.scitotenv.2016.
11.050
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3047

Wang, R. Z., Huang, D. L., Liu, Y. G., Zhang, C., Lai, C., Wang, X., Zeng, G. M., Zhang,
Q., Gong, X. M., & Xu, P. (2020). Synergistic removal of copper and tetracycline from
aqueous solution by steam-activated bamboo-derived biochar. Journal of Hazardous
Materials, 384(384), 121470. https://doi.org/10.1016/j.jhazmat.2019.121470
Wang, Z., Guo, H., Shen, F., Yang, G., Zhang, Y., Zeng, Y., Wang, L., Xiao, H., & Deng, S.
(2015). Biochar produced from oak sawdust by Lanthanum (La)-involved pyrolysis for
adsorption of ammonium (NH4(þ)), nitrate (NO3(-)), and phosphate (PO4(3-)).
Chemosphere, 119, 646–653. https://doi.org/10.1016/j.chemosphere.2014.07.084
Wei, S. P., van Rossum, F., van de Pol, G. J., & Winkler, M. K. H. (2018). Recovery of
phosphorus and nitrogen from human urine by struvite precipitation, air stripping and
acid scrubbing: A pilot study. Chemosphere, 212, 1030–1037. https://doi.org/10.1016/j.
chemosphere.2018.08.154
World Health Organization. (2006). WHO guidelines for the safe use of wastewater, excreta
and greywater. In Excreta and greywater use in agriculture (Vol. 4, pp. 39–42). World
Health Organization.
Wilsenach, J., & van Loosdrecht, M. (2003). Impact of separate urine collection on waste-
water treatment systems. Water Science and Technology, 48(1), 103–110. https://doi.org/
10.2166/wst.2003.0027
Wilsenach, J. A., Schuurbiers, C. A. H., & van Loosdrecht, M. C. M. (2007). Phosphate and
potassium recovery from source separated urine through struvite precipitation. Water
Research, 41(2), 458–466. https://doi.org/10.1016/j.watres.2006.10.014
Wilsenach, J. A., & van Loosdrecht, M. C. M. (2006). Integration of processes to treat
wastewater and source-separated urine. Journal of Environmental Engineering, 132(3),
331–341. https://doi.org/10.1061/(ASCE)0733-9372(2006)132:3(331)
Windeatt, J. H., Ross, A. B., Williams, P. T., Forster, P. M., Nahil, M. A., & Singh, S.
(2014). Characteristics of biochars from crop residues: Potential for carbon sequestration
and soil amendment. Journal of Environmental Management, 146, 189–197. https://doi.
org/10.1016/j.jenvman.2014.08.003
Xie, M., Chen, W., Xu, Z., Zheng, S., & Zhu, D. (2014). Adsorption of sulfonamides to
demineralized pine wood biochars prepared under different thermochemical conditions.
Environmental Pollution, 186, 187–194. https://doi.org/10.1016/j.envpol.2013.11.022
Xu, K., Lin, F., Dou, X., Zheng, M., Tan, W., & Wang, C. (2018). Recovery of ammonium
and phosphate from urine as value-added fertilizer using wood waste biochar loaded
with magnesium oxides. Journal of Cleaner Production, 187, 205–214. https://doi.org/10.
1016/j.jclepro.2018.03.206
Xu, K., Zhang, C., Dou, X., Ma, W., & Wang, C. (2019). Optimizing the modification of
wood waste biochar via metal oxides to remove and recover phosphate from human
urine. Environmental Geochemistry and Health, 41(4), 1767–1776. https://doi.org/10.
1007/s10653-017-9986-6
Xu, T., Lou, L., Luo, L., Cao, R., Duan, D., & Chen, Y. (2012). Effect of bamboo biochar
on pentachlorophenol leachability and bioavailability in agricultural soil. Science of the
Total Environment, 414, 727–731. https://doi.org/10.1016/j.scitotenv.2011.11.005
Yang, F., Zhang, S., Sun, Y., Tsang, D. C. W., Cheng, K., & Sik, Y. (2019). Assembling bio-
char with various layered double hydroxides for enhancement of phosphorus recovery.
Journal of Hazardous Materials, 365, 665–673. https://doi.org/10.1016/j.jhazmat.2018.11.047
Yang, H. I., Lou, K., Rajapaksha, A. U., Ok, Y. S., Anyia, A. O., & Chang, S. X. (2018).
Adsorption of ammonium in aqueous solutions by pine sawdust and wheat straw bio-
chars. Environmental Science and Pollution Research International, 25(26), 25638–25647.
https://doi.org/10.1007/s11356-017-8551-2
3048 S. U. MASRURA ET AL.

Yao, Y., Gao, B., Inyang, M., Zimmerman, A. R., Cao, X., Pullammanappallil, P., & Yang,
L. (2011). Removal of phosphate from aqueous solution by biochar derived from anaer-
obically digested sugar beet tailings. Journal of Hazardous Materials, 190(1–3), 501–507.
https://doi.org/10.1016/j.jhazmat.2011.03.083
Yuan, P., Wang, J., Pan, Y., Shen, B., & Wu, C. (2019). Review of biochar for the manage-
ment of contaminated soil: Preparation, application and prospect. The Science of the
Total Environment, 659, 473–490. https://doi.org/10.1016/j.scitotenv.2018.12.400
Zhang, P., Li, Y., Cao, Y., & Han, L. (2019). Characteristics of tetracycline adsorption by
cow manure biochar prepared at different pyrolysis temperatures. Bioresource
Technology, 285, 121348. https://doi.org/10.1016/j.biortech.2019.121348
Zhang, R., Sun, P., Boyer, T. H., Zhao, L., & Huang, C. H. (2015). Degradation of pharma-
ceuticals and metabolite in synthetic human urine by UV, UV/H2O2, and UV/PDS.
Environmental Science & Technology, 49(5), 3056–3066. https://doi.org/10.1021/
es504799n
Zhang, X., Wang, H., He, L., Lu, K., Sarmah, A., Li, J., Bolan, N. S., Pei, J., & Huang, H.
(2013). Using biochar for remediation of soils contaminated with heavy metals and
organic pollutants. Environmental Science and Pollution Research International, 20(12),
8472–8483. https://doi.org/10.1007/s11356-013-1659-0
Zhang, Y., Li, Z., & Mahmood, I. B. (2015). Effects of corn cob produced biochars on urea
recovery from human urine and their application as soil conditioners. CLEAN - Soil, Air,
Water, 43(8), 1167–1173. https://doi.org/10.1002/clen.201400489
Zhao, Z., Nie, T., & Zhou, W. (2019). Enhanced biochar stabilities and adsorption proper-
ties for tetracycline by synthesizing silica-composited biochar. Environmental Pollution,
254(Pt A), 113015. https://doi.org/10.1016/j.envpol.2019.113015
Zheng, H., Wang, Z., Zhao, J., Herbert, S., & Xing, B. (2013). Sorption of antibiotic sulfa-
methoxazole varies with biochars produced at different temperatures. Environmental
Pollution, 181, 60–67. https://doi.org/10.1016/j.envpol.2013.05.056
Zheng, M., Xie, T., Li, J., Xu, K., & Wang, C. (2018). Biochar as a carrier of struvite pre-
cipitation for nitrogen and phosphorus recovery from urine. Journal of Environmental
Engineering, 144(10), 04018101. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001450
Zhu, X., Li, C., Li, J., Xie, B., L€
u, J., & Li, Y. (2018). Thermal treatment of biochar in the air/
nitrogen atmosphere for developed mesoporosity and enhanced adsorption to tetracycline.
Bioresource Technology, 263, 475–482. https://doi.org/10.1016/j.biortech.2018.05.041
Zornoza, R., Moreno-Barriga, F., Acosta, J. A., Mu~ noz, M. A., & Faz, A. (2016). Stability,
nutrient availability and hydrophobicity of biochars derived from manure, crop residues,
and municipal solid waste for their use as soil amendments. Chemosphere, 144, 122–130.
https://doi.org/10.1016/j.chemosphere.2015.08.046

You might also like