Moiji 2022 Pharmaceuticals and Personal Care Products in Aquatic Environments and Their Removal by Algae-Based Systems.
Moiji 2022 Pharmaceuticals and Personal Care Products in Aquatic Environments and Their Removal by Algae-Based Systems.
Moiji 2022 Pharmaceuticals and Personal Care Products in Aquatic Environments and Their Removal by Algae-Based Systems.
Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere
H I G H L I G H T S G R A P H I C A L A B S T R A C T
A R T I C L E I N F O A B S T R A C T
Handling Editor: Y Yeomin Yoon The consumption of pharmaceuticals and personal care products (PPCPs) has been widely increasing, yet up to
90–95% of PPCPs consumed by human are excreted unmetabolized. Moreover, the most of PPCPs cannot be fully
Keywords: removed by wastewater treatment plants (WWTPs), which release PPCPs to natural water bodies, affecting
Algae aquatic ecosystems and potentially humans. This study sought to review the occurrence of PPCPs in natural water
Genes
bodies globally, and assess the effects of important factors on the fluxes of pollutants into receiving waterways.
Groundwater
The highest ibuprofen concentration (3738 ng/L) in tap water was reported in Nigeria, and the highest naproxen
Pharmaceuticals
Wastewater concentration (37,700 ng/L) was reported in groundwater wells in Penn State, USA. Moreover, the PPCPs have
affected aquatic organisms such as fish. For instance, up to 24.4 × 103 ng/g of atenolol was detected in
P. lineatus. Amongst different technologies to eliminate PPCPs, algae-based systems are environmentally friendly
and effective because of the photosynthetic ability of algae to absorb CO2 and their flexibility to grow in different
wastewater. Up to 99% of triclosan and less than 10% of trimethoprim were removed by Nannochloris sp., green
algae. Moreover, variable concentrations of PPCPs might adversely affect the growth and production of algae.
The exposure of algae to high concentrations of PPCPs can reduce the content of chlorophyll and protein due to
* Corresponding author. Faculty of Sciences and Technology, Norwegian University of Life Sciences, 1430, Ås, Norway.
** Corresponding author.
E-mail addresses: [email protected] (A. Mojiri), [email protected] (J.L. Zhou).
https://doi.org/10.1016/j.chemosphere.2021.132580
Received 17 August 2021; Received in revised form 4 October 2021; Accepted 13 October 2021
Available online 20 October 2021
0045-6535/© 2021 Elsevier Ltd. All rights reserved.
A. Mojiri et al. Chemosphere 288 (2022) 132580
producing reactive oxygen species (ROS), and affecting expression of some genes in chlorophyll (rbcL, psbA, psaB
and psbc).
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A. Mojiri et al. Chemosphere 288 (2022) 132580
naproxen and ketoprofen are the most consumed NSAIDs (He et al., et al., 2020). The most reported hormones are listed as: testosterone,
2018). The exposure to NSAIDs causes severe toxicity in aquatic envi estrone, progesterone, 17β-estradiol, and 17α-ethynylestradiol (Wee
ronments even at ng/L or μg/L concentrations (Thalla and Vannarath, et al., 2020). Disruption of the endocrine system can lead to various
2020). One of the most widely used analgesic and antipyretic agents is developmental, neurological, reproductive, immune and metabolic
paracetamol (Shakeel et al., 2013). Paracetamol contains a benzene disorders (Ingre-Khans et al., 2017).
substituted by a hydroxyl group and the nitrogen atom of an amide
group at the (1,4) para positions (Żur et al., 2018), which can only be 2.2. Personal care products
degraded by hydroxylation and cleavage of the aromatic ring. Hence,
traces of paracetamol can remain untreated in sewage water of various Personal care products are various chemicals applied in soaps, lo
concentrations (Al-Kaf et al., 2017). tions, fragrances, toothpaste, shampoos and sunscreens (Brausch and
Rand, 2011). Liu et al. (2013) reported that the sunscreen UV filters (e.g.
2.1.3. Cardiovascular agents (Blood lipid regulator (BLR) or antilipemic 2-ethyl-hexyl-4-trimethoxycinnamate (EHMC), 4-methyl-benzilidine-
agents, blood pressure, and β-blockers) camphor (4MBC)), antimicrobial agents (e.g. triclosan, triclocarban),
Cardiovascular disorders are the second most common cause of insect repellants (e.g. N,N-diethyl-m-toluamide (DEET)), synthetic
deaths around the world. Thus, consumption of cardiovascular drugs is musks (e.g. nitro musks such as musk xylene, musk ketone, musk mos
significantly high. The presence of cardiovascular compounds in aquatic kene, musk ambrette and musk tibetene) polycyclic musks (such as
environments can have a long-term impact even at trace concentrations galaxolide and toxalide)], and preservatives (e.g. parabens) are the most
(Giebułtowicz et al., 2016). widely used personal care products. The US, China and Japan are the top
Blood lipid regulators (BLRs) are highly consumed as a medicine not countries in the consumption of personal care products (Liu et al., 2013).
only for the treatment of unhealthy cholesterol levels but also for car Eriksson et al. (2003) stated that personal care products are one of the
diovascular diseases and postmenopausal complications (Peña-Méndez most frequently detected compounds in water bodies in the world.
et al., 2020). Among the prescribed medications around the world, the Peck (2006) stated that sunscreen agents (UV filters) are broadly
cardiovascular drugs and lipid regulating agents are two of the most added to lotions and cosmetics as protection against harmful UV radi
consumed drugs. For instance, 24.5% of the most commonly prescribed ation. The hydrophobicity of these compounds (log Kow 5–8) reveals the
drugs in the United States are classified as cardiovascular drugs and lipid potential for bioaccumulation.
regulating agents (Zhang et al., 2020a, 2020b). Most used BLRs are Triclocarban and triclosan are the most commonly reported antimi
fenofibrate, bezafibrate, gemfibrozil and clofibrate, which are crobial agents, which have been added in many personal care products
commonly reported in aquatic environments (Rosal et al., 2010). These (such as hand disinfecting soaps, medical disinfectants, body wash
are considered as the resistant drug to biodegradation with a strong products, kitchen detergents and toothpastes) (Tsai et al., 2008). Both
persistence in the environment (Mourid et al., 2020). In Ontario (Can have the hydrophobic nature, and are persistent in the environment
ada), Patel et al. (2019) reported the high concentration (ng/L) of blood whether aerobic or anaerobic (Zhao et al., 2010).
pressure drugs (7,333,600 of metoprolol, 116,000 of diltiazem, 1,200, For a long time, DEET, a lipophilic organic compound, has been
000 of furosemide, and 22,900 of amlodipine) in water bodies, which applied as an insect repellent, and can be frequently found in aquatic
has been resulted by discharges of five manufacturing facilities. Apart environments (Sun et al., 2016). DEET is mobile and persistent. In the
from that, β-blocker drugs stand as the third most common pharma central east coast of Australia, DEET was reported in 97% of
ceuticals recorded in the aquatic environment (Rezka and Balcerzak, surface-water samples collected from waterways (Costanzo et al., 2007).
2015). Rezka and Balcerzak (2015) stated that atenolol, metoprolol, Synthetic musk fragrances are widely added to several personal care
nadolol, propranolol, sotalol, and timolol are the most common products, such as shampoo, deodorant and detergents for scent
β-blockers detected in aquatic environments. enhancement (Peck, 2006). As mentioned above, two types of synthetic
musk fragrances are nitro musk fragrances and polycyclic musk fra
2.1.4. Central nervous system (CNS) drugs, and antipsychotic and grances. The nitro substituents can be reduced to the amino metabolites
antidepressant of these compounds (Peck, 2006).
Caffeine and diazepam are the most consumed CNS agents. Due to Parabens are also employed as preservatives in products such as food
broad application of caffeine (presence in coffee, sodas, tea and choco and pharmaceutics. This group comprises propylparaben, methylpar
lates as well as in medicaments and appetite modulators), caffeine has aben, butylparaben, ethyl paraben, and benzyl paraben (Peck, 2006).
been reported in different water bodies around the world (Zarrelli et al.,
2014). That is considered as a stable compound under different envi 3. Presence of PPCPs in water bodies
ronmental conditions. Because of small pKa (0.7), high water solubility
(21.7 g/L), low octanol/water partition coefficient (− 0.07), along with Several studies have reported that up to six million PPCPs are
insignificant volatility and molecular mass of 194.19 g, caffeine is commercially available, and their consumption is increasing by 3–4% by
considered as highly persistent in aquatic environments (Mizukawa weight per year (Delgado et al., 2020). PPCPs reach the environment as
et al., 2019). The presence of caffeine in water sources reveals that this components of animal/human wastes, after incomplete absorption and
compound is not completely eliminated from sewage treatment plants. excretion from the body, as well as emissions of medical, agricultural,
Benzodiazepines (BDZ) is a group of psychiatric substances which affect industrial or household wastes (Taylor and Senac, 2014). Environmental
the central nervous system, having anxiolytic, sedative and hypnotic pollution with PPCPs has become a major public concern since these
impacts. Diazepam, alprazolam, oxazepam and lorazepam are the most compounds have been approved to have negative effects on aquatic
important agents in this group (Calisto et al., 2011). organisms (Zhang et al., 2021a, 2021b, 2021c), as well as having a role
in increasing antibiotic-resistant bacteria (Oliveira et al., 2015). Bu et al.
2.1.5. Endocrinology treatment (ET) drugs (2013) expressed that several PPCPs are persistent or pseudo-persistent
Drugs consumed in endocrine therapy can be remarked as endocrine in the environment and hazardous to non-target organisms. PPCPs may
disruptors and therefore require consideration because of their specific arrive water sources through direct release by wastes from hospitals,
hormonal or anti-hormonal properties (Besse et al., 2012). Research industries and households. (Molina et al., 2020). For emphasis, several
demonstrated that hormones are environmentally stable and potentially studies (Xu et al., 2019; Liu et al., 2021) have revealed that the presence
deleterious even at very low concentrations (Olatunji et al., 2017). For of PPCPs in aquatic environments has mostly derived from anthropo
instance, 17α-ethynylestradiol has the potential to trigger numerous genic activities such as the treatment and discharge of different kinds of
endocrine dysfunctions impacts at exposure levels as low as 1 ng/L (Wee wastewater, aquaculture, livestock breeding, and landfill.
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Table 2
Analytical techniques for PPCPs analysis in aqueous solutions.
PPCPs Technique Detector Remarks LOD or LOQa References
(ng/mL, ng/
g)
14PPCPs Liquid chromatography-mass spectrometry NRb Water (A) and methanol (B) were used as 10 (LOQ) Mousel et al. (2021)
(LC/MS) the mobile phase. 1 to 10
(LOD)
Liquid chromatography–mass spectrometry NR The mobile phase was formic acid in water <1 (LOQ) Ensano et al. (2019)
(LC–MS/MS) (A) and acetonitrile–water (B).
8PPCPs Mass spectrometer (MS) NR Acetonitrile (A) and ammonium formate NR Alenzi et al. (2021)
(B) were used as the mobile phase.
5PPCPs Gas chromatography–mass spectrometry Single NR <1(103) Zupanc et al. (2013)
(GC–MS) quadrupole (LOD)
mass
Carbamazepine High-performance liquid chromatography Ultraviolet Acetonitrile (A), and water/formic acid (B) NR Masjoudi et al. (2021)
(CBZ) (HPLC) were used as the mobile phase.
Diclofenac CBZ and DCF were detected at 285 nm and
(DCF) 380 nm, respectively.
Triclosan High-performance liquid chromatography SPD-20A UV-V The mobile phase was HPLC-grade 50(103) Li et al. (2021)
Bisphenol A (HPLC) acetonitrile with a mass fraction of 60% in (LOD)
DEET HPLC grade methane.
PPCPs were detected at 280 nm.
Diclofenac High-performance liquid chromatography UV–Vis Acetonitrile and water were selected as NR Karthik and Philip (2021)
Carbamazepine (HPLC) mobile phase.
PPCPs were detected at 220 nm.
10PPCPs High-performance liquid chromatography photodiode The mobile phase was acetonitrile and 0.02(106) to Zhang et al. (2021)
(HPLC) array (PDA) phosphoric acid. 0.05(106)
(LOD)
5PPCPs Ultrahigh performance liquid NR The mobile phase was formic acid/ NR Schübl et al. (2021)
chromatography coupled with mass- ammonium formate and methanol
spectrometry (UHPLC/MS)
8PPCPs UV-1800 UV-VIS Spectrophotometer – NR – Pashazadeh-Panahi and
Hasanzadeh (2020)
Levofloxacin HP 8453 UV–Visible Spectrophotometer – At 298 nm – Kassab et al. (2010)
a
Limit of Qualification (LOQ) and Limit of Detection (LOD).
b
Not Reported (NR).
water and wastewater can consume lower energy in comparison with Craggs, 2011). The resource recovery of algal biomass and water as
several wastewater treatment approaches. For instance, Yadav et al. effluent treated to a high standard are other advantages of HRAPs over
(2021) reported that microalgae use 0.2 kW-h/m3, while conventional WSPs (Sutherland et al., 2014). HRAPs are shallow (0.2–0.5 m),
treatment methods could consume up to 2 kW-h/m3. Craggs et al. (2013) continuous raceways around which wastewater is gradually mixed by a
expressed 50% energy reduction during treatment of water by using paddlewheel (Mehrabadi et al., 2015). The photosynthesis of algae in
microalgae compared with conventional treatment methods. Algae HRAPs causes dissolved oxygen supersaturation (up to 20 g/L), which
include both macroalgae and microalgae, and microalgae are usually enhances bacterial oxidation of biodegradable dissolved and particulate
better in growth rate and high lipid content than macroalgae (Elrayies, organic matter (Craggs et al., 2012). Hom-Diaz et al. (2017) employed
2018). Main algae-based systems, including stirred-tank photo the HRAPs for the removal of ciprofloxacin. The outdoor batch assays
bioreactors (STPs), high rate algal ponds (HRAPs), rotating algal biofilm showed 40.8% of ciprofloxacin removal at initial concentration (Ci) of
reactors (RABRs), and membrane photobioreactor (MPBRs) have been ciprofloxacin 2.25 mg/L, during day time. However, the indoor light
reported to treat water and wastewater, and remove emerging con batch assays indicated 83.7% of ciprofloxacin removal at Ci of cipro
taminants (Zimmo et al., 2003, Craggs et al., 2014; Mohammed et al., floxacin 1.11 mg/L. de Godos et al. (2012) removed up to 69% of
2014; Fica and Sims, 2016, Praween et al., 2016). tetracycline (Ci = 2 mg/L) by HRAPs. Lindberg et al. (2021) investigated
STPs have a simple design and are conventional reactors, and usually the HRAPs (including Nordic microalgal strains) for removal of 14 active
include a glass tank continuously stirred by impellers or baffles (Ismail pharmaceutical ingredients (APIs). 69% of APIs were removed during 6
et al., 2017). At the bottom of reactor, CO2-enriched air is bubbled to days. By using the HRAP, Matamoros et al. (2014) removed less than
supply a carbon source for algae growth (Mohan et al., 2014). STPs are 30% of carbamazepine and 2,4-D, 40–60% of diclofenac and celestolide,
suitable for shear sensitive microalgae cultivation (Verma et al., 2018). 60–90% of ketoprofen, galaxolide and tonalide, and more than 90% of
Main disadvantage of STPs is the low surface-area-to-volume ratio, caffeine, acetaminophen and ibuprofen.
which in turn decreases light-harvesting effectiveness (Mohan et al., RABRs provide a very good condition for algal biomass production
2014). Ismail et al. (2017) removed 95% of p-aminophenol (an inter (Hoh et al., 2016). In the RABR, a vertically material for the attachment
mediate for the manufacture of paracetamol and acetanilide) and COD of algae rotates through the water or wastewater for absorbing nutrients,
by a stirred-tank photobioreactor using microalgal-bacterial consortium then rotates out of the water to accelerate CO2/O2 exchanges and light
(Chlorella sp. was the main microalgal strain) with hydraulic retention exposure (Zhao et al., 2018). RABRs have several advantages such as
time (HRT) of 4 days. Mojiri et al. (2021a) removed 35.4% of carba simple installation, improving growth of biomass, a good gas exchange
mazepine, 33.1% of sulfamethazine and 36.5% of tramadol with a STP mechanism, and a high nutrient removal efficiency (Woolsey, 2011).
containing Chaetoceros muelleri. The maximum biomass production rate in a pilot-scale RABR reached
In comparison with conventional wastewater stabilization ponds 19 g m− 2 d− 1 (Wang et al., 2018). Hassard et al. (2015) reported a
(WSPs), HRAPs offer an enhanced wastewater treatment by overcoming removal efficiency of 52%–95% for ciprofloxacin, tetracycline and
several drawbacks of WSPs (such as limited nutrient and pathogen trimethoprim during running a modified RBAR. Chen et al. (2021)
removal, and poor and highly variable effluent quality) (Park and removed 70–100% of five PPCPs (oxybenzone, ibuprofen, bisphenol A,
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Table 3
Reported PPCPs in fishes.
PPCPs Concentrations (ng/g) Fish species Remarks References
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Table 3 (continued )
PPCPs Concentrations (ng/g) Fish species Remarks References
Citalopram 51 ± 25
Diazepam 28 ± 9
Venlafaxine 18 ± 12
Hydrochlorothiazide 5±8
Levamisole 11 ± 11
Salbutamol 22 ± 17
Citalopram 41 ± 47 Brown trout Grabicova et al. (2017)
Clomipramine 1.7 ± 1.3
Haloperidol 4.2 ± 3.5
Hydroxyzine 0.27 ± 0.10
Levomepromazine 3.1 ± 2.2
Mianserin 2.0 ± 1.4
Mirtazapine 41 ± 30
Paroxetine 1.6 ± 1.5
Sertraline 44 ± 30
Tramadol 6.0 ± 6.3
Venlafaxine 3.8 ± 3.7
Carazolol 1.0 ± 1.0 Golden grey mullet Muscle Moreno-González et al. (2016)
Carbamazepine 1.2 ± 2.2
Diazepam 0.3 ± 0.3
Nadolol 0.3 ± 0.4
Atenolol 24.4(103) P. lineatus Liver Rojo et al. (2020)
Carbamazepine 5.5(103)
Enalapril 7.0(103)
Sildenafil 17.1(103)
Clopidogrel <0.65 NR Liver Boulard et al. (2020)
Diclofenac 47 ± 7
Diphenhydramine 5.8 ± 0.4
Flecainide 18 ± 1
Lidocaine 3.4 ± 0.3
Norlidocaine 10 ± 3
Tramadol 15 ± 2
Diclofenac 8.8 Barbus graellsii Homogenate Huerta et al. (2013)
Citalopram 0.8 Cyprinus carpio Homogenate
Carbamazepine 17.9 Salmo trutta Liver
Venlafaxine 0.6 Cyprinus carpio Homogenate
Carazolol 3.8 Silurus glanis Homogenate
Salbutamol 2.6 Silurus glanis Homogenate
Carbamazepine 1731 ± 348 Jenynsia multidentata Gill Valdés et al. (2016)
Fluoxetine 36.6–259 Oncorhynchus mykiss Muscle Togunde et al. (2012)
Sertraline 7.5–160.8
Carbamazepine 0.6–1.7
Ibuprofen <0.84
Gemfibrozil <0.40
a
Not reported (NR).
triclosan, and N, N-diethyl-3-methylbenzamide-DEET), which the water samples by algae are the biodegradation, biosorption, photo
elimination of PPCPs was mostly attributed to the degradation by the degradation and volatilization. Matamoros et al. (2015) expressed that
algae. although the ability of algae-based wastewater treatment systems to
MPBRs with a high potential in removal of nutrients from waste eliminate nutrients and heavy metals has been studied well, the removal
water, have been considered as a system that couples the culture of of PPCPs with the algae still needs more studies. Researchers (Mata
microalgae with a continuous biomass separation using a membrane moros et al., 2015; Gruchlik et al., 2018) stated that biodegradation and
filtration system (Novoa et al., 2020). MPBRs enable the system to photodegradation are the main removal processes during the elimina
operate with a short HRT without the washout of microalgae (Honda tion of PPCPs by algae-based systems. In reality, most PPCPs can be
et al., 2017). Application of MPBR in large-scale is limited, which can be eliminated by more than one pathway (R. Liu et al., 2021).
considered as the main drawback of MPBRs, because of membrane
fouling and consequent permeate flux reduction (Novoa et al., 2020).
Thus, the application of MPBRs for the removal of emerging contami 4.1. Biodegradation
nants has not been widely reported. 84.3% of an emerging contaminant
(atrazine) was removed by a microalgal-bacterial MPBR under a hy Biodegradation is one of the main elimination mechanisms of PPCPs
draulic retention time of 12 h and initial pollutant concentration of 0.01 from aqueous solutions by algae-based systems (Hultberg and Bodi,
mg/L (Derakhshan et al., 2019). 2018). Microbial biodegradation comprises varied and complementary
In general, several studies (Matamoros and Rodríguez, 2016) mechanisms, from adsorption of contaminants onto biomass, to miner
expressed that algae-based treatment methods can increase the removal alization where final degradation products are inorganics (e.g., CO2 and
of emerging contaminants from aquatic environments. For instance, H2O) and biomass (Garcia-Becerra and Ortiz, 2018). Papazi et al. (2017)
28% of levofloxacin was eliminated by Chlorella vulgaris (Xiong et al., stated that several factors (such as concentration of organic pollutants,
2017), while 50–64% of clarithromycin was eliminated by Chlamydo temperature, pH, oxygen content, and light intensity) can affect the
monas sp. (Escudero et al., 2020). The removal efficiencies of PPCPs with biodegradation. For instance, Papazi et al. (2017) stated that algal cells
different algae and microalgae species are shown in Table 4. Liu et al. apply more energy for biodegradation at the highest concentrations of
(2021) stated that four main pathways (Fig. 1) to remove PPCPs from organic pollutants in comparison with the energy applied for lower
concentrations. Furthermore, Hong et al. (2008) expressed that when
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A. Mojiri et al. Chemosphere 288 (2022) 132580
two or more organic pollutants are present in influent, there will be the procedure contains four phases: (I) mass transfer of the sorbate from the
competition for biodegradation of different compounds. Additionally, bulk liquid to the hydrodynamic boundary layer around the biosorbent
Al-Dahhan et al. (2018) stated that both biodegradation rate and growth particles;
rate of microalgae can be enhanced with increasing light intensities and (II) film diffusion through the boundary layer to the external surface
adding inorganic carbon sources (such as sodium bicarbonate and CO2). of the biosorbent; (III) intraparticle diffusion toward the interior of the
The main mechanisms of biodegradation can be categorized as biosorbent particle; and (IV) energetic interaction between the sorbate
metabolic degradation that PPCPs serve as the carbon sources or elec molecules and the sorption sites.
tron donors/acceptors for algae; and co-metabolism that additional The biosorption process is usually modeled by the equilibrium dis
organic substrates serve to both sustain biomass production, and act as tribution via Eq. (6) (Aravindhan et al., 2009).
an electron donor for the non-growth substrate (Xiong, 2021). Hena
V
(2021) expressed that biodegradation depends on the cellular meta qe = (C0 − Ce ) (6)
W
bolism of microalgae that involves a series of complex enzymatic acts.
Biodegradation quality rate of organic pollutants with algae can be where initial and equilibrium concentrations of pollutants in water are
calculated based on Eq. (5) (Zhang et al., 2011). In the equation, to defined by C0 and Ce, equilibrium concentration (mg/g) of pollutant in
exclude non-biodegradation, a blank is set with only a culture medium biosorbent is shown by qe, and volume of the solution (L) and the mass of
without algae. algae use (g) are shown by V and M, respectively.
[ ( ) ] Bioaccumulation is described as the intracellular accumulation of
Iq − Mq + Cq + Nq
DR = × 100 (5) sorbate (Chojnacka, 2010). Although bioadsorption is the first step of
Iq
bioaccumulation, not all contaminants adsorbed onto the surface of
microalgae can reach into the cell (bioaccumulation) (Xiong et al.,
where DR (%) indicates the biodegradation quality rate, the initial
2021). The bioaccumulation potential of a chemical in aquatic organ
concentration of pollutant is shown by Iq, the cellular residual amount of
isms plays an important role in the evaluation of environmental hazards.
pollutant is shown by Cq, Mq defines the medium residual quantity of
A high bioaccumulation potential of a chemical in biota indicates the
contaminant, and the non-biodegradation amount of contaminant is
possibility of toxic impact being encountered in aquatic organisms
shown by Mq.
(Geyer et al., 2001).
Algae include enzymes that metabolize a range of xenobiotics in
Xiong et al. (2021) stated three main pathways for transporting
three phases (Wang et al., 2017):
PPCPs (such as antibiotics) through the algae cell membrane into the cell
Phase-I contains oxidation, reduction, or hydrolysis that converts
interiors: (I) PPCPs with low molecular weights and high lipid solubility
lipophilic xenobiotics into more hydrophilic compounds to facilitate
can diffuse through the cell membrane from a region of high (external)
their excretion. Cytochrome P450s are microsomal heme-thiolate pro
to low (internal) concentration through passive diffusion. (II)
teins anchored in the membrane, and usually catalyze the primary step
Passive-facilitated diffusion transfer PPCPs across the cell membrane
of detoxification.
with transporter proteins. (III) Energy-dependent/active uptake, which
Phase-II is characterized by the addition of hydrophilic moieties to
is an active transport process using energy.
accelerate excretion. Xenobiotics with –COOH, –OH or –NH2 and me
(Li et al. (2009)) removed BPA with S. hantzschii, and reported that
tabolites from phase-I might be conjugated with glutathione/glucuronic
higher amounts of BPA could accumulate in cells while increasing the
acid catalyzed by glutathione S-transferases/glucosyltransferases.
initial concentration of BPA. After eight days, the accumulation of BPA
Phase-III comprises compartmentation of xenobiotics in vacuoles or
was 11.53, 35.30 and 45.44 ng BPA/mg fw (fresh weight) at initial
cell walls. The capability of algae to detoxicate xenobiotics is similar to
concentrations of 5.0, 7.0 and 9.0 mg/L BPA, respectively. Wang et al.
the mammalian liver and therefore algae are remarked as “green livers”
(2019a, 2019b) stated that with increasing time, the intracellular ab
for the detoxification of pollutants. 54% and 65% removal of malathion
sorption is greater than the extracellular adsorption during removal of
by S. platensis and A. oryzae were attributed to biodegradation (Mustafa
nonylphenol by marine algae.
et al., 2021).
Biosorption, and bioaccumulation and biodegradation (Fig. 2) are The photodegradation is a transformation process in which complex
the interactions and concentration of organic contaminants in the molecules are decomposed, and is categorized into indirect and direct
biomass, either living (bioaccumulation) or non-living (biosorption) photodegradation (Jiménez-Bambague et al., 2020). If the PPCPs can
(Chojnacka, 2010). This could be divided into three stages: 1) a physi absorb light under the deployed irradiation condition, they would have
cochemical reaction between the cell surface and contaminants, 2) a a potential to undergo direct photolysis. However, if the PPCPs could not
fairly slow transfer of molecules over the cell membrane, and 3) bio absorb the light, then indirect photodegradation possibly occurs in the
accumulation and biodegradation (Xiong et al., 2021). presence of photosensitizers (Liu et al., 2021). Yang et al. (2018) stated
The biosorption of contaminants is a complex procedure containing that algae, with excretion biopolymers such as polysaccharides and
integration of some active and passive mechanisms. These mechanisms proteins, can enhance the photodegradation of PPCPs. Additionally,
vary based on the type of biomass, and culture conditions (Muñoz et al., Tian et al. (2019) expressed that chlorophyll can enhance the photo
2006). Moreover, algae biosorption processes have generally been degradation of emerging contaminants (such as chlortetracycline). Wei
attributed to the structure of cell wall comprising functional groups et al. (2021) stated that chlorophyll in the intracellular organic matters
(such as amino, carboxyl, hydroxyl and sulphate) that can have a role as may play a role as photosensitizers since substituted porphyrin ring is
binding sites for pollutants via electrostatic attraction, ion exchange and one of the important components of chlorophyll that has a vital role in
complexation (Tuzen et al., 2009). For instance, hydrogen bonds were absorbing energy from light sources. Norvil et al. (2016) expressed that
reported as the key mechanism for the elimination of sulfamethoxazole these biopolymers can increase the photodegradation in several mech
and sulfacetamide by marine algae (Navarro et al., 2014). Aravindhan anisms, containing redox cycling, catabolic process, production of hy
et al. (2009) expressed that hydrophobic and donor acceptor in droxyl radicals, and inhibiting photo-oxidation by competitive reaction
teractions have been remarked as important processes in biosorption of with radicals (Sutherland and Ralph, 2019). Overall, algae can facilitate
organic compounds. photodegradation by enhancing the free radical yield (Eqs. (7) and (8);
Silva et al. (2019) stated that the progress of the biosorption Wang et al., 2017). Usually, photodegradation can be calculated by Eq.
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A. Mojiri et al. Chemosphere 288 (2022) 132580
Table 4
Algae and microalgae-based systems to remove PPCPs.
PPCPs removal (% or ng/L) Alga/Microalgae Species Remarks/Removal mechanisms Water sources References
Algae
Alfuzosin 64 (%) Tetradesmus dimorphus and After 7 days, samples were collected from Municipal wastewater Gentili and Fick (2017)
Alprazolam − 49 (%) (green algae) photobioreactor to monito removal
Atenolol 99 (%) efficiencies. Retention time was around 7
Atracurium 97 (%) days. Removal mechanism was
Azelastine 27 (%) biodegradation and photolysis
Biperiden − 490 (%)
Bisoprolol 97 (%)
Bupropion 93 (%)
Carbamazepin − 14 (%)
Cilazapril 61 (%)
Ciprofloxacin 11 (%)
Citalopram 98 (%)
Clarithromycine 90 (%)
Clemastine 40 (%)
Clindamycine 45 (%)
Clonazepam 88 (%)
Clotrimazol 19 (%)
Codeine − 11 (%)
Cyproheptadine − 450 (%)
Desloratidin − 45 (%)
Dicycloverin 71 (%)
Diltiazem 94 (%)
Diphenhydramin 89 (%)
Eprosartan 80 (%)
Fexofenadine − 5.2 (%)
Flecainide 58 (%)
Fluconazole − 17 (%)
Flupetixol − 75 (%)
Haloperidol − 5000 (%)
Hydroxyzine 87 (%)
Ibersartan 6.4 (%)
Loperamide 41 (%)
Memantin 81 (%)
Metoprolol 99 (%)
Miconazole 65 (%)
Mirtazapine − 630 (%)
Nefazodon − 3.8 (%)
Orphenadrin − 13 (%)
Oxazepam 80 (%)
Pizotifen 75 (%)
Ranitidine 75 (%)
Risperidone − 3.2 (%)
Roxithromycine 44 (%)
Sertraline 17 (%)
Sotalol 43 (%)
Bisphenol A 82 (%) Chlorella fusca var (green At the light intensity of 2 W/m2. Removal Aqueous solution Hirooka et al. (2005)
algae) mechanism was biodegradation.
Trimethoprim <10 (%) Nannochloris sp. (green algae) After 14 days, samples were collected to Fresh water (from lake) Bai and Acharya (2017)
Carbamazepine <10 (%) monitor removal efficiencies. Main
Ciprofloxacin <40 (%) degradation mechanism was photolysis for
Sulfamethoxazole >99 (%) ciprofloxacin, and it was photolysis and
Triclosan >99 (%) bioaccumulation for triclosan. For removal of
trimethoprim, the main pathway was
biodegradation, photolysis.
The green alga Nannochloris sp. was cultured
before experiments were conducted.
Salicylic acid >93 (%) Chlorella sorokiniana Photobioreactors was used and sampling was Aqueous solution Santos et al. (2017)
Paracetamol >67 (%) Scenedesmus obliquus done 8–10 days. Removal mechanism was
Salicylic acid >73 (%) Chlorella vulgaris (Green photolysis.
Paracetamol >40 (%) microalgae)
Salicylic acid >22 (%)
Paracetamol >21 (%)
Carbamazepine <21 (%) Scenedesmus obliquus and Experiments were carried out under 90–160 Domestic wastewater Larsen et al. (2019)
Ibuprofen 60 (%) Chlorella vulgaris photon m− 2 s− 1 of light in a 16 h on/8 h off (effluent)
Gemfibrozil <27 (%) cycle. The removal mechanism for Ibuprofen
Triclosan 56-88 (%) and triclosan was biodegradation, and
biodegradation and photodegradation,
respectively.
Diclofenac 71 (%) Coelastrum sp. (dominant High rate algae pond was used. Main Urban wastewater Villar-Navarro et al.
species by more than 90%) degradation mechanism was photolysis. (2018)
Asprin 97 (%) Carbonaceous material Biosorption was the main removal Aqueous solution Ouasfi et al. (2019)
produced from bifurcaria mechanisms. Maximum adsorption capacity
was 2633.04 mg/g.
(continued on next page)
13
A. Mojiri et al. Chemosphere 288 (2022) 132580
Table 4 (continued )
PPCPs removal (% or ng/L) Alga/Microalgae Species Remarks/Removal mechanisms Water sources References
14
A. Mojiri et al. Chemosphere 288 (2022) 132580
Table 4 (continued )
PPCPs removal (% or ng/L) Alga/Microalgae Species Remarks/Removal mechanisms Water sources References
Aspirin 95 (%) Activated porous carbon Maximum adsorption capacity was 970.8 mg/
Ketoprofen 92 (%) material derived from g and 443.4 mg/g for removal of aspirin and
Laminaria digitate (brown ketoprofen, respectively. Biosorption was the
algae) main removal mechanisms.
Tramadol 91 (%) Scenedesmus obliquus (green Maximum adsorption capacity was 42 mg/g. Aqueous solution Ali et al. (2018)
algae)
Algae and microalgae in an integrated system
Ibuprofen 94% Integrated Algal-bacteria in a It was an anaerobic-anoxic-aerobic Urban wastewater López-Serna et al. (2019)
Naproxen 52% photobioreactor. photobioreactor.
Salicylic acid 98% Main Chlorella vulgaris was the dominant
Triclosan 100% microalgae species in the system during step
Propylparaben 100% 1, and Pseudonabaena acicularis and
Scenedesmus acutus were dominant during
second step.
Biodegradation and sorption were the main
removal mechanism.
Metoprolol >78 (%) Algae and constructed Iris pseudacorus, Scirpus sp. and Carex sp., Municipal wastewater Rühmland et al. (2015)
Carbamazepine wetland (CW) Lemna as plant and sand as the media were
Iopromide placed in the CW. And floating algae was in
the CW.
Photodegradation and biodegradation were
the main removal of PPCPs by algae.
Carbamazepine 68.9% Integrated microalgae and Chaetoceros muelleri (marine microalgae) was Synthetic wastewater Mojiri et al. (2021b)
Sulfamethazine 64.8% biochar attached on biochar
Tramadol 69.3%
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A. Mojiri et al. Chemosphere 288 (2022) 132580
Fig. 2. Bioaccumulation and biosorption of PPCPs in algae. (*ESP (extracellular polymeric substance); **Source: Xiong et al., 2021, the permission for re-using the
figure received on August 17, 2021 from Elsevier).
cephalosporins photodegradation, and removal efficiency of >90% for reactive oxygen species (Xiong et al., 2019). Yang et al. (2009) expressed
photodegradation of triclosan, metronidazole, chlortetracycline, para that some antibiotic and antibacterial agents can inhibit the growth of
cetamol and anilines. The photodegradation products can be either less algae even at environmentally relevant concentrations (μg/L). For
or more toxic than the parent compounds; for instance, photo instance, 17.5 μg/L of triclocarban decreased the growth rate of 50% of
degradation products from carbamazepine are more toxic (Patel et al., algae (Yang et al., 2009). Sulfamethazine and sulfamethoxazole reduced
2019). Apart from that, Jiménez-Bambague et al. (2020) stated that the growth rate of S. obliquus in concentrations of less than 0.05 mg/L
recalcitrant and highly hydrophilic PPCPs (such as carbamazepine) are (Xiong et al., 2019).
very stable and resistant to biodegradation and photodegradation. Concentration of chlorophyll is a rational assessment for the activity
The physicochemical properties of the PPCPs, the intensity and of algae in aquatic environments (Tretiach et al., 2007). Additionally,
wavelength of light, the physicochemical properties of the water and the protein content of algae is a vital factor for algae, especially for using as
algae species can affect the phytodegradation (Sutherland and Ralph, feed (Chia et al., 2019). Several studies (Xin et al., 2017; Mojiri et al.,
2019). For instance, Norvill et al. (2016) expressed that the photo 2021a, 2021b) confirmed that low concentrations of PPCPs in a short
degradation of PPCPs by algae-based systems is increased in the pres time can increase the concentration of chlorophyll and carotenoid, and
ence of Fe3+ in water because of photosensitive organic molecules. protein because of two main reasons (Mojiri et al., 2021a): an increase in
Complex of carboxylic acids with iron further increases the hydroxyl chlorophyll and protein content can support algae to decrease the
radical production by photosensitive Fe3+. Apart from that, Bai and accumulated reactive oxygen species in chloroplasts; low concentration
Acharya (2019) reported that the presence of nitrate in the waterway of PPCP causes inductive impact of pharmaceutically active compounds
could enhance the indirect photolysis of triclosan and hormone active on cells. Moreover, Chen et al. (2020b) expressed that increasing the
substances in an algae-based system. Moreover, the presence of oxygen content of protein during exposed to low concentrations of PPCPs can be
can affect the photodegradation. For instance, the presence of oxygen justified by an increase in enzymes synthesis or other energy-producing
increased the photodecarboxylation of naproxen (Boscá et al., 2001). fractions.
High concentrations of PPCPs can reduce the content of chlorophyll
5. Effects of PPCPs concentrations on algae and protein. For instance, more than 50% of protein content and chlo
rophyll of microalgae was reduced by exposure to 50 mg/L of antibiotics
Several studies showed that PPCPs can affect the algae health (Mojiri (Mojiri et al., 2021b). High concentrations of PPCPs may inhibit the
et al., 2021a). In terms of studying the effects of PPCPs on algae, protein synthesis by binding to the 50S subunit of the ribosome. More
important factors which should be considered are growth rate, chloro over, oxidative damage resulted by PPCPs exposure may cause DNA
phyll and carotenoid, and protein content (Mojiri et al., 2021b). damage (Li et al., 2020). Reducing the chlorophyll content can be
Xiong et al. (2020) expressed that low concentration (<2 mg/L) of explained with the reactive oxygen species (ROS)-mediated damage to
PPCPs does not have any significant effects on growth of tolerant species the photosystem and chlorophyll biosynthesis. Chlorophyll in cells
of algae (such as Scenedesmus obliquus and Chlamydomonas). However, Li might be used as a protective way to reduce the ROS in chloroplasts
et al. (2020) reported that roxithromycin (in concentration of 0.25–2 (Mojiri et al., 2021b).
mg/L) had a significant effect on Chlorella pyrenoidosa. Additionally,
they found that the roxithromycin (in low concentrations <0.2 mg/L) 6. Effects of other abiotic factors on algae
did not have a significant effect on growth rate of Chlorella pyrenoidosa
during a short time (less than 14 days) exposure to roxithromycin, but it Several abiotic factors such as HRT, temperature, and light intensity
significantly decreased its growth rate after more than 14 days. In can affect the algae-based systems in terms of PPCPs removal (Miazek
general, several studies (Li et al., 2020; Mojiri et al., 2021a) reported et al., 2015, Fang et al., 2018). HRT, as a key operating parameter in
that low concentrations of PPCPs can improve the growth rate of algae treatment of wastewater, is the time taken for which raw wastewater
because they can be used by algae as a carbon source, and they increased stays in a reactor before its discharge as effluent; thus, it determines the
the chlorophyll content at the beginning. High concentrations of PPCPs quantity of organic matter and volatile solids to be fed into the digester
are toxic to algae and can decrease their growth rate because they can (Ogwueleka and Samson, 2020). Gao et al. (2016) stated that a long HRT
damage cell structures and organelles by disturbing the homeostasis of is generally needed for nutrients uptake by algae. Valigire et al. (2012)
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A. Mojiri et al. Chemosphere 288 (2022) 132580
reported that HRAPs are mostly operated at 2–8 days of HRTs, while • Algae-based systems could remove PPCPs from water bodies up to
longer HRTs have inhibited microalgal growth due to excess DO (Vali 99%.
gore et al., 2012). Kang and Kim (2021) stated that a short HRT com • In comparison with STPBs, RABRs and HRAPs algal bioreactors have
bined with a long solids retention time (SRT), have provided a greatest demonstrated the better performance in PPCPs removal.
productivity and settleability of algal–bacterial consortia. • Short term exposure to low concentration of PPCPs can increase
Other important factors are the light intensity and temperature. The chlorophyll and protein contents in algae, which are however
influence of light availability may affect the growth of microalgae as reduced by increasing PPCPs concentrations and exposure time.
well as production of oxygen through the photosynthesis of the micro
algae (Bazdar et al., 2018). Normally, an increase in light intensity Declaration of competing interest
promotes algal growth up to a photoinhibitory threshold; however, both
the strength of this impact and the threshold differ among species The authors declare that they have no known competing financial
(Nzayisenga et al., 2020). At full-scale outdoor conditions, current interests or personal relationships that could have appeared to influence
algae-based treatment systems suffer from low natural lighting for the work reported in this paper.
effective nutrient conversion due to the shortage of light during the
rainy days. In addition, excessive light at noontime inhibits photosyn Acknowledgments
thesis of algae (Yan et al., 2013). Xu et al. (2021) expressed that very low
and high temperatures can considerably decrease the algal growth rate, The authors would like to express their gratitude to the Norwegian
and negatively affect wastewater treatment using algae. In high tem University of Life Sciences (NMBU, Norway) for providing supports
perature serious inhibition occurs because of inactivation and denatur during writing this paper. Moreover, we really appreciate Dr. Per Ivar
ation of enzymes (Zhang et al., 2021a, 2021b, 2021c). Høvring for his advices.
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A. Mojiri et al. Chemosphere 288 (2022) 132580
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