Resources, Conservation & Recycling 129 (2018) 153–167

Contents lists available at ScienceDirect

Resources, Conservation & Recycling

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

Review

Citrus processing wastes: Environmental impacts, recent advances, and T

future perspectives in total valorization
⁎
Behzad Sataria, Keikhosro Karimia,b,
a
Department of Chemical Engineering, Isfahan University of Technology, Isfahan 84156-83111, Iran
b
Industrial Biotechnology Group, Research Institute for Biotechnology and Bioengineering, Isfahan University of Technology, Isfahan 84156-83111, Iran

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

Keywords: The recent advances and future perspectives in the complete valorization of citrus processing waste (CPW), a by-
Biofuel product of citrus processing industries, are presented in this review paper. First, the importance of valorization of
Green chemistry CPW to develop a bio-economy and to reduce its negative environmental impacts is assessed. A brief survey of
Integrated biorefinery applications of native/modified CPW for nanoparticle, bio-sorbent, and biofertilizer production is presented. As
Pectin
the core part of the valorization scheme and regarding the environmental aspects, the perspectives for the
Sustainable substance
application of CPW are via green extraction techniques, e.g., microwave- and ultrasound-assisted extractions,
and biochemical processes. Furthermore, green extraction and biochemical techniques result in processes’ in-
tensification toward integrated biorefinery models. The superiority of green extraction techniques over tradi-
tional techniques, challenges for implementation, and the valuable extracts obtained by these methods as well as
a summary of their analytical techniques are discussed. The challenges of bioconversion of CPW to biofuels and
fermentative products and strategies to overcome them are later presented. Finally, a literature review on using
the concept of green chemistry for the integrated biorefinery of CPW and its engineering challenges is presented
and a biorefinery scheme is proposed accordingly.

1. Introduction steps. After being harvested, citrus fruits are transported to production
plants. Afterwards, the fruits are graded in a preliminary step, and after
According to the Food and Agriculture Organization (FAO), a total removal of debris, they are stored to be ready for water-washing
of 636,544,883 and 1,106,133,866 tons of fruits and vegetables, re- cleaning, in the second step. At the third step, the fruits’ juice is ex-
spectively, was produced in 2012 (FAOSTAT-FAO statistical database, tracted via pressing and centrifugation; the juice is then heated to ac-
2015). Citrus fruits are the most consumed fruits in the world, because tivate pectic enzymes, and transferred to syrup tanks for concentration
of their nutritional values and health benefits, as a result of having and adding citric acid, enzymes, and vitamin C, to obtain the best
appreciable amounts of secondary metabolites (Lv et al., 2015). Brazil, quality. Finally, the juice is filled into packages, boiled to sterilize, and
China, India, Mexico, Spain, and the USA produce over two-thirds of the packs are labeled (see Fig. 1) (Ngoc and Schnitzer, 2009;
the world’s citrus fruits (Paggiola et al., 2016). The genus Citrus in- Taghizadeh-Alisaraei et al., 2017).
cludes several important fruits, with dominantly sweet orange, man- Approximately one-third of citrus fruits is utilized for processing,
darin, grapefruit, lime, and lemon (Mamma and Christakopoulos, 2014; which produces ca. 50–60% organic waste. CPW has a low pH level
Zheng et al., 2016). Over 61% of the world’s citrus fruit production is (3–4) and is characterized by having high organic matter (95% of total
the share of sweet orange. Sweet orange (or Citrus sinensis) varieties can solids) and high water content (around 80–90%). Table 1 summarizes
be classified into three groups: common oranges (also called white or the proximate composition of major citrus fruits’ byproducts produced
blonde oranges), navel oranges, and pigmented oranges or blood or- in citrus processing industries. This composition includes some fats, free
anges (Stinco et al., 2016). While the first group is mainly intended for sugars (e.g., glucose, fructose, and sucrose), organic acids, carbohydrate
use in juice production industries, the pulpy texture of the second group polymers (cellulose, hemicellulose, and pectin), enzymes (pectines-
and the reddish coloration of the third group make them favorable for terase, phosphatase, and peroxidase), flavonoids, essential oils (mainly
fresh consumption. limonene), and pigments (Boukroufa et al., 2015). The organic acids in
The citrus processing industries are usually involved in four main orange processing waste, i.e., citric, malic, malonic, and oxalic acids,

⁎
Corresponding author at: Department of Chemical Engineering, Isfahan University of Technology, Isfahan 84156-83111, Iran.
E-mail addresses: [email protected], [email protected] (K. Karimi).

http://dx.doi.org/10.1016/j.resconrec.2017.10.032
Received 16 September 2017; Received in revised form 24 October 2017; Accepted 25 October 2017
Available online 06 November 2017
0921-3449/ © 2017 Elsevier B.V. All rights reserved.
B. Satari, K. Karimi Resources, Conservation & Recycling 129 (2018) 153–167

Fig. 1. View of citrus fruit supply chain and the waste valorization.

Table 1
Proximate composition of some major citrus fruits’ by-products (% of dry basis).

Waste Ash Sugar Fat Protein Flavonoid Pectin Lignin Cellulose Hemicellulose Refs.

Lemon peels 2.52 6.52 1.51 7.00 12.54 13.00 7.56 23.06 8.09 Marín et al. (2007)
Sweet orange peels 2.56 9.57 4.00 9.06 4.50 23.02 7.52 37.08 11.04 Marín et al. (2007)
Citrus wastea 3.73 22.9b 3.78c 6.07 – 25.00 2.19 22.00 11.09 Pourbafrani et al. (2010)
Citrus wastea 4.75 33.09b – – – 15.30d 1.95 8.82 7.96e Satari et al. (2017)
Kinnow mandarin 3.23 31.58 – 5.78 – 22.6 0.56 10.10 4.28 Oberoi et al. (2011)

a
Mixture of orange and grapefruit peels, seeds, and leaf residues after juice extraction.
b
Sum of glucose, sucrose, and fructose.
c
Limonene.
d
Galacturonan.
e
Sum of arabinan, xylan, galactan, and mannan.

together compose approximately 1% of dry weight (Angel Siles Lopez 2. The importance of CPW valorization: environmental and
et al., 2010). In citruses, citric acid is the dominant organic acid and economic aspects
generally lemon juice has the highest acidity with over 48 g/L citric
acid (Karadeniz, 2004). The taste of juice is primarily affected by the The valorization of CPW has a great potential for transition toward a
sugars and organic acids, while volatile organic compounds are asso- bioeconomy. Besides, the negative impacts of citrus processing in-
ciated with its aroma. Noteworthy, when CPW is obtained from a juice dustries to the environment make the valorization schemes more im-
production factory, it also contains citrus seeds, which are character- portant. The importance is to mitigate the negative environmental ef-
ized by having high oil content, with dominantly C16 and C18 fatty acids fects via introducing green valorization schemes that lead to an
profile (Anwar et al., 2008). Regarding negative impacts of production integrated biorefinery platform.
of such a huge amount of CPW to the environment and also the con-
tribution of the CPW-derived products to the bioeconomy, the valor-
ization of CPW to food, feed, and fuels is a necessity. 2.1. Emergence of bioeconomy and the share of CPW
The aim of valorization of CPW in the present study is via three
main platforms (Fig. 1): direct use of native/modified CPW, biochem- The global population is exponentially expanding and consequently
ical processes, and green extraction techniques. The paper primarily the demands for human food and feeds are advancing. Industrialized
summarized the direct utilization of CPW for producing nanoporous nations are heavily dependent on crude oil and natural gas for their
materials, biosorbent for heavy metals (unmodified or chemically energy, chemicals, and materials demands. Nonetheless, the political
modified), and biofertilizer. The recent advances in the literature on the instability of some Middle East oil suppliers and also the recent fluc-
using green extraction techniques, i.e., microwave- and ultrasound-as- tuations of oil price make this dependency more challenging (Reboredo
sisted extraction, and biochemical processes for biofuels and fermen- et al., 2016). Besides, the petroleum supplies are limited resources and
tative products production were presented and critically analyzed. there have been always environmental concerns regarding their use.
Challenges of implementation of the green chemistry for CPW valor- Therefore, the ability to meet market demands yet minimize environ-
ization and in integrated biorefinery platforms were discussed. The mental collapse has been of great importance for the future of the
solutions for some of the problems and questions to be answered in the mankind’s life on earth. In this regard, different countries have passed
future for fully utilization of this waste were finally discussed. legislation to move towards bio-based economy for the future (Inghels
et al., 2016). The emerging “bioeconomy” is “a new concept coined by

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the European Commission in 2012 to address the possibilities of the during cleaning activities, meanwhile, it is usually characterized by
conversion of renewable biological resources into economically viable having high BOD and COD (Guzmán et al., 2015). However, the was-
products and bioenergy”, as suggested by Ravindran and Jaiswal tewater characterization for an orange juice facility revealed that it has
(2016b). In this economy, the basic building blocks for materials and considerable amounts of valuable compounds, e.g., fibers, phenolic
energies are derived from renewable biological resources, e.g., bio- compounds, sugars, and organic acids, which can be used to extract the
masses (Joshi et al., 2015a; McCormick and Kautto, 2013; Ravindran byproducts (Viuda-Martos et al., 2011). Additionally, El-Kamah et al.
and Jaiswal, 2016b). In September 2015, the UN Sustainable Devel- (2010) proposed different treatment schemes for the generated waste-
opment Summit agreed to adopt findings of the document “Trans- water, based on integrated anaerobic/aerobic systems, which have
forming our world: the 2030 Agenda for Sustainable Development” shown high removing efficiency for BOD, COD, TSS, oil, and grease.
which expands 17 Sustainable Development Goals (SDGs) for protec- An LCA study and sensitivity analysis, aiming at describing man-
tion of the planet (Matharu et al., 2016). For the USA, Carlson (2016) agement strategies to increase environmental performance for the
comprehensively assessed the biotech sector’s contribution to the US production of Italian citrus-based essential oils and juice, was con-
economy. ducted by Beccali et al. (2010). Based on their results, some re-
Green chemistry’s use, for example, of green extraction, green commendations, with energy and environmental benefits, were pro-
chemical, and biochemical technologies, has recently become a hot posed. Reusing the consumed water (mainly generated in the cleaning
topic in scientific research in order to fulfill our responsibilities with the step) for irrigation, using the railway transportation system for product
environment in addition to develop bioeconomy (Esquivel-Hernández delivery, and adopting efficient technologies, e.g., mechanical vapor
et al., 2017; Forster-Carneiro et al., 2013; Isikgor and Becer, 2015; Miao recompression in the pasteurization and concentration of juice, were
et al., 2017; Pfaltzgraff, 2014; Sheldon, 2014). An example of using suggested.
CPW for developing a bioeconomy was conducted by Paggiola et al. The most important concern in citrus processing industries is the
(2016). They quantitatively assessed the substitution capacity of limo- management of citrus solid waste. This solid waste is typically con-
nene, a green citrus-derived solvent, for petroleum-derived toluene, stituted of the peel, seeds, and leaf residues remaining after the juice
which is nowadays widely used as an industrial cleaning agent. Al- extraction process. Although some solid wastes are also generated from
though their results showed that the potential replacement of toluene packaging and off-specification materials in a juice production facility,
with limonene in a global level is currently unreachable, the substitu- the main CPW here referred to is, in nature, organic waste, which is
tion is feasible in regional places for citrus-producing and −importing generally varied in composition and pH, depending on harvest time,
countries. In the energy sectors, a major transformation from fossil-fuel location, and handling processes. The primary environmental problem
industries to renewable energies is essential, to not only meet the huge of CPW is high fermentability, because of its high carbohydrate content,
demands but also to remain within the limitation of global warming to which can accelerate its degradation (Lin et al., 2013). Traditional CPW
2 °C (or less), as envisaged in the Paris Agreement (2015) (Armstrong reduction strategies, e.g., incineration or landfilling, are nowadays in-
et al., 2016; Peake and Ekins, 2016). In this regard, the high carbohy- sufficient and problematic in terms of environmental impacts and en-
drate content and low lignin content of CPW (Table 1) also make it a ergy efficiency (Wei et al., 2017). A part of CPW is also used as low-
promising lignocellulosic feedstock for second generation fuels, e.g., value cattle-feeding; however, it has low protein content. Regarding the
ethanol and methane (Ruiz et al., 2016), and fine chemicals production high organic content, in 2008, the EU directive establishes that CPW,
(Section 5). like any other kinds of organic waste, cannot be disposed of into a
landfill, unless it has been previously subjected to an energy and re-
2.2. Environmental burdens of citrus processing industries source recovery process (Negro et al., 2017; Negro et al., 2016a). This
situation also exists in a number of South American and Asian countries
The main environmental burdens of fruit production are generally such as China and India. Nonetheless, CPW can be valorized to obtain
reported to be management of pest and disease, fertilization, irrigation, derivatives to be used as a source of energy, e.g., by fermentation, and
soil management, harvest, and weather damage protection (Cerutti other useful chemicals by physical treatments. This may enable the EU,
et al., 2015). To profile the environmental burdens of orange produc- by 2020, to obtain about 20% of their energy demands from renewable
tion in different areas in Brazil, a Life Cycle Assessment (LCA) study was biological resources.
conducted by Coltro et al. (2009). They reported that the production of
1000 kg orange requires ca. 120–4400 MJ energy, 0.3–36 kg diesel, 3. Applications of native/modified CPW as an environmentally
1100–54500 kg water, 0.3–65 kg fertilizers, 0.1–13.5 kg pesticides, and sustainable material
8–650 kg soil correctors, which are mainly varied according to the
cultivation region. These data were evaluated while excluding the en- 3.1. Nanoparticles
vironmental impacts of production of fertilizer and pesticides. The
study further reported that except for “land use”, only 21% of agri- Nanomaterial developments from food processing waste are a quite
cultural lands showed good performance in using pesticides, fertilizers, new field of research, and there are few studies on the use of CPW for
and soil correction compounds. making nanomaterials. Dominantly mesoporous cellulose with a few
The energy used in agrofood sectors during their life cycles is esti- large macropores was obtained from orange peel residues by using a
mated to be 20% of total consumed energy in developed countries, microwave treatment (Balu et al., 2012). In another study, Mariño et al.
which is considered as another source of significant environmental (2015) extracted nanocellulose from citrus waste with an average dia-
burdens. Primary energy consumption and consequently greenhouse meter of 10 nm and a length of 458 nm. Purified cellulose obtained
gas emissions were reported as the main contributors of the global from mandarin peel waste was used to obtain cellulose nanofibrils with
warming potential of these sectors (Beccali et al., 2009). The consumed widths of 2–3 nm (Hiasa et al., 2014). Interestingly, there are other
energy is a cause of major environmental burden in the citrus proces- reports in the literature on using pectin-derived CPW for making mi-
sing industries, as well. An analysis of energy for an orange manu- crosphere (Zhang and Zhou, 2017) and using CPW as a substrate for
facturing facility revealed the total energy intensity of 1.12 MJ/kg or- producing nano bacterial cellulose (Fan et al., 2016).
ange juice, mainly in the forms of electricity and steam, is required, of
which pasteurization followed by packaging are the most energy-con- 3.2. Biosorbents
suming unit operations (Waheed et al., 2008).
In addition, another main environmental concern of a citrus juice Different types of agro-industrial waste, e.g., sugarcane bagasse and
production facility is its high amount of wastewater generated, e.g., fruit peels, have been used as biosorbent for contaminations removal

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Table 2
Adsorption isotherms for different citrus waste–derived constituents for removal of heavy metal ions.

Substrates Metal ions Langmuir isotherm Freundlich isotherm Refs.

qmax (mg/g) b (L/mg) R2 KF n R2

Waste orange peel (at 20 °C) Cu2+ 63.30 0.074 0.965 6.32 1.34 0.98 Guiza (2017)
Citrus waste biomass UVI 39.37 0.029 0.994 11.64 1.297 0.738 Saleem and Bhatti (2011)
Orange peel (at 308 K) AcV 0.38 0.0704 0.980 0.63 0.76 0.99 Khaskheli et al. (2011)
Copolymerization-modified orange peel (OPAA). Cd2+ 293.3 0.022 0.9886 20.36 2.15 0.8649 Feng et al. (2011)
Ni2+ 162.6 0.032 0.9926 5.93 1.45 0.9450
Pb2+ 476.1 0.056 0.9964 103.9 3.88 0.4974
Dried orange peel Pb2+ 89.77 0.0349 0.9263 8.5672 0.4284 0.9703 Liang et al. (2009)
Orange peel xanthate 204.50 0.1318 0.9810 42.8450 0.3088 0.5195

from contaminated water supplies, which is a low-cost and an eco- on citrus waste biomass also fitted quite well to the pseudo-second
friendly solution (Shakoor et al., 2016). Orange peel waste was reported order equation (R2=0.980) (Saleem and Bhatti, 2011). Fitting the ad-
to be capable of arsenic removal from drinking water (Khaskheli et al., sorption data to the pseudo-second order kinetic model suggests that
2011). Grapefruit peels were also used for removal of Cu(II) from chemical sorption may be considered as the rate limiting step for bio-
wastewater stream, where a physisorption mechanism was reported to sorption of the heavy metals on the peels, which presumably involves
occur between oxygen-containing groups of the peels and Cu ions covalent interactions via sharing or exchanging electrons (Feng et al.,
(Romero-Cano et al., 2017). Different process variables, such as pH, 2011).
temperature, contact time, and adsorbent properties, such as adsorbent The adsorption capacity of biosorbents can be calculated by using
dosage and concentration, have been shown to be effective in bio- equilibrium adsorption isotherms, and the most commonly used ad-
sorption (Guiza, 2017; Saleem and Bhatti, 2011). sorption isotherms are Langmuir and Freundlich isotherms. The
Chemical modification of orange peel by, e.g., graft copolymeriza- Langmuir equation is,
tion, or introducing sulfur groups to the peel via carbon disulfide
Ce 1 C
treatment, was reported to enhance its adsorption capacity for heavy = + e
qt qmax b qmax (4)
metals (Feng et al., 2011; Liang et al., 2009). Treatment of grapefruit
peel by using DIC (Instantaneous Controlled Pressure Drop) was re- where qmax is the monolayer capacity of the biosorbent (mg/g), and b is
ported as a feasible method for increasing porosity and surface area and the biosorption constant (L/mg).
subsequently improving its adsorption capacity for Cu(II) (Romero- The Freundlich isotherm is,
Cano et al., 2017).
1
The amount of biosorption can be calculated by Eq. (1). qe = KF Ce n (5)
(C − Ce ) V
qe = 0 In this equation, KF and n show the capacity of adsorption and its in-
m (1) tensity, respectively.
where C0 and Ce are the initial and equilibrium concentration of ad- Table 2 shows the results of fitting the adsorption isotherms to the
sorbed ion (mg/L), V is the volume of solution (L), m is the amount of biosorption data of metal ions for different citrus wastes. The correla-
biosorbent (g), and qe is the amount of adsorption at equilibrium (mg/ tion coefficient values (R2) showed better fits of experimental data to
g). The amount of biosorption rapidly increases at the initial times of the Langmuir equation and consequently predicted a monolayer me-
adsorption and then the rate of adsorption decreases until it reaches a chanism for biosorption of heavy metals by different CPW. Ghimire
constant amount of adsorption. et al. (2002, 2003) reported this mechanism for arsenic removal from a
The kinetics of adsorption can be further modeled by pseudo first- Lagergren isotherm by using orange waste. They reported maximum
order and pseudo-second order models. Lagergren’s pseudo first-order sorption capacities (mg/g) of 70.43 for orange waste and 143.25 for
model is described as (Ho and McKay, 1998), phosphorylated orange juice residue in ArIII adsorption and 143.25 for
phosphorylated orange waste in ArV adsorption (Ghimire et al., 2002;
k1
log (qe − qt ) = log qe − t Ghimire et al., 2003). Immobilization of orange waste with zirconium
2.303 (2)
(IV) was reported to improve its adsorption capacity for phosphate
where qt is the amount of adsorption at time t (mg/g) and k1 is the removal to 57 mg/g, compared with 13 mg/g and 43 mg/g for zirco-
pseudo first-order adsorption rate constant (min−1). The pseudo-second nium ferrite and a Zr(IV)-loaded resin, respectively (Biswas et al.,
order model is described as (Behnam et al., 2015; Zou et al., 2006), 2008).
Beyond the studies on using raw or chemically modified CPW for
t 1 t
= + biosorption, pectin based biosorbents were reported to have high ca-
qt k2 qe2 qe (3) pacity for remediation of heavy metals from aqueous environments. For
where k2 is the pseudo-second order adsorption rate constant (g/ example, Lessa et al. (2017) reported on the high adsorption capacity of
mg.min). pectin and pectin/cellulose microfibers beads extracted from orange
These models were used for the evaluation of the kinetic mechanism waste for remediation of methylene blue in an aqueous solution. Si-
of Pb2+, Cd2+, and Ni2+ sorption on modified orange peel (Feng et al., milarly, Pangeni et al. (2014) used a Ca-modified orange pectin for
2011). The results showed that the linear model could not predict the removal of radioactive elements Cs(I) and Sr(II) via a cation exchange
experimental qe values in spite of having high correlation coefficient mechanism. According to their results, the adsorption capacity for Cs(I)
values (R2), while the pseudo-second order kinetics closely matched the and Sr(II) were found to be 1.22 and 0.83 mmol/g, respectively
equilibrium data. Similarly, the pseudo-second order equation better (Pangeni et al., 2014).
predicted the behavior of adsorption of phosphorous on zirconium(IV)
immobilized orange waste rather than the pseudo-first order equation, 3.3. Biofertilizer
in terms of both coefficient of determination and adsorption capacity
(Behnam et al., 2015). The adsorption kinetics of hexavalent uranium Another important application of CPW is its use as an organic

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B. Satari, K. Karimi Resources, Conservation & Recycling 129 (2018) 153–167

fertilizer, by making compost by adjusting the waste’s C/N ratio, pH, et al. (2016) quantitatively analyzed 170 volatile compounds of
and water content to 24:1, 6.3, and 60%, respectively, as Angel Siles grapefruit pulp, i.e., monoterpenes, sesquiterpenes, terpenic alcohols
Lopez et al. (2010) recommended. They further studied, in detail, the and aldehydes, aliphatic alcohols and aldehydes, ketones, esters, and
main characteristics of a mature compost for this application. Another alkanes, each with different cultivars. Limonene is also categorized as a
feasible use for the production of biofertilizer from citrus pulp was terpene, which is discussed later. Citrus peel residues are rich sources of
reported by Panuccio et al. (2016). They reported that proper mixing of phenols and carotenoids, which can be used to enhance the shelf life of
animal manure, maize silage, and citrus pulp yielded considerable food and beverages (Okino Delgado and Fleuri, 2016).
amounts of biogas, and the digestate is an antioxidant-rich compound The recovery of phenolic compounds from CPW residues has been
that can be used as fertilizer in agriculture. accomplished through green extraction techniques, e.g., ultrasound-
assisted extraction (UAE) and microwave-assisted extraction (MAE)
(Dahmoune et al., 2013; Hayat et al., 2009; Hayat et al., 2010; Kala
4. Green extraction superiority over traditional extraction
et al., 2016). MAE was reported to be a better method rather than UAE
methods to obtain high-value bioactive/nutraceutical extracts
and traditional solvent-assisted rotary extraction for phenolic acid ex-
from CPW
traction from mandarin citrus peels, in terms of higher extraction effi-
ciency and antioxidant activity (Hayat et al., 2009). Total phenolic
Ultrasound- and microwave-assisted extraction, the widely used and
compound recovery of up to 15.78 and 15.22 mg gallic acid equivalents
environmentally friendly extraction techniques, have been applied to
(GAE)/g were obtained from Citrus limon residues using MAE and UAE
the extraction of natural products from a variety of resources. Besides
methods, respectively (Dahmoune et al., 2013). Nayak et al. (2015)
the effectiveness of these methods, selectivity for the product recovery,
compared the potential of MAE, UAE, and traditional solvent-assisted
fast and easy operation, and lower energy consumption and CO2
extraction (SAE) for the recovery of polyphenols from Citrus sinensis
emissions, are among the technical and environmental benefits of these
peel. The highest amount of total phenolic content, 12.20 mg GAE/g
methods (Banerjee et al., 2017; Chemat et al., 2017; Ferrentino et al.,
dry weight, was obtained by using MAE. Furthermore, total antioxidant
2016; Flórez et al., 2015). Microwave can provide high but controllable
activity for the microwave-assisted extracts was higher compared with
heating rates and allow performance of an integrated extraction pro-
other extraction techniques.
cess. The high water content of CPW cannot limit its applications, be-
cause of the good interaction of microwave with dielectric water,
helping the applications of this technology (Pfaltzgraff et al., 2013). 4.1. Extraction of flavonoids and carotenoids
In addition to traditional batch mode extraction using ultrasound
and microwave, some hybrid configurations, aiming at enhancing Flavonoids are phenolic compounds that present in high amounts in
product recovery, have been developed (Fig. 2). Moreover, the combi- citrus peel and have nutraceutical advantages because of mainly their
nations of ultrasound-assisted extraction with some innovative techni- antioxidant activities. Flavanones are the major class of flavonoids,
ques, i.e., microwave, DIC process, and supercritical fluid extraction, available in citrus fruits which are further classified into glycoside and
were reported as among the most promising hybrid techniques (Chemat aglycone flavanones, based on the availability (or not) of a glycoside
et al., 2017). Water is usually used as the extraction solvent in such group in their structure (Bocco et al., 1998; Roowi and Crozier, 2011).
systems, as water is an inexpensive, non-toxic, and environmental be- The flavonoid contents of orange peel are considerably different ac-
nign solvent; because of water’s intrinsic properties, the products’ cording to the cultivation local of the plant. Total flavonoid content of
purification is facilitated (Filly et al., 2016). The kinetics and me- orange peel extract was reported to be 14.0–31.9 mg/g orange peel
chanism of these extraction techniques would be industrially interesting extract (Chen et al., 2017). The most abundant glycoside flavanones in
and has been reviewed, in detail, in the literature (Chemat et al., 2017; citrus peel were reported to be naringin, hesperidin, and neohesperidin,
Pradal et al., 2016). and the concentration of aglycone flavanones were lower than that of
Bioactive compounds, e.g., lipids, minerals, vitamins, peptides, fatty the glycosides (Molina-Calle et al., 2015). Hesperidin was found to be
acids, polyphenols, dietary fibers, and carotenoids, are found in small the dominant flavonoid among the four major flavonoids of orange peel
amounts in plant-derived food waste (Serna-Cock et al., 2016). Al- extracts, i.e., narirutin, hesperidin, nobiletin, and tangeritin (Chen
though there is no restrict classification, bioactives are classified as et al., 2017). Hesperidin was also found as the dominant flavonoid in
phenolic compounds, terpenes and terpenoids, and alkaloids. Zheng the peel of different oranges from Citrus sinensis varieties (Manthey and

Fig. 2. New configuration technologies in using ultrasound- and microwave-assisted extraction: (a) Sono-Soxhlet-assisted extraction, (b) Sono-Clevenger-assisted extraction, (c) steam
distillation microwave-assisted extraction, and (d) gravitational microwave-assisted extraction (1. microwave hydrodiffusion and gravity, 2. microwave dry-diffusion and gravity, and 3.
vacuum microwave-assisted hydrogravity). The pictures were modified from Flórez et al. (2015) and Chemat et al. (2017).

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B. Satari, K. Karimi Resources, Conservation & Recycling 129 (2018) 153–167

Grohmann, 1996). biotechnologically-based methods have been developed for limonene

Flavonoids in citrus fruits are commonly solvent-extracted by production (Jongedijk et al., 2016). (+)-Limonene can be easily ob-
ethanol and/or ethanol-methanol blends. Besides this traditional ex- tained from CPW in a cold extraction process, and then is recovered by
traction method, hot-water extraction, irradiation-assisted extraction, simple centrifugation or steam distillation (Ciriminna et al., 2014).
adsorption, UAE, enzyme-assisted extraction and supercritical fluid Traditional solid-liquid extraction, by e.g., the Soxhlet apparatus, using
extraction, have been developed. The newest method for the recovery pure and/or mixed organic solvents, is another method for the extrac-
of phenolic compounds, including flavonoids, using membrane tech- tion of limonene. On the other hand, some green extraction techniques,
nologies has been discussed by Castro-Muñoz et al. (Castro-Muñoz e.g., supercritical fluid extraction, steam explosion, MAE, and UAE
et al., 2016). Several methods have been developed to quantify flavo- methods have been developed (Negro et al., 2016a). Negro et al.
noids. These methods include traditional determination of total phe- (2016b) extracted D-limonene from flavedo of orange peels via ap-
nolic content using the Folin–Ciocalteu reagent, which is an over- plying an accelerated moderate temperature extraction; up to 0.48%
estimation, and more precise analytical techniques, e.g., LC–MS and (w/w wet basis) D-limonene was extracted at 130 °C for 60 min. Attard
LC–MS-MS, for quantification of trace amounts (Molina-Calle at al., et al. (2014) extracted significantly higher amounts of D-limonene at
2015). shorter times from orange waste via MAE compared with the conven-
Under optimized condition of UAE, i.e., sonication power of 150 W tional heating. They further mathematically modeled the D-limonene
at 40 °C and using 4:1 ethanol: water ratio as solvent, naringin and extraction process and realized that it consists of an initial extraction
hesperidin yields of 70.3 and 205.2 mg/100 g fresh weight were ob- step from the exterior of cells followed by transmembrane diffusion.
tained from orange peel (Khan et al., 2010). M’hiri et al. (2015) opti- Although the diffusion coefficient at the first step was comparable for
mized the processing conditions for three extraction techniques, i.e., microwave and conventional heating, the transmembrane diffusion
MAE, UAE, and supercritical CO2 extraction (SCE), to obtain the highest coefficient was reported to be significantly higher for MAE, which led to
total phenol and flavonoid contents, and compared them to the con- a greater yield for this method (Attard et al., 2014). Aside from MAE,
ventional solvent extraction method. The optimum conditions for UAE, microwave-assisted hydrodistillation (MAHD) has been successfully
MAE, and SCE were reported to be 125 W for 30 min at 35 °C, 200 W for applied to extract EOs in wet citrus peel waste, with advantages of
180 s, and 10 MPa (at 80 °C) or 50 MPa (at 35 °C) for 30 min, respec- reducing costs, avoiding additives usage, and improving process yield
tively. (Bustamante et al., 2016).
Carotenoids are a type of tetraterpenoid, which are organic pig-
ments found in the chloroplasts and chromoplasts of plants and display 4.3. Pectin
antioxidant activities. More than 600 natural products are found to be
carotenoids and a strong relationship has been observed between the Pectin, also known as pectic polysaccharides, is a hetero-
intake of carotenoids and health benefits (Zou et al., 2016). The color of polysaccharide block copolymer made from a backbone of 300–1000
orange juices is primarily affected by the carotenoid pigments and the saccharide units of (1,4-α-linked) galacturonic acid and (1,2-linked)
carotenoid profile of juice is diversified from different kinds of xan- rhamnose, substituted with side branches of (1,4-linked) β-D-galactose
thophylls and both colored and colorless carotenes (Stinco et al., 2016). and/or (1,5-α-linked) L-arabinose (Ciriminna et al., 2015; Mohnen,
Carotenoids are obtained from various red and orange fruits and 2008). Pectic polysaccharides are comprised of four types of poly-
vegetables by traditional organic solvent extraction, which is often saccharides; homogalacturonan (HG), rhamnogalacturonan type I (RG-
expensive and environmentally harmful (Lawaetz et al., 2016). The use I), rhamnogalacturonan type II (RG-II), and xylogalacturonan, with HG
of supercritical CO2 and hydrolytic enzymes for extraction of car- and RG-I being the most abundant (Karboune and Khodaei, 2016).
otenoids is among the most efficient and environmental friendly pro- Pectin is available in the primary cell wall of terrestrial plants and is
duction methods. abundant in most vegetables and fruits (Ciriminna et al., 2015). It is
soluble in water and can add a desirable texture to food and beverages.
4.2. Extraction of essential oils (limonene) At low water concentration, pectin acts as a hydrocolloid, capable of
trapping water and forming gels. Because of its properties as a stabi-
Essential oils (EOs) are among the aromatic and volatile compounds lizing or thickening agent, it has applications in food products, such as
extracted from plant materials. EOs are important for plant defense jams. Furthermore, as a result of its biodegradability, biocompatibility,
since they have often shown antimicrobial effect against foodborne edibility, and chemical versatility, it is a suitable matrix for the making
pathogens. Citrus EOs have recently gained considerable attention for of edible active films with vast applications in food packaging (Espitia
use as flavorings in the food industry, because they are generally re- et al., 2014). Binding of pectin to low-density lipoprotein was reported
cognized as safe by the Food and Drug Administration (FDA) and are to reduce lipid absorption during digestion, making suitable dietary
tolerable with many foods. Citruses are the origin of approximately 400 product (Karboune and Khodaei, 2016).
EOs, and are composed of 85–99% volatile and 1–15% non-volatile
components. The volatiles are constituted of monoterpene (e.g., limo- 4.3.1. Isolation of pectin from CPW
nene), sesquiterpene hydrocarbons, and their oxygenated derivatives, Besides pectin, other polysaccharides, i.e., xyloglucan and glucur-
e.g., aldehydes (such as citral), ketones, acids, alcohols and esters onoxylan, generally exist in the cell wall of food waste. Xyloglucans
(Espina et al., 2011). have the ability to bind tightly to cellulose; and rather than xyloglu-
Limonene is the richest citrus essential oil, with a concentration of cans, pectin makes the majority of contacts with cellulose surface (Van
73.9-97% (w/w EOs). D-limonene was obtained from orange peel. Dyk et al., 2013). The complexity of cell wall structure and the mole-
Limonene is a renewable chemical with vast applications in flavor and cular interactions between its constituents make pectin extraction a
fragrance, a green solvent for extraction, and as an active agent for tedious process, requiring cell wall disruption to obtain the entrapped
functionalized products (Ciriminna et al., 2014). Chirality is important polysaccharides.
in the properties of limonene in flavor and fragrance agents, since Commercial pectin is currently being produced from citrus peel and
(+)-limonene (also R- or D-limonene) has a pleasant and orange-like apple pomace by treating the cell walls with hot dilute acid solution
odor, while (−)-limonene (also S- or L-limonene) has a harsh turpen- (e.g., HCl, HNO3, and H2SO4) followed by a final precipitation step
tine-like odor (Jongedijk et al., 2016). Currently, the dominant limo- using isopropanol or ethanol and filtration. Careful processing condi-
nene enantiomer in the market is (+)-limonene, which is mainly pro- tions with regard to temperature, time, and pH are necessary to prevent
duced from the byproduct of citric fruit processing by different polymeric degradation and to avoid losing the “hairy” regions of the
extraction methods. Global demand, however, is high and even polymer (Ciriminna et al., 2015; Karboune and Khodaei, 2016; Satari

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Table 3 strategies (Lin et al., 2013; Nanda et al., 2016) to convert CPW to en-
Yields of “green-labeled” pectins extracted from different citrus waste. ergy and fuels, several waste-to-energy bioconversion routes have been
developed (Karmee, 2016; Martín et al., 2010; Satari et al., 2016;
Substrate Extraction method Pectin References
yielda Torquato et al., 2017; Yasin et al., 2013). Biofuels are biologically
produced from renewable carbon resources and are important as sus-
Orange peel Enzymatic extraction 12.5% Donaghy and McKay tainable substitutes for fossil fuels, to meet the huge demand for liquid
Lemon peel 18.0% (1994)
fuels and to be less dependent on fossil fuels (Hashemi et al., 2016;
Orange peel Microwave heating 18.0% Kratchanova et al.
(2004) Taherzadeh and Karimi, 2008). Gaseous biofuels, e.g., biogas and bio-
Orange peel Microwave heating 18.13% Guo et al. (2012) hydrogen, liquid biofuels, e.g., ethanol and butanol, fermentative pro-
Orange peel Microwave-assisted 18.59% Prakash Maran et al. ducts, e.g., lactic acid, and even solid biofuels, were produced from
extraction (2013) CPW. Different food processing wastes, including CPW (Torquato et al.,
Grapefruit peel Ultrasound-assisted 29.25% Xu et al. (2014)
2017), were reported to be capable of producing hydrogen via dark-
heating extraction
Lime peel Enzymatic extraction 23% Dominiak et al. fermentation, photo-fermentation, and/or combined-fermentation (Van
biomass (2014) Dyk et al., 2013).
Citrus peel Subcritical water 21.95% Wang et al. (2014)
Orange peel Microwave-assisted 24.2% Boukroufa et al.
5.1. Pretreatments and their effects on downstream processes
waste extraction (2015)
Grapefruit peel Ultrasound-assisted 27.34% Wang et al. (2015)
heating extraction CPW contains considerable amounts of sugars, i.e., fructose, glu-
Sour orange peel Microwave-assisted 29.1% Hosseini et al. (2016) cose, and sucrose, and also carbohydrate polymers dumped in the
extraction structure of the waste. Although the free sugars can be easily water-
a extracted (Satari et al., 2016), for efficient release of fermentable sugars
Maximum g pectin/g DW of raw substrate.
from carbohydrate polymers to produce gaseous fuels and fermentative
products, a pretreatment step is usually required before enzymatic
et al., 2017). Another problem of this method is its negative environ-
hydrolysis (Satari et al., 2017). Most food processing wastes are lig-
mental impacts, limiting its application, since it produces hazardous
nocellulosic in nature and different pretreatment methods may apply to
contaminants during treatment (Mamma and Christakopoulos, 2014).
them. Lignocellulosic pretreatment is usually refers to a “physical”,
Facing these deficiencies, consumer demand has recently moved toward
“chemical”, “biological”, or a combination of these methods, and is
so-called “green-labeled” pectin (Zykwinska et al., 2008; Zykwinska
employed to open up the lignocellulosic recalcitrant structures and
et al., 2009). Recently, Adetunji et al. (2017) extensively reviewed the
make them amenable to enzymatic hydrolysis and/or microbial attacks
principles and mechanisms, operational issues, and benefits and
(Carlsson et al., 2015; Taherzadeh and Karimi, 2008). Ravindran and
drawbacks, of some novel techniques for pectin extraction. Table 3
Jaiswal (2016a) comprehensively reviewed the pretreatment strategies
reviews some studies for pectin extraction via green extraction pro-
of lignocelluloses for food and food processing industry waste. How-
cesses from different CPWs. Despite their potential costs, enzymatic
ever, because of low lignin content, the hydrolysis of CPW, compared
extraction techniques have been widely used as an environmentally
with usual lignocelluloses, is not too problematic, and the pretreatment
friendly way to extract green-labeled pectin (Karboune and Khodaei,
methods have mainly focused on hydrothermal processing. Hydro-
2016; Martínez Sabajanes et al., 2012). The enzymes can degrade the
thermal processing is primarily aimed at removing and/or lowering
backbone, substituents, or side chains of pectin structure. Various
limonene and other chemicals that show inhibitory effects for the en-
pectinolytic enzymes including endo-/exo-polygalacturonase, pecti-
ergy valorization route. For example, steam pretreatment of CPW at
nesterase, pectin lyase, and pectate lyase have been used for pectin
160 °C for at least 4 min caused a reduction of D-limonene content to
extraction with minimal adverse chemical modifications. Proteases and
less than 0.1% (Widmer et al., 2010). The inhibitory effects of limonene
cellulases, which act on protein and cellulose in the cell wall, have been
on bioconversion of CPW to two major biofuels, i.e., bioethanol and
also used for green-labeled pectin extraction from citrus peel
biogas, are discussed in following sections.
(Zykwinska et al., 2008). UAE was reported to yield higher pectin, by
16.34%, from grapefruit peel, compared with the conventional heating
5.1.1. Inhibition of ethanol-producing microorganisms by limonene
extraction. The extracted pectin was characterized as having different
The presence of limonene in fermentation media causes an in-
properties depending on the heating type applied in the extraction
hibitory effect on ethanol-producing microorganisms (Table 4). Initial
process (Wang et al., 2016). MAE, which is used for pectin extraction
and final threshold concentrations of D-limonene for inhibiting ethanol
from CPW in the presence of a solvent or in a solvent-free medium, has
production by S. cerevisiae were reported at 0.33% and 0.14% (v/v),
been reported as a successful method (Table 3). Prakash Maran et al.
respectively (Wilkins et al., 2007b). A minimum inhibitory peel oil
(2013) obtained a maximum 19.24% pectin yield via MAE from orange
concentration of 0.01% (v/v) was reported for ethanolic fermentation
peel under the optimum conditions of power 422 W, treatment time
of orange peel by Pichia kudriavzevii KVMP10 (Koutinas et al., 2016).
169 s, pH 1.4, and a solid-to-liquid ratio of 1:16.9 g/mL. MAE of pectin
For the ethanologenic bacterium Zymomonas mobilis (at 37 °C),
provides the advantages of reduced extraction time (by several min-
minimum concentrations of orange peel oil for inhibition of ethanol
utes) and energy consumption. Moreover, as stated by Budarin et al.
production were reported at 0.05%, 0.10%, and 0.20%, after 24, 48,
(2015), using microwave irradiation to recover valuable molecules
and 72 h, respectively, and no inhibition was observed after 96 h
from bio-waste generally has the advantages of recoveries at lower
(Wilkins, 2009). Mucor indicus, a filamentous ethanol-producing fungus,
temperatures than conventional heating, and highly functional mole-
and Rhizopus sp., isolated from tempeh, have shown tolerance to
cules will be produced. Despite the potential advantages, the high cost
maximum 2% D-limonene in semi-synthetic media under aerobic and
of this method limits its uses in industry and further optimizations are
anaerobic conditions (Lennartsson et al., 2012). The two zygomycetes
required in order to develop the process scale-up (Adetunji et al., 2017).
are capable of producing ethanol at high concentrations of the anti-
microbial compounds available in orange peel hydrolyzates, which are
5. Technologies and challenges for bioconversion of CPW to intolerable to almost all microorganisms.
biofuels and fermentative products
5.1.2. Effects of limonene on anaerobic digestion
Besides thermal and thermochemical technologies, i.e., incinera- Removal of limonene is also necessary for efficient biogas produc-
tion, pyrolysis and gasification, and hydrothermal carbonization tion from CPW. Ruiz and Flotats (2014) investigated the effects of citrus

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Table 4
Inhibition of ethanol-producing microorganisms by limonene.

Substrate Ethanologenic Fermentation conditions Limonene Refs.

microorganism concentrationa

Enzymatic hydrolysates of citrus peel S. cerevisiae Simultaneous saccharification and fermentation, 0.14% Wilkins et al. (2007b)
waste anaerobic condition in glass bottles at 37 °C
Solutions modeling hydrolyzed S. cerevisiae Submerged fermentation, anaerobic condition in 0.05% Wilkins et al. (2007a)
Valencia orange peel waste Kluyveromyces marxianus baffled flasks at 37 °C
A model sugar solution with orange Zymomonas mobilis Submerged fermentation, anaerobic condition in shake 0.05% Wilkins (2009)
peel oil flasks, 30 °C and 37 °C
Modelling orange peel hydrolysates by M. indicus Submerged fermentation under aerobic and anaerobic 2.0% Lennartsson et al.
semi-synthetic media Rhizopus sp. conditions, 32 °C, in shake flasks and bioreactor (2012)
Orange peel hydrolysates Pichia kudriavzevii Submerged fermentation, 30 °C and 42 °C, in shake 0.01% Koutinas et al. (2016)
KVMP10 flasks and bioreactor

a
Minimum concentration of limonene for showing an inhibitory effect (v/v).

Table 5
Biogas production from pretreated citrus processing wastes.

Substrate Pretreatment Organic loading rate Biogas yield Refs.

3
Orange peel waste Limonene removal by steam 1.20–3.67 kgCOD/m d and solid 0.27–0.29 LSTP CH4/g added COD corresponded to the Martín et al. (2010)
distillation retention time of 25 d biodegradability of 84–90%
Citrus waste Using membrane bioreactor 3.0 kg VS/m3/day, 30 d 0.33 Nm3/kgVS Wikandari et al.
(2014)
Waste orange peel Hexane extraction (20 °C for 10 min) Batch reactor for 33 days 0.217 mCH43kgVS−1 Wikandari et al.
of limonene (2015)
Citrus waste Biodegradation pretreatment and Batch reactor for 30 days Maximum 176.05 mLCH4kgVS−1 Su et al. (2016)
Orange pulp Milling CSTR, 18 days 0.25 mCH43kgVS−1 Galí et al. (2009)
Orange seed Ripening Batch reactor, mesophilic 657 LCH4kgVS−1 Sanjaya et al. (2016)
Orange pulp conditions, 60 days 311 LCH4kgVS−1
Orange peel 48 LCH4kgVS−1

EOs on anaerobic digestion (AD). Limonene was reported to have in- the toxic effects of the inhibitors (Wikandari et al., 2014).
hibitory effect on AD in concentrations greater than 200 mgkg−1,
presumably due to the production of cymene and other biodegradable 5.2. Enzymatic hydrolysis and fermentation
inhibitory compounds during the AD process (Ruiz and Flotats, 2016).
A 70% removal of D-limonene through pretreatment resulted especially The presence of pectin in the pectin-containing substrates makes
in the convenience of thermophilic bacteria in the biomethanization of them resistant to hydrolysis (Xiao and Anderson, 2013). Dilute-acid
orange peel waste (Martín et al., 2010). The effects of different pre- hydrolysis of citrus waste, even at 210 °C, was reportedly unable to
treatments, mainly aiming at limonene removal, on biogas production depolymerize poly-galacturonic acid, while the hydrolysis process is
using citrus wastes are presented in Table 5. The values of biochemical usually followed by the synergistic action of cellulases, β-glucosidase,
methane potential (BMP) for different citrus wastes were reported to be and pectinase (Santi et al., 2015; Talebnia et al., 2008). Hydrolysis of
176–657 LCH4.kgVS−1. Limonene concentrations up to 2.5 g/L did not the lignocellulosic materials by the “enzymatic” processes has generally
affect the BMP values, although they slowed the process. For half emerged as a prominent process for the production of monomeric su-
maximal concentration of limonene to be an inhibitor to the anaerobic gars for subsequent biofuels production (Taherzadeh and Karimi, 2007;
digestion of microcrystalline cellulose, the value was reported to be Zhu et al., 2011). A combination of hydrolytic enzymes is generally
423 mg/kg (Ruiz and Flotats, 2016). Steam explosion reduced limonene required for complete hydrolysis of the biomass. Cellulose is hydrolyzed
concentration by 94.3% and increased 426% methane production to by the synergistic action of endo-1,4-β-D-glucanases, exo-1,4-β-D-gluca-
434LCH4.kgVS−1 compared with that of obtained from the untreated nases or cellobiohydrolases I and II, and 1,4-β-D-glucosidases (Karimi
samples (Forgács et al., 2012). et al., 2013). Hemicellulases are depolymerases and debranching en-
The choice of AD digester and operating conditions is important to zymes that synergistically hydrolyze hemicellulose from mixed sources
decrease the inhibitory effect of limonene. Peel waste and wastewater (Taherzadeh and Karimi, 2007). Because of the synergistic action of the
of a citrus juice production facility were biogasified under a thermo- enzymes, the combination of both the cellulase and pectinase was re-
philic condition in a leach-bed batch anaerobic digester (25 days) and ported to be more effective to hydrolyze orange peel than the use of one
in a down-flow stationary fixed film reactor, respectively (Koppar and of them (Grohmann and Baldwin, 1992). Wilkins et al. (2007c) opti-
Pullammanappallil, 2013). Accordingly, no significant inhibitory effect mized the enzymes’ loading for efficient hydrolysis of grapefruit peel
of limonene was observed for both feedstocks. Another strategy for waste. They reported that a minimum loading of 5 mg pectinase and
removing the negative effect of limonene on AD performance is to co- 2 mg cellulase per g peel dry matter is required to yield the most glu-
digest CPW with other biowastes. By this strategy (anaerobic co-di- cose.
gestion), Calabrò et al. (2016) obtained maximum 370 and The enzymatic hydrolysis and fermentation can be traditionally
300LCH4.kgVS−1 from orange peel waste under mesophilic and ther- performed by separate enzymatic hydrolysis and fermentation, or via
mophilic conditions, respectively. It is notable that besides limonene, integrated processes, i.e., simultaneous saccharification and fermenta-
fruit flavors, e.g., aldehydes, terpenes, and alcohol, at concentrations of tion; non-isothermal simultaneous saccharification and fermentation;
over 0.5%, showed inhibitory effects on batch AD and considerably simultaneous saccharification, filtration, and fermentation; and si-
reduced methane production (Wikandari et al., 2013). Biogas produc- multaneous saccharification and co-fermentation. Another approach,
tion from CPW by membrane bioreactor, e.g., by using hydrophilic called consolidated bioprocessing (CBP), can convert biomass to bio-
polyvinylidene difluoride (PVDF) membranes, was suggested to reduce fuels in a single process by using anaerobic bacteria capable of

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B. Satari, K. Karimi Resources, Conservation & Recycling 129 (2018) 153–167

producing cellulosome enzymes with considerable activity. CBP is a

Wilkins et al. (2007b)

Widmer et al. (2010)

Boluda-Aguilar et al.
more effective process than the others; however, it is in its developing

Joshi et al. (2015b)

Santi et al. (2015)

Choi et al. (2013)

Choi et al. (2015)

Grohmann et al.
stage and needs more studies, especially in metabolic engineering
(Maitan-Alfenas et al., 2015; Salehi Jouzani and Taherzadeh, 2015).
References

(1994a)

(2010)
5.3. Biochemicals from submerged cultivation of CPW hydrolysates

Enzymatic hydrolysates from CPW can be used as sugar-containing

0.49 g/g and overall productivity of 3.4 g h−1

Ethanol concentrations of 14.4–29.5 g/L and

substrates for the production of different types of fermentative pro-

Maximum 41 g/L ethanol and 19.5 g/L

ducts, e.g., ethanol and butanol, succinic acid, citric acid, and lactic
acid (Li et al., 2010; Liang et al., 2016; Rivas et al., 2008). Several

without nutrients supplementation

studies have been performed on ethanol and butanol production from
Ethanol concentration or yield

CPW, to be used as liquid fuels (Awan et al., 2013; Choi et al., 2015;
Ethanol yields of 76–94%
3.96 w/v yield of ethanol

Joshi et al., 2015b; Santi et al., 2014). Table 6 summarizes the results of
some studies on ethanol production from different citrus wastes. Con-
Ethanol yield 90.6%

yields, 90.2–93.1%
50–60 L/1000 kg

siderable amounts of ethanol were obtained via applying the pretreat-

ment, hydrolysis, and fermentation of CPW. Notably, since the hydro-
lysates from citrus waste contain a variety of sugars, including pentoses,
4.7 g/L

hexoses, and galacturonic acid, the fermentative microorganism should

be able to assimilate them to obtain a high conversion yield. Grohmann
et al. (1994b) reported the capability of an ethanologenic construct of
Escherichia coli in galacturonic acid fermentation. Mucor indicus and
Rhizopus sp. were also reported to be able to consume galacturonic acid,
as well (Karimi and Zamani, 2013; Lennartsson et al., 2012).
Ethanol-producing
microorganism

Orange peel with less than 0.1% limonene, which is the threshold
S. cerevisiae

S. cerevisiae

S. cerevisiae

S. cerevisiae

S. cerevisiae

S. cerevisiae

S. cerevisiae

concentration to inhibit succinate and acetate generation and bacterial

growth, was converted to succinic acid using Fibrobacter succinogenes
E. coli

S85, and a maximum 0.12 g/g acid yield was obtained (Li et al., 2010).
Obtained from autohydrolysis of orange peel, on 38.2 g/L free sugars
Pectinase (0–396 IU/g), cellulose (0-0.18 FPU/g), and β-glucosidase (0–52.3

Cellulase (0.122 FPU/mg protein), pectinase (240 IU/mg protein), xylanase

(2.65 U/mg), and β − glucosidase (2.6 IU/mg solid), solid loading 1% (w/v)
Acid hydrolysis, 1% v/v acid concentration, 10 min residence time and 15%
Cellulase (Celluclast 1.5 L, 2 mg/g), β-glucosidase (Novozym 188, 2.1 mg/g),

In-house enzyme from A. citrisporus (12–16 mg protein/g) In-house enzyme

Acid hydrolysis (0.5% H2SO4, 180 °C) or enzymatic hydrolysis: cellulase (6

supplemented with calcium carbonate and methanol, a maximum

Cellulase (Celluclast 15L, 1.9 mg protein/ga), pectinase (Pectinex Ultra SP,

Cellulase (6.6 FPU/100 g), β-glucosidase (59.4 IU/100 g), and pectinase
0.8 mg protein/g), and β-glucosidase (Novozym 188, 1.6 mg protein/g)

9.2 g/L citric acid was produced by Aspergillus niger CECT 2090 (Rivas
et al., 2008). Lactic acid was observed to be the dominant chemical
produced in fermentation broth of different agricultural peel wastes by
using mixed cultures (Liang et al., 2016). Submerged fermentation of
orange peel by Pseudomonas aeruginosa MTCC 2297 produced 9.18 g/L
rhamnolipid biosurfactant with a surface tension reduction of up to
31.3 mN/m (George and Jayachandran, 2009). Citrus waste free sugars,
from T. longibrachiatum (10–25 mg protein/g)

which are easily water extractable, were previously reported as a

or 12 FPU/g) and pectinase (25 or 50 U/g)
and pectinase (Pectinex Ultra SP, 5 mg/g)

carbon- and nutrient-complete medium for cultivation of zygomycetes

fungi to obtain valuable fungal oil, chitosan, and protein (Satari et al.,
2016).

5.4. Solid state fermentation of CPW

w/v substrate loading

Solid state fermentation (SSF), which is the growth of microorgan-

isms on moist substrates, is an attractive process for the production of
(42.0 IU/100 g)

industrial enzymes from CPW (Farinas, 2015; Mamma et al., 2008).

Hydrolysis

Physicochemical characteristics, e.g., critical humidity point and water

IU/g)

absorption index, as well as microbiological properties of orange and

lemon peel have proven their use as suitable substrates for SSF by, e.g.,
Aspergillus niger (Orzua et al., 2009). Pectinolytic, cellulolytic, and xy-
Ethanol production by different citrus processing wastes.

lanolytic enzymes have mainly been the focus of enzymes’ production

Acid-catalyzed steam-
Popping pretreatment

Without pretreatment

from CPW. Different parameters, e.g., temperature, pH, time, culture

Acid pretreatment

medium, initial moisture level, and type of bioreactor and aeration, are
explosion (ACSE)
Steam explosion

Steam explosion

among the influential factors for the production of enzymes via SSF
Pretreatment

(Farinas, 2015). Pectinase can be industrially produced by citrus waste

Milling

owing to its moisture content with no need for harsh pretreatment

ACSE

before use. Microorganisms used in enzyme production are usually

Gram dry matters of CPW.

fungi, especially filamentous fungi like species of Aspergillus and Rhi-

Citrus processing waste

zopus genus (El-Bakry et al., 2015). Mesophilic fungi, e.g., A. niger,

Mandarin peel waste

Mandarin peel waste

Orange peel waste

Fusarium oxysporum, Neurospora crassa, and Penicillium decumbens, were

Citrus peel waste

Citrus peel waste

used for enzyme production under SSF on dry orange peels (Mamma
Orange peel

Orange peel

et al., 2008). Under optimal conditions, A. niger was reported as the best
Substrate

candidate for polygalacturonase and pectate lyase and xylanase pro-

Table 6

duction. In another study, A. niger was cultivated on citrus peel, and a

a

maximum 265 and 65 U/g pectinases and xylanases, respectively, was

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B. Satari, K. Karimi Resources, Conservation & Recycling 129 (2018) 153–167

produced by the fungus (Rodríguez-Fernández et al., 2011). For better obtained by steam distillation extraction. In another study, Fidalgo
control of process variables in SSF to produce pectinase by A. oryzae, et al. (2016) used water as solvent and MW as energy source for the
the addition of sugarcane bagasse to the citrus pulp was recommended extraction of pectin and EOs from orange and lemon peels. The most
(Pitol et al., 2016). A 48.4% sugarcane bagasse mixture made the pulp promising result of this study was reported to be the ability of scaling
matrix more porous and avoided the problems of bed shrinkage in a up the process for lemon peels, while the yield, quality, and environ-
pilot-scale packed-bed bioreactor (Pitol et al., 2016). mental viability of the extracted pectin and EOs were comparable on
Although CPW does not have a high protein content, the proteome experimental and semi-industrial scales (Fidalgo et al., 2016). Another
profile of 2.5-9.0% protein amount of citrus peel was reported to be novel extraction configuration, based on UAE and MAE, for biorefinery
composed of 1109 protein types, of which 366 proteins were found of citrus peel to obtain EOs and pectin was developed by Gonzalez-
solely in the peel and 46 in both the peel and the pulp (Matharu et al., Rivera et al. (2016). Their extraction process provided the advantages
2016). However, this small amount can negatively affect the costs of of faster processing and easy scalability, and the best configuration
enzyme isolation and purification, when the waste is used as the sub- decreased consumed energy by 27 times compared with hydrodistilla-
strate for enzyme production (Ravindran and Jaiswal, 2016b). To en- tion for EOs biorefining. The technology for total valorization of fruit
rich the protein content of CPW, thereby covering protein needs in and vegetable products using UAE and MAE is even more quickly ad-
animal and human nutrition, usually the production of microbial pro- vancing. A “dry” biorefinery concept without solvent or adding water to
tein, or so-called single cell protein, by SSF has been performed obtain EO, phenolic compounds and fibers, was recently introduced by
(Mamma and Christakopoulos, 2014). Jacotet-Navarro et al. (2016). EO and water were first extracted by
Besides industrial enzymes production, the growth of some micro- treating the waste with MHG, followed by UAE of the remaining cake
organisms, e.g., S. cerevisiae, Kluyveromyces marxianus, and kefir, on (using the constituent water) to extract other chemicals. Although the
various food waste can industrially valorize the waste by adding nu- method was used for the total valorization of ginger press cake, the
trient minerals, aroma volatile compounds, and protein. An example of authors here suggest that this method can be applied to CPW bior-
this method is flavor synthesis, e.g., “fruity” esters, ethyl hexanoate, efinery, as well.
and aroma compounds, acquired through industrial yeast strains via Although the complexity and sometimes the higher costs associated
SSF of orange peel, which was performed by Mantzouridou et al. with the MAE, rather than the conventional extraction methods, were
(2015). An option for the production of bioactive phenolic compounds considered as the main challenges of process industrialization, green
is via SSF of inexpensive agro-industrial residues. Bioactive compounds extraction techniques provide non-denatured extracts without produ-
are produced by different microorganisms as secondary products, after cing major environmental contaminants (Barba et al., 2016; Ciriminna
growth is complete (Martins et al., 2011). Mantzouridou et al. (2015) et al., 2016; Rombaut et al., 2014). A study on the economic feasibility
used Saccharomyces cerevisiae for SSF of orange peel waste to produce of orange peel valorization by MAE for the production of D-limonene
yeast flavor and other valuable chemicals. They obtained maximum and pectin on an industrial scale was conducted by Pfaltzgraff et al.
amounts of 253 and 3009 mg of volatile aroma esters and total poly- (2013). Assuming the use of at least 10,000 t of waste in a plant located
phenols, respectively, from each kg of fermented orange peel. Rossi near the waste generation facility, 152 and 1080 t of D-limonene and
et al. (2009) obtained a maximum amount of 99.60 μmol/LG total vo- pectin per annum were obtained, respectively. Estimating the total cost
latiles via SSF of citric pulp by using Ceratocystis fimbriata. of plant to be £4.7 million, a profit of £7.3 million per annum can be
obtained by selling the products. Nonetheless, to our knowledge, no
6. Integrated biorefineries of CPW: environmental considerations study was found in the literature regarding the environmental assess-
and engineering challenges of green chemistry ment of MAE for CPW biorefinery.
Integrated biorefineries for CPW using biochemical technologies,
Recently, different valorization strategies within the context of e.g., fermentation and anaerobic digestion, have also been developed,
biorefinery have been developed in order to stabilize lignocellulosic and the economic and environmental aspects have been assessed. In
wastes while producing valuable foods/feeds (Bateni and Karimi, 2016; most cases, green technologies coupled with a hydrothermal treatment,
Ciriminna et al., 2017). Most of these valorization strategies usually aiming at using less/no chemicals, are usually considered as a green
lead to producing individual products that are only marginally profit- process. To make better sense of the economic assessments, it is useful
able. Green chemical processes, e.g., green extraction techniques and to provide the price of the major products obtained in the biorefinery of
biochemical processes, for the biorefinery of CPW attempt process in- CPW (Fig. 3). In Fig. 3, the values on the x-axis represent market price,
tensification (see Fig. 1). First and foremost, green extraction methods no matter the sources from which they were obtained. An integrated
are eco-friendly; while, they have developed as powerful tools with the biorefinery is economically feasible if and only if the price of its pro-
purposes of improving extraction yield with a fast rate, increasing heat ducts remains as close as possible to market prices. The y-values are
and mass transfer, and ease of operation. As suggested by Budarin et al. global demands, in which non-renewable resources in most cases
(2015) and discussed earlier, MAE is one of these innovative techni- nowadays have high shares to provide them. An example of a cost-ef-
ques. Additionally, UAE and enzymatic-assisted extraction have been fective biorefinery approach for the valorization of CPW via hydro-
used as green extractions. They are usually solvent-free, which elim- thermal treatment (dilute-acid treatment at 150 °C for 6 min) and bio-
inates the risk of environmental concerns. While these techniques have chemical processes (i.e., fermentation and anaerobic digestion) was
proved to be potent, their use in an integrated biorefinery is rare. previously reported by Pourbafrani et al. (2010). This biorefinery led to
An example of an integrated biorefinery of orange peel waste based the production of 39.64 L ethanol, 45000 L methane, 8.9 L limonene,
on green and solvent-free extraction techniques to obtain EOs, poly- and 38.8 kg pectin from 1 ton of citrus waste (fresh weight basis).
phenols, and pectin, was described by Boukroufa et al. (2015). The Economic analysis of such a process for CPW biorefinery for production
biorefinery method used ultrasound (US) and microwaves (MW) as the of ethanol, methane, and limonene was then conducted by Lohrasbi
only energy sources, and in a closed-loop sustainable fashion, the va- et al. (2010). Ethanol production cost in this biorefinery was generally
luable compounds were obtained with high yields. They obtained up to reported to be sensitive to plant capacity and transportation cost from
24.2% pectin yield by microwave heating (500 W for 3 min) compared waste generation to the valorization facility, ranging from 0.46 to 2.55
with 18.32% pectin yield via conventional extraction (120 min). In the USD/L (Lohrasbi et al., 2010). A total 0.91 USD/L price of ethanol was
optimized condition of ultrasound power and temperature (i.e., obtained in a base case with 100,000 tons/year capacity and 10 USD/
0.956 W/cm2 and 59.83 °C) a polyphenol yield of 50.02 mg GAE/100-g ton transportation cost, indicating the economic feasibility of the pro-
was obtained. Moreover, up to 4.22% EO was obtained by microwave cess.
hydrodiffusion and gravity processing (MHG), comparable to that Aside from the economic considerations, environmental assessments

162
B. Satari, K. Karimi Resources, Conservation & Recycling 129 (2018) 153–167

methane for electricity production resulted in a 77% reduction in GHG

Methane emissions, compared with using natural gas.
1.300E+09 An integrated process for a pilot plant by using steam and citric acid
to produce p-cymene, hydrogen, and pectin from orange peels was
developed by Dávila et al. (2015), and techno-economic and environ-
1.299E+09 mental assessments were performed for the plant. The plant was also
Ethanol designed to produce electricity by gasification of the remaining cellu-
8.0E+07 lose, hemicellulose, and lignin from the process. Although electricity
7.0E+07
6.0E+07 production in the plant covered the energy requirements of the process,
5.0E+07 it generated negative environmental and economic impacts. Using 1
4.0E+07
3.0E+07 ton/h orange peel, production costs of 5.27 and 3.53 USD/kg for p-
2.0E+07 Acetic acid cymene and pectin, respectively, were obtained in the plant without
1.0E+07
Limonene electricity generation (Dávila et al., 2015).
8.0E+04 Pectin
6.0E+04 Taking everything into accounts for the biorefinery of CPW using
4.0E+04 green chemistry, it is very important to integrate the valorization
2.0E+04
0 200 400 600 800 1000 14200 14400 scheme, i.e., biowaste pretreatment, recovery of chemicals, and bio-
conversion processes. This is desirable not only because of the marginal
profitability of single-product valorization scheme, but also for the
Fig. 3. Market price versus global demand for some major value-added chemicals derived negative environmental impacts associated with new waste generation,
from citrus processing waste.
e.g., depectinized peel in current commercial pectin production plants
(Satari et al., 2017). Fig. 4. suggests a proposal for integrated bior-
of integrated biorefineries of CPW using biochemical technologies have efinery of CPW using green extraction techniques and biochemical
been performed. Cameron et al. (2016) developed a process via con- processes. This proposal will help to use the whole waste by avoiding
tinuous steam injection at 150 °C followed by steam-explosion to re- the production of byproduct residues, yielding an economically sus-
cover pectin, phenolic compounds, and some other secondary meta- tainable biorefinery by production of variety of chemicals, while re-
bolites from CPW. Meanwhile, the method is considered as an ducing the environmental footprint. However, as stated by Fava et al.
environmentally friendly approach, because it enhanced the recovery of (2015), the industry to develop these integrated processes is still im-
pectic polysaccharides and phenolic compounds. Pourbafrani et al. mature and primarily influenced by high processing costs. These
(2013) assessed the greenhouse gas (GHG) emissions associated with methods must be further examined and validated in order to be ap-
the biorefinery of CPW. Two configurations for the biorefinery were plicable on an industrial scale. Process intensification strategies and
considered: a large biorefinery with ethanol, methane, limonene, and optimization of the use of energy and water, optimizing recovery and
digestate as products, and a small biorefinery producing methane, li- improving product quality, and sustainability issues, should be prior-
monene, and digestate. Based on the results of the large biorefinery, itized to offset the high capital costs of integrated biorefinery plants.
using ethanol (E85) to displace gasoline in vehicle fueling resulted in a Finally, the most important consideration in integrated biorefineries
134% reduction in GHG emissions. In the second configuration, using on an industrial scale is the economic feasibility of the process. For

Fig. 4. An integrated biorefinery model for citrus processing waste

using green chemical technologies and biochemical processes.

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B. Satari, K. Karimi Resources, Conservation & Recycling 129 (2018) 153–167

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