Trends in Food Science & Technology 98 (2020) 1–9

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Trends in Food Science & Technology

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

Principles of halal-compliant fermentations: Microbial alternatives for the T

halal food industry
Ercan Karahalil∗
Akdeniz University, Department of Food Engineering, Antalya, 07058, Turkey

A R T I C LE I N FO A B S T R A C T

Keywords: Background: Microbial food ingredients produced using biotechnology have a wide range of applications in the
Microbial products food industry. With new technological improvements such as genetic modification, microbial products can be
Halal media produced more effectively. Microbial products and the new ways of producing them have led to some confusion
Genetic modification for consumers in recent years. Religions and lifestyles are determinative factors in the food consumption pre-
Chymosin
ferences of different societies. People who are followers of a religion or philosophy of life, such as Islam, inquire
Cochineal
about the microbial ingredients of the foods they consume. For Muslim societies, who follow Islam, it is critical
Gelatin
that microbial products match the criteria of the Islamic diet. Therefore, they require some basic principles that
must be followed in the production of bioproducts.
Scope and approach: The aim of this review is to summarize the basic principles of producing microbial food
ingredients that are used for halal foods.
Key findings and conclusions: To evaluate the steps of a fermentation process from an Islamic point of view and to
determine the control points for halal requirements would eliminate any questions about the foods that are
prepared using microbial metabolites. Nowadays, many biotechnology companies have invested in modifying
their production processes to comply with halal principles so that they can reach the halal food market. In the
future, it is expected that the share of halal microbial products will increase in the biotechnology market.

1. Introduction or halal principles (Fischer, 2008; Kwon & Tamang, 2015).

Religious beliefs and philosophies of life have a restrictive effect on
food consumption of their followers (Fay & German, 2008). In parti-
cular, religious attitudes are one of the decisive factors for consumer
behaviors in religious groups (Kwon & Tamang, 2015; Mukhtar &
Mohsin Butt, 2012). Muslims are one of the largest belief groups and
have a set of dietary rules. In Islam, The Quran (The Holy Book of
Islam) and The Hadiths (The Words of Prophet Muhammad), the two
fundamental religious texts, are taken into account to determine food
consumption preferences. Although there are many ideas and texts
presented by Islamic scholars, these two texts are of higher priority in
terms of degrees of acceptance and they provide some specific guide-
lines about which foods are proper to consume for Muslims (Armanios
& Ergene, 2018). Consumption of pork, dead carrion, blood, all blood
derivatives, alcohol and all harmful materials to human health are
forbidden and identified as haram (non-permissible) in Islamic termi-
nology. On the other hand, foods being free from these elements are
called halal. Evaluation of substances and methods that are proper to
Islamic dietary rules in food processing is defined as halal requirements
Foods that meet halal requirements have a significant economical
share of the global food market. Considering the increase in the po-
pulation of Muslim communities, which constitute about 25% of the
population in the world, the increase is foreseen to continue (Pew,
2017). In addition, it is also estimated that the size of the global halal
market, which includes other halal products such as pharmaceuticals
and personal care products, will reach $2.6 trillion by 2020 (Grand,
2018).
A right-to-know request for food consumption is one of the most
debated issues worldwide. To this end, people from different religious
groups prefer foods that are certified by agencies that investigate and
certify the foods based on principles of consumers’ beliefs. Muslim
consumers, one of the largest religious groups, require foods that do not
have any non-halal ingredients. However nowadays, some ingredients
that are used frequently in food production can belong to one of the
prohibited sources stated above (Al-Mazeedi, Regenstein, & Riaz,
2013). For example, some part of the total global gelatin and chymosin
production is derived from pigs, while most of the rest is from cattle
that were not slaughtered in keeping with Muslim religious

∗
Akdeniz University, Faculty of Engineering Department of Food Engineering, Antalya, 07058, Turkey.
E-mail address: ercankarahalil@gmail.com.

https://doi.org/10.1016/j.tifs.2020.01.031
Received 21 June 2019; Received in revised form 23 January 2020; Accepted 24 January 2020
Available online 31 January 2020
0924-2244/ © 2020 Elsevier Ltd. All rights reserved.
E. Karahalil
requirements for the slaughter of animals. Thus, foods that are pro-
duced with these ingredients are most likely considered haram. Cur-
rently, fermentation techniques to produce these components provides
a significant advantage to overcome possible confusions if the microbial
production is done in accordance with halal requirements. Moreover,
the interest in halal-certified food components has increased the de-
mand for halal microbial products and brought an advantage to pro-
ducers in market competition. Therefore, this growing demand moti-
vates biotechnology companies to cooperate with halal certification
bodies (Fischer, 2015).
Recombinant DNA technology is one of the most important devel-
opments for the production of microbial ingredients. It provides many
advantages such as high yield for the production of microbial products.
As for the Islamıc perspective, as long as the recombinant DNA tech-
nology that is used for genetically modified organisms (GMO) is com-
patible with halal principles, it is a key approach to increase the number
of halal bioproducts. Although there are still debates about factors such
as gene source and the necessity of modification, some recombinant
products have had halal approval for many years.
Some issues of biotechnology are still debated from a halal point of
view in addition to the more general concerns of the public, whereas
biotechnological applications are generally acknowledged as helping to
improve human well-being and to eliminate undesired situations like
diseases. For example, many vital components that are used in the drug
industry have been produced using GMOs. Such positive benefits of
biotechnology may make the use of biotechnology compulsory ac-
cording to Islamic belief (Peacock, 2010). In fact, biotechnology is a
good alternative to the production of additives and processing aids like
L-cysteine, gelatin and chymosin, which are still major sources of con-
troversy. In this way, halal ingredient producers can overcome some
difficulties such as low efficiency, high cost and the use of a limited-
number of raw materials (Al-Mazeedi et al., 2013).
Before and after any fermentation, a number of requirements should
be matched to ensure halal status of bioproducts. Growth media com-
ponents found in agars, agents such as antifoam agents added during
fermentation, and substances used for procedures done after the fer-
mentation period are critical, with those of animal origin. Therefore,
while developing fermentation media formulations, halal requirements
should also be considered in addition to other factors, i.e., sustainable
quality, easy availability, and cost (Dodge, 2009; Piggott, 2002).
Understanding control points in microbial production can provide
an increase in the range of halal food products. This review is under-
taken to address the stages of microbial production and to present
general guidelines that should be followed to ensure that the final
product is halal. Genetic modification (GM), one of the key points in
bioproduction, is evaluated from an Islamic perspective. Also, microbial
substitutes can become alternatives to some compounds which create
concerns in terms of their origins and processing methods for halal
compliance.
2. Fundamental principles for halal bioproduction
Fermentation processes, which are used to generate high value-
added products, are basically composed of upstream (preparations be-
fore fermentation) and downstream (treatments after fermentation)
steps. While doing these steps, some specific principles should be con-
sidered if the goal is to produce halal microbial products. A foodstuff
that contains microbial ingredients is evaluated according to whether it
is produced complying with halal principles. The following control
points must be considered in the production of halal bioproducts: (i)
microorganisms’ source, (ii) microorganisms' growth medium, (iii)
fermentation process, (iv) downstream processing, and (v) packaging
and labeling. Meanwhile, since halal requirements prioritize the pro-
tection of human health at any stage of fermentation processes, mate-
rials that have been scientifically proven to have an adverse effect on
human health cannot be accepted by Islamic rules (Qaradawi, 1994).
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Trends in Food Science & Technology 98 (2020) 1–9
That is why the necessity of using healthy materials is not emphasized
separately in the steps above.
2.1. Microorganisms
It is well known that microorganisms can be isolated from a wide
variety of environments such as leaves, fruits, soil, water, milk. To
employ microorganisms that are obtained from a halal and hygienic
environment in fermentations is a critical prerequisite to have a final
halal product. Fermentations done with microorganisms that are iso-
lated from non-halal sources like blood, animal feces, and dead animal
body parts, etc. are non-halal. For example, it has been reported that
some probiotic bacteria, antimicrobial reuterin and non-steroidal es-
trogen-secreting bacteria that are isolated from pigs should not be used
for halal microbial production (Kurniadi & Frediansyah, 2017). How-
ever, many studies carried out with haram-origin microorganisms are
available in the literature. To produce proteases, amylase, pectinase,
xylanase, cellulase, lipase, and ligninase with the aim of industrial use,
many microorganisms were isolated from various environments are
included dead animals, animal fecal sediments, freshwater ice, soil,
sediment, algae, plants, rocks, and microbial mats (Loperena et al.,
2012). Similarly, some lactic acid bacteria strains (LAB) were isolated
from human feces and their functionality was investigated using them
for fermented products containing various vegetables (Park, Lee, Kim, &
Shin, 2002). In another study with LAB, Zamora, Carretero, & Pares
(2006) compared spray- and freeze-drying dehydration technologies in
the long-term preservation of 12 LAB cultures isolated from porcine
blood. As considering these two studies, certifiers need to determine if
non-halal-origin microorganisms can be used directly to carry out a
halal-compliant fermentation. There do not seem to be any studies that
indicate whether microbes from filthy sources can become halal after
multiple generations in halal-based media.
GM is another topic of confusion: whether it is an appropriate way
of selecting a microbial strain for a halal-based fermentation. Gene
source, status of final product and long-term potential effects on human
health are generally discussed to evaluate GMO from the perspective of
Islam. Therefore, with the aim of eliminating potential doubts about
gene sources, some researchers (Abdullah, Ma’Radzi, Saleh, Kamal, &
Yaacob, 2011) have declared that mix cultures where GMO can be
found should not be used unless their gene origins are known. And they
suggested that it is preferred that the microorganisms are only derived
from halal-based sources.
2.2. Growth media for inoculum preparation
The content of the growth medium should also be approved as halal
in addition to the microorganisms. To promote microbial growth, some
materials containing non-halal elements are commonly used as growth
media. For example, brain heart infusion broth and brain heart infusion
agar are used to grow microorganisms. They can contain pork gelatin,
pork brain, and heart derived tissues. In a study, Corynebacterium glu-
tamicum that is used for the production of L-ornithine was developed in
a growth media containing brain heart infusion (Kim, Lee, & Lee, 2015).
In another study, an amylase production was done using by Bacillus
licheniformis MTCC 1483 using solid-state fermentation technique and
brain heart infusion broth was used (Kaur, Kaur, Kaur, & Sondhi, 2017).
Another non-halal ingredient that is used to develop a starter culture is
blood, which are used to grow bacteria, molds and yeast (Kurniadi &
Frediansyah, 2017). For example, Acinetobacter baumannii as a cell
factory was developed using a bloody agar to produce an inulinase
enzyme (Muslim, Ali, Salman, Al Kadmy, & Muslim, 2015). In another
study, Pourzardosht and Rasaee (2017) cultivated Streptococcus zooe-
pidemicus in a bloody broth with the aim of producing hyaluronic acid.
It was also reported that fish blood that contains digested protein was
used to prepare starter cultures in the production of some fermented
foods (Fanous, 2010). The addition of the microorganisms to the
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fermentation medium, which is termed inoculation, is another neces-
sary procedure to start a fermentation process. Several emulsifiers, that
are fat-based such as polysorbates, can be used during inoculation. For
example, tween 80 (also known as polysorbate 80) was often used to
prepare inoculum solution (Karahalil et al., 2017; Karahalil, Germec,
Karaoglan, Yatmaz, Coban, Inan, et al., 2019). The origin of such ma-
terials needs to be checked carefully. After incubation, microbial cul-
tures that are obtained from growth medium can be stored for a long
time at −80 °C with cryoprotective agents. Glycerol, lactose, skimmed
milk powder, and whey are the most commonly used cryoprotectants
for this purpose (Alonso, 2016). Apart from these, active carbon is also
being used for the preservation of microorganism, though it is essen-
tially applied as an agent in the clarification of fruit juice and treatment
of water. Active carbon can be produced from animal sources in addi-
tion to plant-based materials. In some studies, it has been reported that
active carbon was used as a carrier material for the long-term pre-
servation of sensitive microorganisms since it provides high genetic
stability and preservation of viability during storage by lowering the
degree of freezing of cells with its thermal properties (Alonso, 2016;
Malik, 1990). These animal-origin agents, which can be applied in
single or different combinations, should be halal-approved.
2.3. Fermentation media
Fermentation media is a controlled environment in which microbial
productions are done. As a principle, some nutrient components must
be found in fermentation media for microbial growth and product
synthesis. Two major group of nutrients that are added to the medium
are carbon and nitrogen sources. Many materials including animal-
based substances are used as a carbon source for fermentations. For
example, Lopes, Gomes, Silva, and Belo (2018) prepared microbial oils,
citric acid and lipase using Yarrowia lipolytica W29 with lard as the
substrate. In another study, microbial red pigments were produced from
glycerol using Monascus ruber CCT 3802 in submerged fermentation
(Meinicke et al., 2012). Nitrogen can also be obtained from animal
sources, the origin of them must be known. Nitrogen sources such as
meat extract, meat peptone, and hydrolyzed protein should not be de-
rived from blood, animals that are not halal, non-halal slaughtered
cattle. Some tryptones that are digested with porcine-derived trypsin
enzyme cannot be used if the aim is to produce halal bioproducts.
Traditionally the slaughter by Ahl al-Kitab (an Arabic term for people of
the book, mainly Muslim) was considered appropriate for centuries.
However, Islamic authorities from various Islamic schools (Sunni,
Shiite, etc.) have become more restrictive about the religious identity of
the slaughterer due to concerns about non-Islamic preslaughter and
slaughter methods (Armanios & Ergene, 2018). However, Jewish
slaughter of animals is identical to Muslim slaughter although a prayer
is said over a group of animals rather than over each animal
(Regenstein, Chaudry, & Regenstein, 2003). Efforts have been suc-
cessfully made to have the Jewish slaughterman say the Muslim bles-
sing at the time of slaughter.
In recent years, low-cost materials have been used with the potential
to enrich the fermentation medium rather than expensive and high-
purity resources to minimize fermentation costs in biotechnological
studies. Slaughterhouse wastes, that are either raw or processed, are
used as an economical group of materials for this purpose. Meat meal,
bone meal, feather meal, meat-bone meal, blood meal, and animal bone
char are some of the materials that have been used to improve product
yield (Nikolay et al., 2013; Turhan, Bialka, Demirci, & Karhan, 2010;
Villa et al., 2013; Yatmaz et al., 2016). Whey has been also used as a
nitrogen source in the fermentation processes to produce microbial
products that are used in foods (Germeç et al., 2019; Karahalil, Germec,
& Turhan, 2019). These media enrichment elements, which have high
nitrogen content, should be derived from a permissible source.
Sulaiman, Othman, Baharuddin, Mokhtar, and Tabatabaei (2014) as-
serted that halal microbial production could be more credible if the
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Trends in Food Science & Technology 98 (2020) 1–9
wastes that are generated in halal food plants were used as substrates.
2.4. Fermentation process
Fermentation equipment such as bioreactor vessels in which fer-
mentations are to be carried out should be appropriate. An assurance is
needed that no impurities that violate the halal status of the fermen-
tation remain due to previous uses of the equipment (Al-Mazeedi et al.,
2013). After a fermentation process, microorganism residues, fer-
mented media, and the residues that result from target products and by-
products are impurities that may occur. To prepare it, it can be sub-
jected to autoclaving and washing operations. Additionally, the
cleaning procedures applied to bioreactors and their probes depend on
precisely what was done with them in the previous fermentation pro-
cess. In some plants, kosher-compliant fermentations are also done in
addition to halal bioproduction and a ritual cleansing procedure is
applied to provide kosherization. As a requirement of this procedure,
the equipment is cleaned thoroughly with soaps, and detergents prior to
keeping inactive for 24 h. In the last step, the system is flooded using
hot water or steam under the supervision of a kosher inspector (Al-
Mazeedi et al., 2013; Fischer, 2015).
In addition to media ingredients, some agents can also be added to
the media for various functionalities during fermentation. For example,
Rahim, Hasan, Harith, and Abbas (2017) added gelatin to the fermen-
tation medium to maintain the microbial growth against the negative
effects of mechanical strength. Enzymes are also added to media as
processing aids. In some studies, enzymes were used to reduce complex
substrates (agroindustrial wastes, etc.) into more basic components
before fermentation since they can then be consumed more easily by
microorganisms (Turhan et al., 2010). Another noteworthy point to
consider for a fermentation process is foam formation, which limits
product secretion and makes media vulnerable to microbial con-
tamination. To overcome this problem, antifoam agents are used, which
may be made of synthetic materials or animal substances such as blood
serum or fat derivatives. These processing aids should be halal certified.
In fermentation processes, various techniques might be used to
obtain high-yield and low costs. One of them is the immobilization
technique which is used to ensure that the cells can be used repeatedly
and are not adversely affected by physicochemical changes (pH, tem-
perature, etc.) in the fermentation media. It is based on the principle of
restricting the movement of microorganisms and enzymes using poly-
meric support materials and is commonly used. Some of the support
materials used for immobilization are of animal origin. Animal protein-
based polymers such as gelatin, and inorganic adsorbents including
activated charcoal and charcoal bone, have to be halal-approved. Of
protein-based polymers, casein or whey proteins obtained from whey
that occurs during cheese production with non-halal based enzymes
should be also checked for halal assurance (Alonso, 2016; Datta,
Christena, & Rajaram, 2013; Qureshi & Maddox, 1995). Another
strategy that is frequently used in fermentation processes is a biofilm
technique, which has been developed to allow the use of microorganism
more than once. The biofilm technique used bioreactors with special
tubes with special tubes called plastic composite support materials
(PCS) fixed to its agitator shaft. PCS have been used for fermentations to
produce lactic acid, lysozyme, pullulan, etc. (Cheng, Demirci, &
Catchmark, 2011). The composition of PCS depends on the fermenta-
tion requirements, and they can be contained various ingredients.
However, the use of PCS that include bovine albumin and red blood
cells makes the halalness of these (Ercan & Demirci, 2015; Germec,
Yatmaz, Karahalil, & Turhan, 2017).
2.5. Downstream processing
In downstream processes, impurities are eliminated to isolate the
target product from the fermented medium. These treatments usually
require the addition of some materials as filter aids, flocculating agents,
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buffer salts, acids, and bases. Filters and flocculants that are used in
downstream processes should satisfy halal requirements (Dodge, 2009).
Some chemical flocculants only be used limitedly for the purification of
halal bioproducts because they have an adverse effect on human health,
although widely used in non-food flocculation procedures (Wibisono,
Sucipto, Perdani, Astuti, & Dahlan, 2018).
Activated carbon and bone char are agents that can be used to re-
move some impurities present in the fermented media (Qureshi &
Maddox, 1995). Activated carbon can be used in slurry form, packed
columns and applied singly or in combination with Celite (Gonçalves,
2011). Activated carbon columns are frequently used to recover oli-
gosaccharides and to remove salts, coloring matter and other impurities
from culture media (Mûkhtar & Ijaz, 2014; Sarhaddar, Scheibl,
Berghofer, & Cramer, 1997). Although activated carbon is mainly
produced from vegetable materials mostly, some still is produced from
animal sources (bone, etc.). The world's leading active carbon suppliers
have received approval certificates from various halal certification
bodies in different regions of the world to assure their Muslim custo-
mers' demand (Wibisono et al., 2018).
2.6. Packaging and labeling
Standardization agents, preservatives and packaging materials that
are used for preparing a halal final product, need to meet halal re-
quirements. It is a must to know the origins of materials that are used
for packaging that may be obtained from animal by-products, such as
stearates, and coating materials (Ermis, 2017). Another material that
needs to be checked is stabilizer agents such as bovine serum albumin
that is used to prepare the final product in powder form by freeze-
drying (Srirangsan, Kawai, Hamada-Sato, Watanabe, & Suzuki, 2011). If
packaging materials that are not obtained from appropriate sources are
used, which may lead to concerns about the halal status of products
since the materials that contact food directly may migrate into the
products. Riaz and Chaudry (2018) suggested that several label mate-
rials (paper, plastic-based ones, etc.) that are used directly on food
products’ packaging may migrate into foodstuffs in minute quantities
and this should be taken into consideration by halal-certifying agencies
in the process of certifying. Apart from that, use of the statement of
“halal” on the label without receiving any certificate from a halal or-
ganization, is an important problem for Muslim consumers wanting to
obtain a real halal product. However, it is not possible for consumers to
learn whether substances such as processing aids that are not required
to be stated on the label were use or to know the halal status of the
equipment used. Therefore, the safest way is to be assured that the
products comes from a credible halal organization. Likewise, halal food
manufacturers should only use ingredients that are certified by a re-
cognized halal certification body. On the other hand, Askomi, Yusop,
and Kamarulzaman (2018) reported that halal logos and signs are used
for non-certified products in some countries. To prevent potential vio-
lations in halal-labeling, some novel approaches such as QR code and
barcode are benefitted in recent years. Mobile applications with such
novel approaches work connecting the databases of halal organizations.
Thus, halal-conscious consumers can easily learn whether a halal-la-
beled product really has been certified by that agency using a mobile.
3. Genetic modification technology from an Islamic perspective
and its potential use in fermentation processes
Genetic modification (GM) is a gene transfer that is carried out to
transfer a gene from one living thing to another. Genetically modified
foods are the foods that are processed by a GMO (Majid, Abidin, Majid,
& Chik, 2015). Genetic engineering and biotechnology create oppor-
tunities for expanding the supply of new foods making changes in
specific characteristics of traditional foods (Ziegler, 2007). Further-
more, it is asserted that GM technology has many advantages such as
reducing the use of pesticides and herbicides, achieving a sustainable
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Trends in Food Science & Technology 98 (2020) 1–9
yield, providing an increased yield in agriculture and animal hus-
bandry, and decreasing hunger problems (Akhmetova, 2016;
Muhammad, 2010). Microorganisms are also genetically modified and
used in fermentation studies to provide high yields, to limit or com-
pletely inhibit unwanted by-products. Despite all its advantages, GM
food is being challenged by some groups in different countries with
religious and ethical concerns (Atalan-Helicke, 2015; Brown, 2011). It
has been also discussed in Muslim societies for a long time. Despite
these debates, almost none of the halal certification organizations and
Islamic authorities entirely object to the use of GMOs. Decisions on the
GMOs were made substantially while the status of genetically modified
plants is still discussed. The discussions of the fermentation processes
that are done with GMOs and evaluation of recombinant bioproducts as
food ingredient can be categorized under 4 headings: gene source, gene
transfer between different living species (from bovine to plants, from
animal to microorganisms, etc.), effects of the final product on human
health and environment, and the necessity of GM.
It has been reported that if a gene derived from non-halal donors
like pigs is propagated artificially and transferred to a halal host, the
microbial final product is not accepted as halal. (Che Man & Sazili,
2010). Nevertheless, several researchers raised the issue that the em-
ployment of fully synthetic genes that have really no porcine material,
needs to be addressed by Islamic scholars (Regenstein, Chaudry, &
Regenstein, 2013; Riaz & Chaudry, 2003).
As a gene donor, plants are the most reliable one for gene transfer
between different living species since they have no restrictions in the
aspect of halal requirements as long as they are non-toxic. Even if genes
from animal sources are transferred to an approved host, they are
questioned whether they are forbidden animals or not. Also, as long as
the gene to be transferred is obtained from allowed animals, it is not
considered whether the animal is alive or dead (Institution, 1997;
Khattak et al., 2011). On the other hand, the necessity of doing long-
term toxicity tests for recombinant metabolites is emphasized by Is-
lamic authorities constantly. Although some concerns about health
were put forward, it was reported that no adverse effect on health has
been detected to date in the use of GM technology for microorganisms
according to some current publications (Blair & Regenstein, 2015;
Csutak & Sarbu, 2018). As a key point is that the reason for using GM is
important for halal status. Islamic belief undoubtedly supports bio-
technological studies that contribute to the prosperity of mankind po-
sitively. Namely, gene transfer processes need to provide a benefit such
as high efficiency or low cost, in addition to being compatible with the
gene requirements stated above. However, some genetic researches are
done using GM just with the purpose of designing fishes with different
colors. Because such studies aimed to achieve only a visual pleasure,
these kind of GM performance are considered as controversial from the
Islamic perspective (Gong et al., 2003; Tonelli et al., 2017).
Overall, despite some challenges, the genetic modification which is
made compatible with halal requirements can offer competitive alter-
natives for the halal food industry.
4. Microbial alternatives to some questionable ingredients in
terms of halalness
A significant share of the global production of some ingredients
(gelatin, L-cysteine, etc.), which have various functions in food pro-
cessing, is produced from non-halal sources. The use of these in-
gredients in food processes has created debates for the halal status of
those manufactured-foods. Animal and plant-based sources have var-
ious disadvantages in the production of halal ingredients. Animal
sources lead to concerns due to their origin problem while plant-based
ones can be produced limited titer owing to the problem of low yield.
Hence, researches on potential sources for halal food production has
gained importance. Microorganisms, which have become a more effi-
cient resource with the recombinant DNA technology, have been a re-
markable option for halal producers in recent years. Considering that
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Table 1
Summary of studies considering halal requirements.
Publication title
Production of effective microorganism using halal-based sources: A review
Use of hydrolysates from yellowfin tuna (Thunnus albacares) heads as a complex nitrogen
source for lactic acid bacteria
Production of cysteine: Approaches, challenges and potential solution
Determination of natural carotenoid pigments from freshwater green algae as potential
halal food colorants
Hydrolyses of meat and soybean proteins using crude bromelain to produce halal peptone
as a complex nitrogen source for the growth of lactic acid bacteria
microbial production has many advantages (fast-growing of micro-
organisms, high productivity etc.) comparing other ingredient sources,
it is clearly seen that its products can be a good substitute in terms of
providing low cost and being easy to reach, for processing aids such as
pepsin, lipase, and gelatin that are derived forbidden animals. From this
perspective, biotechnology is a key technology that offers alternatives
for halal food industry. With recent advances, many organic compounds
can be produced by biotechnological processes. Some researchers have
produced halal microbial products and media to be used in halal fer-
mentations, as given in Table 1. Overall, the most needed ingredients
from microbial substitutes for halal food production, are (i) protein-
based ingredients, (ii) red colorants and (iii) aromas (Hartel, Joachim,
& Hofberger, 2018; Riaz & Chaudry, 2018).
4.1. Protein-based ingredients
Many protein derivative compounds are used for different purposes
in the food industry. Particularly, low-cost materials are preferred to
reduce the cost of protein production. Among the low-cost materials,
animal sources have a major share as a raw material in the production
of protein-derivatives. As an animal by-product, whey is a valuable
protein source. Its total production worldwide is estimated at around
180–190 million tons annually (Ranganathan, Chauhan, Gokul,
Vijayalakshmi, & Shanmugam, 2018). However, for halal assurance,
enzymes that are used while producing whey (namely cheese) should
not be derived from forbidden sources. This is a major point for halal
certification because an important part of whey is used in the food
industry. Except whey, blood and other slaughterhouse wastes are
considered as a low-cost source for the protein production due to their
occurrence in massive quantities in the worldwide. It is reported that
blood is used for different purposes in the food industry such as strong
gel formation and high emulsification, etc. (Álvarez, Bances, Rendueles,
& Díaz, 2009). Therefore, some companies have developed and pa-
tented some food additives derived from blood (Ofori & Hsieh, 2012).
Another problem is to use blood-derived proteins as processing aids,
which are used in the food industry for many functions without the
necessity of stating on the label. Also, these derivatives can be involved
in food, such as supplementing foods with blood-derived proteins in-
stead of more valuable proteins. To fight these frauds, alternative
methods of analysis have been studied in several countries (Jiang,
Fuller, Hsieh, & Rao, 2018; Lecrenier et al., 2016). Islamic authorities
do not approve the usage of blood in food production because the
physicochemical structure of crude blood or processed derivatives does
not alter completely during food processing (Kashim et al., 2017). It is
reported that 30% of total blood released in the world is used in the
food industry and approximately 15% of total blood is processed to
produce protein (Ofori & Hsieh, 2012). These issues lead to doubts for
Muslim consumers. As a solution for halal food production, bio-
technology provides the following alternatives for protein-based in-
gredients:
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Trends in Food Science & Technology 98 (2020) 1–9
Aim of study Reference
Production of halal-based media for Abdullah et al. (2011)
microbial growth
Production of a nitrogen source for Safari et al. (2012)
halal media
Production of halal cysteine Ismail et al. (2014)
Production of halal carotenoid Othman, Noh, Nurrulhidayah, Hamizah, and
pigments Jamaludin (2017)
Production of a nitrogen source for Utami, Kusuma, Satiti, Rahayu, and
halal media Cahyanto (2019)
4.1.1. Single cell protein
Animal sources except for wastes are a high-cost raw material for
protein production, this led to that researchers investigate alternative
protein sources. To this end, researches have focused on insects, plants
and microorganisms to produce a protein with low cost and high
amount. Nevertheless, in Islamic dietary rules, except locust which is
generally accepted to be halal by Hadiths, all insect-like creatures are
not the same for Muslims. For example, Shiism, which is the Islamic
school constitutes more than 10% of all Muslims population, does not
support the use of any insects. The Hanafisim, one of the most common
Islamic schools, considers as makruh (unpleasant despite certainly not
forbidden). Therefore, there is a lack of consensus between different
Islamic schools about insects (Armanios & Ergene, 2018). That is why,
the problem of low yield in the production of plant-based ingredients
and the lack of consensus of Islamic authorities in the halal status of
insects have made the use of microbial proteins more advantageous for
the halal food industry (Van der Spiegel, Noordam, & Van der Fels-
Klerx, 2013; Van Huis, 2013).
Single Cell Protein (SCP) is a considerable alternative offered by
biotechnology for the consumers that avoid blood and porcine origin
proteins. The aim of the production of SCP is to obtain biomass (cell
mass) at as high. Contrary to many fermentations, the target product of
SCP fermentation is the microorganism itself. Through this aim, bac-
teria, fungi, yeasts and some species of algae can be used in submerged
and solid-state fermentations (Nalage et al., 2016; Ravindra, 2000).
Despite some studies reporting that SCP consumption leads to gastro-
intestinal issues (Dzeladini, Chan, & Kummerow, 2017; Ravindra,
2000), it has been declared that SCPs can be used in food compositions
if some elements (contaminants such as heavy metals, nucleic acids that
lead to a lack of urease in human metabolism, etc.) can be removed
from SCP following microbial production (Ravindra, 2000). Mycopro-
teins, which are a kind of SCP, are detected to be a high-quality protein
type similar to milk protein in studies that are done with volunteers.
Further, mycoproteins have physiological benefits such as decreasing
total and low-density lipoprotein cholesterol levels, enabling a sense of
satiety, and reducing glycemic index when present in carbohydrate-rich
foods (Finnigan, Needham, & Abbott, 2017). The USA, the European
Union countries and South Africa have given the necessary legal ap-
provals to some companies for the past 30 years to sell foods, which are
enhanced with mycoproteins that are produced from the cytoplasm of
microorganisms like Fusarium venenatum. Foods enriched with myco-
proteins have been approved also by some halal certification bodies
(Asgar, Fazilah, Huda, Bhat, & Karim, 2010; Miller & Dwyer, 2001).
4.1.2. Gelatin
Gelatin is a term used to describe a protein group that has not found
in nature. It is derived from collagen, which is a protein-based structure
found in animal connective tissues. Gelatin has various functions such
as gelling and thickening in the food industry (Boran & Regenstein,
2010). The most used sources in food-grade gelatin production are
porcine skin (46%), bovine skin and hides (29%) and porcine and bo-
vine bones (23%), respectively (Duconseille, Astruc, Quintana,
E. Karahalil
Meersman, & Sante-Lhoutellier, 2015). As a promising gelatin-type for
the halal food industry, fish gelatin was manufactured approximately
350.000 tons annually, corresponds to an economic value of $2 billion
(Boran & Regenstein, 2010). However, fish gelatin has a small share in
the total production of gelatin for the present though used commer-
cially. Additionally, in some studies, insects (Mariod et al., 2011;
Mariod & Fadul, 2015) and frogs (Tümerkan, Cansu, Boran, Regenstein,
& Özoğul, 2019) have been proposed as a new source for gelatin pro-
duction. Gelatin is one of the most needed ingredients for the halal food
industry, however, the origin issue of gelatin leads to concerns for
Muslim consumers. In recent years, advances in genetic engineering
have allowed microbial production of gelatin, nevertheless it is not
commercialized yet (Rutschmann, Baumann, Cabalzar, Luther, &
Hennet, 2014; Werten, Eggink, Stuart, & de Wolf, 2019). Hence, studies
are done to produce food-grade recombinant gelatin using bovine col-
lagen in a variety of microbial expression systems. Furthermore, in the
production of recombinant gelatin, the use of gene fragments in desired
lengths and in different compositions makes it possible to produce a
standard quality gelatin. To sum up, recombinant gelatins produced
using a halal gene source have become a potential source for halal
gelatin since it both eliminates concerns such as slaughter type and
allows to be produced in a sustainable quality (Shah & Yusof, 2014).
4.1.3. L-Cysteine
L-cysteine is a sulfur-containing amino acid. It is widely found in
nature and commonly used in the food, pharmaceutical and cosmetic
industries. Nevertheless, many sources that found cysteine are not
feasible to manufacture L-cysteine in high amounts. Through this pur-
pose, human hair and animal feather hydrolysis methods have been
used to produce L-cysteine in industrial-scale for many years. With
considering the halal requirements, it is forbidden for Muslims to
consume the foods that are processed with additives derived from
bristles and any dead animals, human hair, and the feathers obtained
from animals not slaughtered with Islamic rules. The Muslim Consumer
Group (a halal organization in the USA) declared that L-cysteine can be
obtained from permissible animals such as chicken and duck feathers
while they are alive or slaughtered with Islamic rules. Also, Regenstein
(2012) reported that sheep wool as a cysteine source can be used if it is
sheared from alive sheep.
Researches on the L-cysteine production by fermentation have in-
creased in recent years. Some industrial processors make large-scale
cysteine production with bacteria that have a regulated metabolism.
The cysteines that are produced by microbial producers are certified by
local organizations in many countries, especially the USA, Germany,
and China (Wacker, 2007). Moreover, 90% of the cysteines that are
produced by fermentation can satisfy the aspect of quality standards the
food and pharmaceutical industries. In another study, it was reported
that production costs of microbial L-cysteine are lower compared to the
conventional methods (Ismail, Hashim, Jamal, Othman, & Salleh,
2014).
4.1.4. Chymosin, pepsin and lipase enzymes
Enzymes, one of the most widely used components of the food in-
dustry, can be obtained from animals, plants and microbial sources.
Plants as enzyme source are generally regarded as safe from the Islamic
perspective whereas it is crucial to make sure that animal enzymes are
not isolated from a prohibited animal. For example, a significant share
of the total world production of lipase enzyme that is used in lipid
modification is of porcine origin (Amid, 2015). Similarly, chymosin and
pepsin, which are used as coagulants in cheese production, can be ob-
tained from animals that are prohibited, or animals not slaughtered by
the Islamic method. However, Muslim societies demand all products
that they consume to be derived from halal sources, and microbial
enzymes are seen to be a safe option. As stated above, safe micro-
organisms should be used to produce food-grade microbial enzymes.
Recombinant chymosin has been adopted as a good alternative by
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Trends in Food Science & Technology 98 (2020) 1–9
Islamic scholars and it is the first halal-approved recombinant product
(Amid, 2015; Riaz & Chaudry, 2003). It can be produced using ge-
netically modified microorganisms, which are developed using genes
from calf, camel, goat, etc. In recent years, microbial chymosin has been
comprised of 70–80% of total chymosin production (Yegin & Dekker,
2013). It is also reported that metabolites such as enzymes, which fulfill
halal requirements, create opportunities for their producers to increase
their market share. That is because, the halal food industry has a con-
sumer group which expands massively in recent years. The products
manufactured by this industry, may also be preferred by secular con-
sumers. On the other hand, the companies which do not make pro-
duction in halal conditions could have challenges in drawing attention
of Muslim consumers (Fernandes & Carvalho, 2017; Taylor & Linforth,
2002). This encourages big companies to invest for halal bioproduction.
Novozymes, a major processor company of microbial enzymes, has
agreed with IFANCA (Islamic Food and Nutrition Council of America, a
halal certification body in USA) to meet the demands of the Muslim
consumers and has adapted its production procedures. Routine audits of
its plant in Denmark are carried out by this organization. Novozymes
has a revenue of around $ 2 billion annually with contributions of halal
and kosher (means permissible food, drug etc. for Jews) bioproduction
(Fischer, 2015). Besides, if a company that is engaged in production
under halal conditions request to experience a new component or
method, they have to consider the requirements of its contracted halal
organization. From this view, it is indicated that certification bodies are
effective in innovative approaches that are developed by companies
(Fischer, 2008). Another point, microbial chymosin should be able to
compete with the haram derivative ones in terms of productivity as well
as being non-contaminated with any prohibited substances. Elbarbary
et al. (2010) compared porcine pepsin with microbial rennet obtained
from Rhizomucor miehei in the enzymatic digestion of commercial calf
lactoferrin. The results of the study showed that microbial rennin can be
a good substitute for porcine pepsin in terms of technical properties. In
the same study, the lactoferrin hydrolysates that can be used in halal
food formulations were produced.
GRAS (Generally Recognized as Safe) as a basis for the regulations
in the United States, is considered as an important factor all over the
world when deciding whether an enzyme can be used with food. Even if
an enzyme has GRAS (generally recognized as safe) status, this is not
enough for a halal assurance. Although GRAS status considers such
criteria as health and environmental protection, it is not fully compa-
tible with halal requirements. Such as, to approve the pepsin enzyme
originating from porcine as safe is one of the divergences between halal
and GRAS status (Administration, 2000a).
4.2. Red color substances
Colorants are additives used in many areas of the food industry.
Color substances, which are classified as synthetic and natural, are
preferred depending on meeting the requirement that they protect
human health and they are compatible with Muslim consumers’ pre-
ferences. Although synthetic colorants are generally more stable than
natural ones, many synthetic colorants were banned by some European
countries, USA, Canada and Japan as they lead to carcinogenic and
mutagenic effects. For example, carmoisine, which is a red synthetic
colorant, is prohibited for use in foods in Sweden, the USA, Japan, and
Canada. Similarly, any kind of use of synthetic colorants in food in-
dustry is not permitted in Norway (Dikshit & Tallapragada, 2018;
Hartel et al., 2018). Although many synthetic colorants have halal ap-
proved, natural alternatives are drawing more attention. Natural color
enhancers have been preferred more in food industry due to consumers'
trends towards natural products in recent years. It is projected that
natural colorant market will grow at a rate of 6.2% annually for the
period of 2015–2019 and to reach $ 1.7 billion by 2020 (Cortez, Luna-
Vital, Margulis, & Gonzalez de Mejia, 2017; Rodriguez-Amaya, 2019).
Despite all, some natural color agents are not exactly appropriate for
E. Karahalil
human health and consumer preferences (veganism, religious concerns,
etc.). Blood, a natural color enhancing agent that is used to give a bright
red color to food sauces, can lead to some health problems. For ex-
ample, in a study, hepatitis E RNA was detected in crude porcine blood
that is prepared for use in meat products, and it was declared that these
foods may also be carriers of hepatitis E virus (Boxman et al., 2017;
Ofori & Hsieh, 2012). Considering such studies, it is clear that blood is
not a good option as colorant for halal production due to following two
reasons: it has some potential health risks and it does not compliant
with the halal requirements. Another red colorant that is used as a food
additive is cochineal. Cochineal is obtained by ethanol extraction from
an insect that is called Dactylopius coccus Costa. Carminic acid, which is
the active substance of cochineal, is found about 2% in the extract
(Hartel et al., 2018). Such as blood, cochineal can also be used limitedly
due to its origin and lead to some health problems such as allergic re-
actions and asthma (Müller-Maatsch & Gras, 2016; Voltolini, Pellegrini,
Contatore, Bignardi, & Minale, 2014). Sigurdson, Tang, and Giusti
(2017) reported that the poor consumer perception of the insect source,
potential allergenicity associated with insect protein, and relatively
high cost are the restrictive factors for the use of cochineal. In addition
to these factors, the lack of consensus of Islamic schools on the halal
status of insects is a crucial disadvantage for use in halal food pro-
duction. Therefore, investigations on alternative methods and sources
to produce new colorants have become more important.
Microbial color agents obtained by fermentation are an alternative
to plant, insect and synthetic-based colorants. They are of great re-
levance because of their high yields compared to other sources.
Contrary to the seasonal limitations of plant-based sources, pigment-
producing microorganisms are always present in nature. Furthermore,
microbial colorants can be produced from various microorganisms
(yeast, bacteria, fungi and some algae species) in high amounts.
However, it has been reported that single-celled algae or fungi (espe-
cially Ascomycetous species) is preferred more to develop new micro-
bial colorants due to their production capability at the industrial-scale
(Nigam & Luke, 2016). Additionally, the reduction of process costs
using low-cost substrates for generating colorants has increased the
interests of biotechnology companies. Some companies have commer-
cialized Natural Red color agent that is synthesized by Penicillium ox-
alicum (Dufossé, 2018). New microbial pigments have been developed
every year. That is why microbial red colorants can be a promising
alternative if they are produced abiding by halal requirements.
4.3. Aromatic compounds
In aroma production, some suppliers take into account halal re-
quirements in addition to other quality standards. Global companies
have made this adaptation considering their target market, particularly
Asian and Middle East countries. For this purpose, aroma producers use
a reduced number of raw materials and remove non-halal processing
aids to adapt their process procedures for halal aroma production
(Barnekow et al., 2007; Berger, 2007).
It is known that ethanol is used as a solvent to produce aromas such
as vanilla from plants by conventional approaches (extraction etc.).
According to FDA standards, after extraction, natural aroma extracts
should contain approximately 35% ethanol (Administration, 2000b).
However, when a company requests to gain a halal certificate to any of
its products (e.g., flavor, flavored-food), many certifying agencies
permit an ethanol residue at the minimal level technologically
achievable due to the status of ethanol in Islamic dietary rules. For
example, IFANCA accepts to be used flavoring agents with a limit of the
ethanol residue of 0.5% in the ingredient, i.e., the vanilla is dried after
extraction (Riaz & Chaudry, 2018). Similarly, the Department of Islamic
Development Malaysia (JAKIM, a certification body in Malaysia) and
Indonesian Ulema Council (MUI, an Islamic scholar council in In-
donesia) permits to use alcohol less than 0.5% and 1.0%, respectively
(Bali, 2017). On the other hand, instead of organic solvents such as
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Trends in Food Science & Technology 98 (2020) 1–9
ethanol, eco-friendly strategies (wet extraction, ionic liquid-assisted
extraction, etc.) have been developed to recover from aroma sources
(Gmoser, Ferreira, Lennartsson, & Taherzadeh, 2017). These innovative
approaches can be applied achievable in the microbial flavor produc-
tion as well as the plant-based processes. With the novel methods that
do not need the use of ethanol, the use of biotechnology in the aroma
production can be a more advantageous alternative for the halal food
industry.
5. Future trends and conclusion
Nowadays, biotechnology and microbial products are inevitable
elements of the food industry. Biotechnological applications have many
advantages and they can contribute to the halal food industry as long as
the processing aids, food additives, and methods that are used in food
processing do not violate halal assurance. A microbial production is a
precious option for the halal food producers to supply components such
as chymosin and gelatin, since Muslim consumers are concerned for
these components to be derived from non-halal sources. If a genetic
modification process meets halal requirements, it can be possible to
produce various halal bioproducts at high efficiency. Furthermore, the
development of new halal bioproducts can facilitate the supply of ma-
terials that are used as an additive for the halal food industry. Finally,
comprehensive research should be done to produce various food-grade
metabolites under halal conditions, and these products should be
widely commercialized.
Acknowledgement
The author would like to acknowledge the valuable contributions of
Mrs. Sule Nur Kutlu, from Connecticut University, Hartford, CT, USA.
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