International Journal of Aquatic Research and Environmental Studies 2(2) 46-78 2022

A Review on the Application of Phytogenics as Feed Additives

for Aquatic Animals
Kazempoor R.1; Alavinezhad S.S.2*; Pargari M.M.3; Shakeri Y.S.3;
Haghighi M.M.3
Received: February 2021 Accepted: July 2021
Abstract
Feed preparation is the most expensive part of the aquaculture industry. In recent years, studies
have been conducted on the utilization of plants’ wastes and by-products (such as peel, pulp, and
kernels) as phytogenetic materials and sources of protein and nutrients for preparing feed in the
aquaculture industry, which have yielded promising results. These wastes are recycled by
processing as feed additives and returned to the feed chain, and because they are waste products
of plants and fruits, prepared phytogenic feed additives cannot be regarded as feed sources for
humans. In the future, there will be large quantities of fruit and vegetable waste, which have the
potential to be recycled and returned to the feed chain by being processed as additive feed for
aquatic animals. Phytogenics encompass a wide range of substances that can be classified based
on plant origin, the processing method, and composition but generally found in the form of herbs
and spices, or as plant extracts, essential oils, and oleoresins. The phytogenic properties of plants
are related to the various secondary metabolites produced by them. These metabolites are used
as growth and appetite stimulants. Furthermore, these metabolites induce the secretion of bile
and other digestive enzymes. They are not a threat to the environment, and their benefits as
substitutes for antibiotics have been promising. The antioxidant, anti-cancer, analgesic,
antimicrobial and antiparasitic effects of these products have been proven so far but the main
function reported for these compounds in the host is to improve gastrointestinal microbiota and
immune function (modulating cytokine production by epithelial cells). However, the mechanisms
of action of these products are not yet completely understood, and further studies are needed to
divulge the potential side effects of phytogenic substances on the host, the environment, and on
gastrointestinal microbiota. Understanding these mechanisms will ensure us about the safety of
these herbal additives for fish, consumers, and the environment. Despite some applications of
plant materials in aquaculture, their widespread use for feed preparation is still limited due to the
lack of sufficient knowledge on the mechanisms of action of phytogenic materials. So, a better
understanding of the effects of these compounds, which are derived from plant and fruit wastes,
on the host’s physiology will provide us with the opportunity to use these substances more widely
in the aquaculture industry. In the present review, we discuss the studies conducted on the use of
phytogenic materials as feed additives for aquatic animals, as well as their effects, advantages,
and disadvantages.

Keywords: Phytogenics, Feed Additives, fish, shrimp, immunesystem, growth

performance

1- Department of Biology, Roudehen Branch, Islamic Azad University, Roudehen, Iran.

2- Department of Aquatic Health and Diseases, Faculty of Veterinary Medicine, University of
Tehran, Tehran, Iran.
3- Department of Aquatic Health and Diseases, Faculty of Veterinary Medicine, Science and
Research Branch, Islamic Azad University, Tehran, Iran.
*Corresponding author: [email protected]
47 Kazempoor et al., A Review on the Application of Phytogenics as Feed Additives for Aquatic ...

Introduction producers is providing adequate and

Phytogenic feed additives or inexpensive nutrients to achieve the
phytobiotics are among the functional ideal growth rate and non-destructive to
feed additives that have been widely the environment. The use of low-protein
studied in recent years. Phytogenic feed feeds and low amounts of nutrients lead
additives are non-destructive bioactive to inefficient use of nutrients. As a
compounds of the environment derived result, increased feed intake increases
from plants, including herbs, spices, susceptibility to disease and increases
essential oils, and extracts. Glycyrrhizin, production costs. The production of
liquiritin, glabridin, polysaccharides, more waste also causes damage to the
flavonoids, alkaloids, anthraquinone, environment (Goncalves and Santos,
saponin, and azadirachtin are among the 2015).
active ingredients in these phytogenic The presence of endemic pathogens
compounds (Bhujel et al., 2017). Acids, and pandemic diseases constantly
alcohols, aldehydes, acyl esters, sulfur- endangers aquaculture farmers around
containing compounds, coumarins, and the world to achieve a balanced
homologues of polypropanoid are other production system. The prevalence of
studied molecules (Yang et al., 2015). A fish diseases is one of the main
wide range of phytogenics in farmed limitations for the development of
aquatic animals have been studied aquaculture (FAO, 2020). In the past,
mainly due to their properties including antibiotics were used to prevent these
improved taste in feed, increased problems. But today, producers are
growth, stimulated immune system, looking for alternative ways due to the
improved intestinal microbiota, increasing awareness of consumers
antimicrobial, antiparasitic and antiviral about environmental problems and
activities. bacterial resistance to the indiscriminate
Global aquaculture production use of antibiotics against zoonotic
(including aquatic plants) is 110.2 pathogens. A significant number of
million tons, with an initial sales value studies have focused on the search for
of 243.5 billion dollars. Total antibiotic alternatives with similar
production includes 80.0 million tons of antimicrobial and growth-promoting
edible fish and 30.1 million tons of effects without causing residues,
aquatic plants (Bharathi et al., 2019). bacterial resistance, and potential side
According to the FAO, global effects for animals. Functional feed
aquaculture production is estimated to additives are an alternative to antibiotics
reach 80 million tons by 2050. The and in addition to nutritional value have
aquatic feed contains 50 to 80 percent of health benefits for animals (Korzekwa et
rearing costs, and successful aquaculture al., 2016; Waagbø and Remø, 2020).
depends on a balanced diet and low-cost This study aimed to investigate the
production. As a result, one of the most effects of phytogenic feed additives on
important challenges for aquaculture aquatic nutrition as an alternative
 International Journal of Aquatic Research and Environmental Studies 2(2) 2022 48

strategy for antibiotics to achieve Technological additives

sustainable aquaculture. This classification refers to a group of
additives that affect the technological
Classification of phytogenic aspects of the feed. These additives do
compounds not directly affect the nutritional value of
Phytogenic feed additives are classified the feed, but may indirectly affect the
into three main groups, which include nutritional value of the feed by
sensory additives, technological improving maintenance or hygienic
additives, and zootechnical additives. properties, such as mycotoxin
Some of these additives have more than contaminants in feed (Pandey et al.,
one positive effect, but they can not be 2019).
precisely classified in one of the above
groups (Karásková et al., 2015). Zootechnical additives
These additives improve the nutrient
Sensory additives status and livestock production. These
This group of additives usually compounds provide specific nutrients
stimulates the appetite through the effect and help to use the nutrients in the diet
they have on the taste or color of feed more effectively (Pandey et al., 2019).
(such as plant pigments). The most These additives include immune
commonly used sensory additives are regulators, digestive stimulants, and
carotenoid pigments, which are sourced growth stimulants of non-microbial
from carrots, chlorella, marigolds origin, and substances that enhance the
(Tagetes erecta L.), or lutein (Karásková quality of animal products. These
et al., 2015). Astaxanthin is one of the additives are divided into three
known carotenoids in aquatic animals. subgroups: Immunosuppressive
The use of astaxanthin improves the compounds (oligosaccharides,
color of fish fillets (Teimouri et al., especially beta-glucans that stimulate
2013). Other studies on carotenoid the activity of cells, enzymes, and other
pigment include increased redness in factors involved in immunity),
goldfish and carp (Hancz et al., 2003), compounds that improve production
production of vivid colors (including performance or quality of livestock
blue and green) in marine invertebrates products (cinnamaldehyde and turmeric)
(Davies, 2009), and increased redness in They are effective in improving
dwarf gourami (Baron et al., 2008). digestion and absorption of nutrients)
However, the instability and high cost of and compounds that reduce oxidative
natural carotenoids have limited the use stress (polyphenols, carotenoids,
of these compounds (Englmaierová et betalains, and curcumin, which are
al. 2014). effective in reducing the level of free
radicals (ROS)) (Karásková et al.,
2015). The use of these feed additives in
aquaculture can be a powerful solution
49 Kazempoor et al., A Review on the Application of Phytogenics as Feed Additives for Aquatic ...

to limit nitrogen depletion in the 2013a). The use of dietary supplements

environment by improving feed has been suggested to compensate for
efficiency, saving nutrients, and using the problems caused by replacing FM
proteins, and helping manage fish health with a diet containing phytogenic plant
(Goncalves and Santos, 2015). proteins. According to studies,
According to reports, Feeding with phytogenic compounds improve nutrient
phytogenic feed additives including retention and growth function in aquatic
AROMEX® ME Plus and FRESTA® F organisms (Karásková et al., 2015;
Plus, oregano, anise, and citrus peel Encarnação, 2016). Induction of
essential oils reduced excreted ammonia secretion of digestive enzymes is one of
in feed animals (Veit et al., 2011; Hong the mechanisms of phytogenics in
et al., 2012). increasing growth performance which
stimulates appetite and thus increases
The role of phytogenics in aquatic feed intake and conversion efficiency
growth performance (Wenk 2003; Liu et al. 2011). For
In recent years, rations containing fish example, spices such as peppers (such as
(FM) and fish oil have been used more capsaicin and piperine) and other
selectively due to reduced availability essential oils containing
and simultaneous price increases, while cinnamaldehyde stimulate amylase
many efforts are being made to find production (Steiner and Syed 2015).
alternative protein sources for profitable Phytogenic additives (especially
and sustainable aquaculture (FAO, essential oils) increase the taste and
2018; Slater et al., 2018). Plant products smell of feed, increase palatability and
have been proposed as an alternative to thus increase fed consumption
FM in aquatic feed due to their low cost, (Kroismayr et al., 2006). This is
availability, and high protein (Gatlin et probably due to the antioxidant effects of
al., 2007; Olsen and Hasan, 2012). But phytogenic compounds, which help
the use of plant products is the cause of maintain the quality of the diet and
problems such as high levels of anti- prevent the spread of unpleasant odors
nutritional factors in plant proteins, lack (Franz et al., 2010; Solà-Oriol et al.,
of essential amino acids, lower 2011). However, there is little evidence
digestibility, high levels of insoluble to increase the palatability of diets
carbohydrates, and high fiber, which containing phytogenic compounds in
reduces the palatability of these plant fish and shrimp (Giannenas et al., 2012;
proteins compared to animal proteins Volpatti et al., 2013).
(Hardy, 2010), and leads to reduced
growth in fish and shrimp that feed on The role of phytogenics in the growth of
plant protein (De Francesco et al., 2004; cold water fish
Enterria et al., 2011; Montero et al., Giannenas et al. (2012) reported that
2005; Peres and Oliva-Teles, 2006; using phytogenic additives including
Sudaryono And Evans, 1999; Zhu et al., carvacrol and thymol showed no
 International Journal of Aquatic Research and Environmental Studies 2(2) 2022 50

significant difference in feed intake in The role of phytogenics in shrimp

the diet of Rainbow trout growth
(Oncorhynchus mykiss) compared to The research by Goncalves and Santos
control diets. But in fish fed with (2015) is one of the studies on the effect
carvacrol and thymol, feed efficiency of phytosanitary additives on shrimp
increased significantly compared to fish growth performance. Based on the
fed with the control diet. In the study of results of this study, the use of
Giannenas et al. (2012), feeding on diets commercial phytogenic feed additive
fortified with carvacrol and thymol Digestarom® P.E.P. MGE in the diet
improved feed efficiency. But it did not containing small amounts of fish
affect fish weight gain compared to the increased weight, increased feed
control group. The study by Peterson et conversion ratio, and growth rate
al. (2014) has not reported the weight compared to shrimp that did not use
gain of trout fed with the commercial dietary supplements. In another study,
phytogenic supplement Digestarom® papaya leaves increased protein
P.E.P. MGE. digestion, feed conversion ratio, and
growth in Penaeus monodon shrimp
The role of phytogenics in the growth of larvae (Peñaflorida, 1995). In addition,
warm water fish a significant increase in digestive
Zheng et al. (2009) evaluated the effect enzymes (amylase, protease, and lipase)
of carvacrol and thymol separately in and better feed conversion efficiencies
combination with each other and were observed in Post-larvae of P.
combination with oregano essential oil monodon fed with enriched Artemia
in canal catfish. The results of this study with ginger (Zingiber officinale)
showed that fish that consumed oregano (Venkatramalingam et al., 2007).
essential oil, and fish that used carvacrol
alone or a combination of thymol and The role of phytogenics in the
carvacrol gained more weight than fish improvement of immune system
in the control group. In a study by function
Ceulemans et al. (2009) on the nutrition Numerous studies have reported the use
of Nile tilapia (Oreochromis niloticus) of phytobiotics in aquaculture to
with a diet containing a mixture of plant stimulate the activity of immune system
extracts and natural emulsifying agents, components (Rao et al., 2006; Sahu et
feed conversion and protein al., 2007; Ardó et al., 2008). Antioxidant
consumption efficiency were more effect of phytogenic mechanisms in
favorable than control diets. The use of improving immune function. The
sweet potato skin in the diet also antioxidant activity of phytogenic
improved growth performance and compounds is due to their ability to
nutritional efficiency in Nile tilapia destroy free radicals, inhibit reactive
(Omoregie et al., 2009). oxygen species (ROS) and other oxygen
radicals produced in cells and tissues.
51 Kazempoor et al., A Review on the Application of Phytogenics as Feed Additives for Aquatic ...

However, high concentrations of these in cold-water fish (especially rainbow

compounds have been reported to trout). In the study of Giannenas et al.
exhibit peroxidation antagonistic (2012) on the effect of feeding rainbow
effects (Llana-Ruiz-Cabello et al., trout with carvacrol and thymol
2015). Phytogenic compounds are (although the fish were not sick in the
involved in modulating the expression of challenges) a significant increase in the
proinflammatory and anti-inflammatory activity of glutathione-based enzymes
cytokines by disrupting NF-κB signaling (glutathione reductase, glutathione-S-
pathways mediated by TLR and MAPK transferase), an increase in lysozyme
(Somensi et al., 2019; Zhou et al., 2014; levels and catalase activity and a
Wu et al., 2017; Liu et al., 2019). In this significant decrease in serum nitric
regard, several studies have shown that oxide (NO) were observed. These results
phytochemical compounds including indicate the effect of phytogenic
curcumin (Shehzad et al., 2011), caffeic additives on intrinsic safety parameters.
acid phenyl ester (CAPE) from bee In the study of Gulec et al. (2013), the
propolis (Lee et al., 2010), epicatechin use of feed containing vegetable oils
(Bahia et al., 2008), grape seed extract (Thymus vulgaris and Foeniculum
and grape brand (GSGME) (Gessner et vulgare) significantly increased the
al., 2013), Cinnamaldehyde (Wondrak amount of total protein, albumin,
et al., 2010) and Purple Potato cholesterol, triglycerides, bilirubin, K
Anthocyanins (Hwang et al., 2011) Na, Ca, Mg, and decreased plasma
Increase the expression or transfer of glucose and chlorine levels in rainbow
Nrf2 and reduce or inhibit NF-κB trout exposed to Yersinia ruckeri.
activation. Plant compounds that alter
the Nrf2 and NF-κB pathways can The role of phytogenics in improving the
protect the host against oxidative stress, immune system of warm water fish
reduce inflammation, and ultimately According to the results of Yin et al.
improve animal health and growth (2006), the extract of Milkvetch root
performance. Lectin-mediated pathways increased phagocytosis of leukocytes
are another mechanism by which and lysozyme activity in the Nile tilapia.
phytogenic compounds can improve the In another study, Asimi and Sahu (2013)
immune system (LaFrentz et al., 2012) investigated the effect of feeding on
because lectins can activate complement extracts of thyme (Thymus vulgaris),
and are involved in improving innate rosemary (Rosmarinus officinalis), and
immunity (Ourth et al., 2007). fenugreek (Trigonella foenum graecum)
on Mozambique tilapia (Oreochromis
The role of phytogenics in improving the mossambicus). They observed increased
immune system of cold water fish phagocytic activity, increased white and
Numerous studies have been performed red blood cells, and increased hematocrit
on the effect of phytogenic additives on levels. In addition, they reported an
improving the immune system function increase in plasma lysozyme and
 International Journal of Aquatic Research and Environmental Studies 2(2) 2022 52

myeloperoxidase activity after infection larvae of Penaeus indicus shrimp

with Streptococcus iniae. In Labeo (Immanuel et al., 2004; Citarasu, 2010)
rohita, the root extract of Withania and the improvement in the survival rate
somnifer increased Nitro blue of Litopenaeus vannamei shrimp have
tetrazolium levels, phagocytic cell been reported as a result of the use of
activity, lysozyme activity, and total herbal supplements (Yu et al., 2008). It
immunoglobulin levels (Sharma et al., has also been reported that the mixture
2010). Also, Indian ginseng root extract of Chinese herbal supplements increases
(Ashwagandha) stimulated the immune nonspecific immunity in shrimp (Luo,
system and reduced stress caused by low 1997; Chansue et al., 2000). He et al.
pH and iron toxicity in water (2017) have reported the increased
(Laltlanmawia et al., 2019). Injection of immunity in Litopenaeus vannamei
Astragalus polysaccharides (APS) shrimp as a result of using stout camphor
increased IL-1β mRNA levels in a dose- extract (Yeh et al., 2009) and a
dependent manner in the renal head and combination of organic acids (citric acid
regulated TNF-α transcription in the and sorbic acid) and essential oils
gills and spleen (at high concentrations (thymol and vanillin) as dietary
of APS). TNF-α mRNA was also supplements. The study by Kesselring et
significantly increased in the renal head al. (2021) showed that feeding a diet low
(at low concentrations of APS) and in FM and phytogenic supplementation
regulated Lysozyme-C mRNA levels in increased the total number of hemocytes
gills (at low concentrations of APS) and (THCs) and red blood cells compared to
spleen (at moderate concentrations of a diet high in fish (FM). According to
APS) in common carp (Cyprinus carpio) similar studies, the decreased FM levels
(Yuan et al., 2008). According to Nahak typically affect shrimp defense
and Sahu (2014), the use of basil aerial mechanisms and reduce hemocytes (Van
part extract in feed increases RBC, de Braak et al., 2002). Also, a low-FM
WBC, serum protein, and hematocrit (at diet with phytogenic supplementation
concentrations of 2.5 and 5%) and reduced ALT and LDH activity levels
decreases serum glucose (at 5%) in compared to the low-FM diet group
Walking catfish (Clarias batrachus) and which shows that the use of phytogenic
this compound acts as a strong immune supplements improves the health status
stimulant. of L. vannamei by reducing the risk of
cell damage and tissue necrosis.
The role of phytogenics in improving the
immune system of shrimp The role of phytogenics in increasing
The increase in survival rate is one of the mucosal immunity
most important effects of increased Mucosal safety in aquatic animals has
immunity due to the use of phytogenic been considered by many researchers in
compounds in shrimp. For example, the recent years due to its diversity and
increase in survival rate in the post- characteristics. Mucosal-associated
53 Kazempoor et al., A Review on the Application of Phytogenics as Feed Additives for Aquatic ...

lymphoid tissue (MALT) immunity is main mucosal lymphoid tissues in fish is

divided into Gut-associated lymphoid depicted in Figure 1. In addition, the
tissue (GALT), Skin-associated effect of phytogenics against fish
lymphoid tissues (SALT), and Gill- pathogenic organisms is suggested in
associated lymphoid tissue (GIALT) Figure 2.
(Lazado and Caipang, 2014). Mode of
action of phytogenics at the level of the

Figure 1: Suggested mechanisms of cell activation by the transient receptor potential (TRP) cation
channels mediated by phytogenics’ bioactive compounds in mucosal-associated lymphoid
tissues (MALTs). Bioactive compounds activate TRP channels leading to intracellular
Ca2+ increase and non-canonical activation of the TAK complex. In parallel, stimulation
by pathogen-associated molecular patterns (PAMPs) may facilitate the activation of TLR
and TRP signaling pathways. TLR, toll-like receptors; MyD88, myeloid differentiation
primary response 88; TAK, transforming growth factor beta (TGFβ) activated kinase;
TAB, TGFβ activated kinase binding protein; ROS, reactive oxygen species; NF-kB,
nuclear factor kappa-B; IKK, inhibitor of NF-kB kinase; MAPK, mitogen-activated
protein kinase; AP1, activator protein 1; CYP, cytochromes P450; P, phosphorylation
(Firmino et al., 2021).
 International Journal of Aquatic Research and Environmental Studies 2(2) 2022 54

Figure 2: Summary of the proposed mode of response induced by phytogenic bioactive compounds
in fish mucosal tissues. The effects against representative types of common pathogens on
the most studied mucosal-associated lymphoid tissues in fish so far are represented in the
figure. (A) Gills. (B) Gut. (C) Skin. Gilthead seabream (S. aurata) was used in the figure
as a representative aquaculture-relevant fish (Firmino et al., 2021).

Figure 1 Suggested mechanisms of cell activated kinase binding protein; ROS,

activation by the transient receptor reactive oxygen species; NF-kB, nuclear
potential (TRP) cation channels factor kappa-B; IKK, inhibitor of NF-kB
mediated by phytogenics’ bioactive kinase; MAPK, mitogen-activated
compounds in mucosal-associated protein kinase; AP1, activator protein 1;
lymphoid tissues (MALTs). Bioactive CYP, cytochromes P450; P,
compounds activate TRP channels phosphorylation (Firmino et al., 2021).
leading to intracellular Ca2+ increase and
non-canonical activation of the TAK The role of phytogenics in increasing
complex. In parallel, stimulation by skin mucosal immunity
pathogen-associated molecular patterns The skin plays a key role as the first line
(PAMPs) may facilitate the activation of of defense against various pathogens in
TLR and TRP signaling pathways. TLR, fish (Hoseinifar et al., 2017). Most
toll-like receptors; MyD88, myeloid studies on the effects of phytogenic
differentiation primary response 88; additives on skin mucosal immunity
TAK, transforming growth factor beta have shown an increase in skin mucosal
(TGFβ) activated kinase; TAB, TGFβ immune markers or increased
55 Kazempoor et al., A Review on the Application of Phytogenics as Feed Additives for Aquatic ...

antibacterial activity of skin mucosa The role of phytogenics in increasing

(Heyman et al., 2015; Adel et al., 2015a; gastrointestinal mucosal immunity
Adel et al., 2015b; Gholamhosseini et The gastrointestinal tract (especially the
al., 2020; Heydari et al., 2020; Kurian et intestine) is mainly composed of
al., 2020; Mirghaed et al., 2020; physical, chemical, immunological, and
Mohammadi et al., 2020; Paknejad et microbiological components. Therefore,
al., 2020; Rashidian et al., 2021; Yousefi it is a selective barrier between the host
et al., 2021). Lysozyme, alkaline and its surrounding environment
phosphatase, complement and protease (Yegani and Korver, 2008). As a result,
activities, total immunoglobulin, and any damage or disruption of its normal
protein content in fish skin mucosa are function suppresses immune responses
markers that have been evaluated and and reduces animal productivity
have antibacterial potential in vitro (McDevitt et al., 2006). In recent years,
against pathogens. Unfortunately, few the study of phytogenic compounds'
studies have attempted to identify the effect on mucosal immunity has become
underlying mechanisms that regulate the necessary due to the importance of the
immune system (Firmino et al., 2021). mucosal barrier in defending fish against
the invasion of pathogens (Yu et al.,
The role of phytogenics in increasing gill 2020).
mucosal immunity Studies on the effect of phytogenic
Studies on the effects of phytogenic feed substances on the intestine include
additives on gill structure and function evaluation of changes in
are very limited. Some studies have morphoanatomical parameters such as
reported the protective effects of these improved integrity, increased length,
compounds in reducing width, and the number of goblet cells
histopathological lesions of the gills due (Abdel-Latif et al., 2020; Heluy et al.,
to exposure to toxic elements or 2020; Ferreira et al., 2016; Abdel-
pathogens (Vickers, 2017; Khafaga et Tawwab et al., 2018; Vickers, 2017;
al., 2020; El Euony et al., 2020). Araruna et al., 2020), modulation of
According to the results of Yuan et al. intestinal lymphocyte count (Hernández
(2008), injection of astragalus et al., 2016; Valladao et al., 2017),
polysaccharides (APS) had no effect on improvement in the level of humoral
IL-1β mRNA level in the gills but immune markers such as lysozyme
regulated TNF-α and Lysozyme-C (Sutili et al., 2016), improvement in the
mRNA transcription at high and low activity of antioxidant enzymes (Hoseini
doses of APS in the gill of common carp and Yousefi, 2019; Reyes-Cerpa et al.,
(Cyprinus carpio). 2018), reducing the expression of
proinflammatory genes such as tnfa and
tnfb (Zhang et al., 2020) and modulation
of intestinal microbiota composition
(Zhang et al., 2020; Mousavi et al.,
 International Journal of Aquatic Research and Environmental Studies 2(2) 2022 56

2016; Araruna et al., 2020). The positive phytogenics on mucosal parameters

effects of phytogenetics on the (Valladão et al., 2019; Navarrete et al.,
morphology of small intestinal tissues 2010; Vickers, 2017; Hernández et al.,
and villi increase nutrient digestibility 2015; Vazirzadeh et al., 2019). The use
(Steiner and Syed, 2015). Other effects of phytogenic compounds as food
of phytogenics on the gastrointestinal additives in non-optimal doses and their
tract include stimulating gastrointestinal negligible effect on the bacterial
secretions and increasing mucus composition of fish intestines is one of
production as a result of increasing the the main causes (Sutili et al., 2018).
number of goblet cells in the intestine Studies on the effect of phytogenic
(Goncalves and Santos, 2015). The food additives on the gastrointestinal
bacterial status of the gastrointestinal mucosa are divided into two main
tract changes under the influence of groups: the effect on the microbial flora
genetic factors, feeding habits, and the and the intestinal histomorphology.
environment (Austin, 2006; Wong and Modification of intestinal microbial
Rawls, 2012; Gómez and Balcázar, flora has been considered by Hongbai et
2008). However, the intestinal bacterial al. (2004) using different Chinese plants
community and the metabolites in carp, Ran et al. (2016) using a
produced by them have significant commercial mixture of thymol and
effects on the host health status by carvacrol in hybrid tilapia (O. niloticus x
modulating the immune system and O. aureus), and Giannenas et al. (2012)
affecting metabolism (Bento et al. 2013; using phytogenic supplementation
Lazado and Caipang, 2014). Limited containing thymol and carvacrol in
studies have examined the effects of rainbow trout. According to a study by
phytogenics as feed additives on Sutili et al. (2016) using gradient gel
intestinal microbiota in fish. Previous electrophoresis (DGGE) analysis, the
studies have focused on the effect of use of American basil (Ocimum
these plant substances as dietary americanum) essential oils with food did
ingredients instead of additives and their not affect the intestinal microbiome in
effect on microbial communities of fish Sciaenops ocellatus. In the study by
intestines (Ringø et al., 2008; Silva et Navarrete et al. (2010) using
al., 2011; Reveco et al. 2014; Zarkasi et temperature gradient gel electrophoresis
al., 2017). Studies on the microbial flora (TGGE) analysis, a diet containing
of the gastrointestinal tract are often thyme-derived essential oil supplement
limited to identifying lactic acid (Thymus vulgaris) showed no effect on
bacteria. Therefore, evaluation of the the intestinal bacterial composition of
feed additives' effects on mucosal tissues rainbow trout. In the study of Bello et al.
using the results of these studies is not (2012), an increase in the height and
complete and acceptable and leads to width of the villi and the depth of crypt
incorrect conclusions. Also, some was observed in Clarias gariepinus fed
studies have not reported any effect of with onion residues and walnut leaf.
57 Kazempoor et al., A Review on the Application of Phytogenics as Feed Additives for Aquatic ...

Also, according to Goncalves and inhibition of bacterial movement,

Santos (2015), the use of commercial depletion of ATP reservoirs, elimination
phytogenic additives Digestarom® of proton stimulus, inhibition of quorum
P.E.P. MGE in a low-fish diet improved sensing (QS), and reduction of bacterial
the structure of midgut microvilli biofilm formation (Kachur and Suntres,
compared to shrimp that did not use 2020).
dietary supplements. Quorum Sensing (QS) is involved in
regulating a wide range of different
The role of phytogenics in inhibiting physiological processes of bacteria,
microbial pathogens especially in aggravating factors that are
The antimicrobial properties of important during the pathogenic process
phytogenic compounds vary according (Greenberg, 2003; Vendeville et al.,
to the location of hydroxyl or alkyl 2005; Xavier and Bassler, 2003;
groups and the release properties of Defoirdt et al., 2013). In this regard,
lipopolysaccharides (Yang et al., 2015). there is evidence for the ability to disrupt
About phenolic terpenoids, the hydroxyl QS by various phytogenic compounds
group and the presence of non-localized including alfalfa seed extract (Vikram et
electrons are important elements for al., 2010), plants (Koh and Tham, 2011),
their antimicrobial function (Lambert et and essential oils (Bjarnsholt et al.,
al., 2001; Ultee et al., 2002). Hellander 2005; Choo et al., 2006; Zhou et al.,
et al. (1998) also reported that thymol 2013). Unfortunately, the use of QS
and carvacrol have a high ability to inhibition strategies to control bacterial
degrade outer membranes .This function infections is unknown in aquaculture
is mainly due to their ability to release (Yang et al., 2015). The first report on
lipopolysaccharides. Phytogenics aquatic animals was made by Manefield
penetrate the bacterial membrane due to et al. (1999) on furanone extracted from
their lipophilic properties and disrupt the the Australian microalgae (Delisea
structure and function of bacteria by pulchra). Based on the results of this
expanding the membrane, increasing study, this combination increased the
membrane fluidity and permeability, survival of shrimp larvae exposed to
disrupting membrane proteins, pathogens such as V. campbellii, V.
inhibiting respiration, and altering ion harveyi, and V. parahaemolyticus
transport. (Firmino et al., 2021). These (Defoird et al., 2007). Organic
compounds also play a role in reducing compounds such as cinnamaldehyde and
infection by detecting and accumulating its derivatives have also been reported to
microbial pathogens through lectin- be effective against V. harveyi in Brine
mediated pathways (Ourth et al., 2007; shrimp (Niu et al., 2006; Brackman et
LaFrentz et al., 2012). Other al., 2008) and Macrobrachium
mechanisms of phytogenics as Rosenbergii larvae (Pande et al., 2013).
antibacterial compounds include
inhibition of flagellin synthesis,
 International Journal of Aquatic Research and Environmental Studies 2(2) 2022 58

The role of phytogenics in inhibiting sativum), and mugwort (Artemisia

microbial pathogens in cold water fish vulgaris), Gbadamosi et al. (2016) using
Studies on the effect of phytogenetics on Moringa oleifera, and Pachanawan et al.
increasing the resistance of cold-water (2008) using dry leaf powder and
fish to bacterial pathogens are much less ethanolic extract of Psidium guajava.
than warm-water fish, and studies have Asimi and Sahu (2013) in the study of
been limited to rainbow trout. In a study feeding with extracts of thyme (Thymus
by Menanteau-Ledouble et al. (2015), vulgaris) rosemary (Rosmarinus
the use of a commercial phytogenic food officinalis) and fenugreek (Trigonella
additive (containing oregano, anise, and foenum graecum) extracts in
citrus oils) increased the survival of Mozambique tilapia (Oreochromis
rainbow trout (Onchorhynchus mykiss) mossambicus) and Zilberg et al. (2010)
exposed to Aeromonas salmonicida in in the study of feeding with Rosmarinus
three forms of Intraperitoneal injection, officinalis extracts in Nile tilapia
immersion in bacterial solution and reported increased resistance and
living with infected fish. According to decreased fish mortality after infection
these results, the highest effect of with Streptococcus iniae.
phytogenics in protecting fish from Numerous studies have been
pathogens was in the form of immersion. performed on catfish, including the
Also, according to Gulec et al. (2013), effect of using garlic peel (Allium
fortification of the diet with oils sativum) on increasing resistance to
extracted from Thymus vulgaris and Aeromonas hydrophila infection in the
Foeniculum vulgare can increase the fingerlings of African catfish
resistance to Yersinia ruckeri in rainbow (Thanikachalam et al., 2010). Zheng et
trout by increasing the levels of some al. (2009) also evaluated the effect of
biochemical parameters and carvacrol and thymol separately, in
electrolytes. combination with each other and
combination with oregano essential oil
The role of phytogenics in inhibiting in canal catfish. In this study, fish were
microbial pathogens in warm water fish challenged with this diet for 8 weeks and
Most studies have been performed on the then with Aeromonas hydrophila. After
effects of phytogenics on increasing the challenge with A. hydrophila, the lowest
resistance of tilapia to bacterial diseases. mortality was observed in the group fed
Numerous studies have reported with oregano and then the fish fed with
increased resistance of tilapia to thymol and carvacrol. In another study,
Aeromonas hydrophila challenge due to Peterson et al. (2015) found that feeding
the use of phytogenic compounds which with a commercial phytogenic feed
include studies by Jayathirtha and additive (Digestarom® PEP MGE;
Mishra (2004) using E. officinalis containing the essential oils of carvacrol,
supplement, El Deen and Razin (2009) thymol, anethole, and limonene)
using crude garlic extract (Allium increased survival rates in juveniles of
59 Kazempoor et al., A Review on the Application of Phytogenics as Feed Additives for Aquatic ...

canal catfish (Ictalurus punctatus) farming industry is currently facing

exposed to Edwardsiella ictalurid. Other several episodic viral diseases. White
studies on warm-water fish include spot syndrome (WSSV) virus causes
Minomol (2005) on the effect of 100% mortality in shrimp farms (Selvam
Emblica officinalis on reducing the et al., 2020). In this regard, according to
incidence of microbial infection in Yogeeswaran et al. (2012), the use of
Carassius auratus and the results of Withania somnifera (Yogeeswaran et
Volpatti et al. (2013) on-resistance of al., 2012) and phytogenic
European sea bass fed carvacrol against supplementation ™ Phytocee (Selvam et
Vibrio anguillarum. al., 2020) as a dietary supplement
increases the survival of shrimp exposed
The role of phytogenics in inhibiting to White spot disease. However, the
microbial pathogens in shrimp results of studies show the antiviral
There are also studies on the protective effects of medicinal plants on aquatic
effect of nutrition with phytogenes viruses and the extensive research
exposed to bacterial pathogens in capacity to investigate the effects of
shrimp. According to Goncalves and these plant compounds as food additives
Santos (2015), the use of a diet in vivo.
containing the commercial phytogenic For example, in vitro studies include
compound Digestarom® P.E.P. MGE Micol et al. (2005) report on the
increased resistance and decreased inhibitory effect of olive leaf extract
mortality in shrimp exposed to Vibrio (Olea europaea) on Viral hemorrhagic
parahaemolyticus. Also, according to septicemia (VHSV) and the effect of
the report of Yatip et al. (2018), the use eighteen Thai plant extracts (Cassia
of fermented Japanese soy extract alata, Clinacanthus spp., Clinacanthus
(Natto) in the diet led to a reduction in nutans, Calophyllum inophyllum, Hura
mortalities due to Vibrio harveyi in crepitan, Glinus oppositifolis,
white leg shrimp Penaeus vannamei. Momordica cha rantina, Ocimum
sanctum (white), Ocimum sanctum
The role of phytogenics in inhibiting (red), Phyllanthus reticulatus,
viral pathogens Phyllanthus urinaria, Phyllanthus
The antiviral effects of plant compounds acidus, Orchocarpus siamensis,
are mainly due to the inhibition of virus Phyllanthus amarus, Phyllanthus
transcription, reducing its proliferation debelis, Psidium guajava, Tinospora
in host cells and thus increasing the crispa and Tinospora cordifolia) on
innate immune response (Syahidah et CHSE-214 cells were reported in vitro
al., 2015). In this regard, few studies against infectious hematopoietic
have been performed on the effect of necrosis virus (IHNV), Oncorhynchus
phytogenic food additives in inhibiting masou virus disease (OMV) and
viral pathogens in aquatic animals, Infectious pancreatic necrosis (IPNV)
which is limited to shrimp. The shrimp (Direkbusarakom et al., 1996). Also in
 International Journal of Aquatic Research and Environmental Studies 2(2) 2022 60

the study of Harikrishnan et al. (2010) study by El Deen and Razin (2009), the
Intraperitoneal injection of aqueous, use of crude garlic extract (Allium
ethanolic, and methanolic extracts of sativum) and mugwort (Artemisia
Punica granatum leaves increased vulgaris) controlled Trichodina's disease
resistance to lymphocystis disease virus in Nile tilapia. Chitmanat et al. (2005)
(LDV) in Olive flounder (Paralichthys showed that the use of garlic and Indian
olivaceus). According to Novriadi and almond extract (Terminalia catappa)
Haw (2015), immersion of tiger grouper reduces Trichodina infection in tilapia.
(Epinephelus fuscoguttatus) in herbal Chansue and Tangtrongpiros (2005) also
solution © AquaHerb increased fish reported that the addition of dried
resistance to iridovirus infection. almond leaves (Terminalia catappa)
could kill monogenic parasites in
The role of phytogenics in inhibiting Carassius auratus. According to
parasitic pathogens Fridman et al. (2014), the use of the
Most of the studies on the effect of plant aqueous extract of garlic (Allium
compounds on parasites in aquatic sativum) in the diet of guinea fowl
animals have been related to external (Poecilia reticulata) infected with
parasites and the preferred prescription Gyrodactylus turnbulli and
method is immersion due to the lack of Dactylogyrus sp. significantly reduced
proper implementation of prevention the mean prevalence and severity of
methods in aquaculture farms (Reverter parasites. Militz et al. (2013) showed
et al., 2014). Numerous studies have that the use of garlic supplements as
been done on the inhibitory effects of prophylaxis leads to a significant
plant compounds on parasites including reduction in infection of Neobenedenia
Gyrodactylus turnbulli (Fridman et al., sp. (Monogenea: Capsalidae) in farmed
2014), Anacanthorus penilabiatus barramundi (Lates calcarifer).
(Martins et al., 2002), Neobenedenia sp.
(Militz et al., 2014), Ichthyophthirius The role of phytogenics in improving
multifiliis (Zhang et al., 2013), the quality of fish carcasses
Dactylogyrus intermedius (Wu et al., Carcass composition including fat and
2011) and Gyrodactylus kobay ashii protein are factors that have been
(Zhou et al., 2017). However, limited evaluated in some studies as a result of
studies have reported the effects of feeding with phytogenic food additives
phytogenic dietary supplements on the in aquatic animals. The results of
prevention and control of parasitic Peterson et al. (2014) study on catfish
diseases. Existing mechanisms are fillets fed with phytogenic feed additive
involved in improving immune function (Digestarom® PEP MGE) showed less
(especially mucosal immunity). Some fillet fat (31.3 vs. 35.9) and slightly
studies in tilapia have reported a higher fillet protein (62.4 vs. 61.2%).
protective effect of phytogenes against Less fat in seafood is beneficial because
Trichodina infection. According to a it reduces waste, increases efficiency,
61 Kazempoor et al., A Review on the Application of Phytogenics as Feed Additives for Aquatic ...

reduces bad taste, and reduces storage antibiotics on farms. This ban indicates
problems. Also in the study of rainbow the need to develop alternative therapies
trout, the stability of lipids against (More, 2020). The use of herbal
oxidative damage and the activity of compounds is one of these alternative
glutathione-based enzymes in the fillets therapies that have attracted a lot of
of both thymol-treated fish and attention in recent years. The global
carvacrol-treated fish improved market for phytogenic food additives is
(Giannenas et al. 2012). The results of estimated at $ 753 million in 2020 and is
these studies show that herbal projected to reach $ 1.098 million by
supplements may have a beneficial 2025 (Firmino et al., 2021). Herbal
effect in reducing fillet fat, increasing compounds can be effective alternatives,
protein deposition, and increasing especially for the prevention of diseases
carcass antioxidant activity. However, caused by bacteria and parasites in
the results of studies in some cases show aquatic animals. However, studies on
the lack of phytogenic compounds' this subject have shown varying degrees
effect on improving carcass quality. of effectiveness, and the use of
According to the results of Zheng et al. phytogenic compounds to control
(2009), feeding canal catfish with parasites through immersion has had
carvacrol and thymol separately, in limited success. The reason for this can
combination with each other and be attributed to factors such as extraction
combination with oregano essential oil methods, part of the plant that is used as
did not affect carcasses and fillets among raw material, the concentration of
the control and treatment groups. additives, prescription method, and
storage conditions before feeding, which
Prospects for the future greatly affects their performance
The world's population today is about (Reverter et al. 2014). Determining the
seven billion and will reach nine billion optimal dose in the use of phytogenic
by 2050. Feeding the world's population compounds is also very important
by 2050 will be a major challenge. because it increases losses if
Therefore, aquaculture will replace inappropriate doses are used
fishing and most of the required protein (Ikhwanuddin et al., 2014). Further
will be provided from aquatic sources studies are also needed to determine the
(Costello et al., 2020). The use of quality, bioactive components, and
antibiotics and chemicals as stimulants classification of the chemical
for the growth and treatment of diseases composition of these phytogenics to be
in aquaculture has raised concerns in used to develop standard extraction
many countries. These compounds cause protocols, determine prescribing
environmental pollution and are methods and determine the optimal dose
dangerous to human health. In 2022, in fish and crustaceans (Reverter et al.,
several countries and the European 2014). The fastest way to use phytogenic
Union (EU) will ban the use of compounds is by injection, but this
 International Journal of Aquatic Research and Environmental Studies 2(2) 2022 62

method is very troublesome and stressful clove basil, Ocimum gratissimum,

in fish and crustaceans. Therefore, leaf extract and its susceptibility to
feeding prescription is the most Listeria monocytogenes
appropriate and available method infection. Fish and Shellfish
(Yoshida et al., 1995). One of the Immunology, 78, pp.346-354.
valuable initiatives that will help Abdel-Latif, H.M., Abdel-Tawwab,
develop the use of these phytogenic M., Khafaga, A.F. and Dawood,
compounds in the future is the M.A., 2020. Dietary oregano
stabilization of various phytogenic essential oil improved the growth
compounds such as volatile essential oils performance via enhancing the
using methods such as matrix- intestinal morphometry and hepato-
encapsulation. This allows these renal functions of common carp
compounds to remain active in more (Cyprinus carpio L.)
parts of the gastrointestinal tract (GIT) fingerlings. Aquaculture, 526,
and their positive effects are not limited pp.735432.
to a small part of the GIT (Goncalves Adel, M., Amiri, A.A., Zorriehzahra,
and Santos, 2015). J., Nematolahi, A. and Esteban,
Despite numerous reports of the M.Á., 2015a. Effects of dietary
benefits of using phytogenic compounds peppermint (Mentha piperita) on
in experimental studies, inconsistencies growth performance, chemical body
in their effects on host growth and composition and hematological and
systemic safety and a lack of immune parameters of fry Caspian
understanding of how they work in white fish (Rutilus frisii kutum). Fish
intestinal health and intestinal and Shellfish Immunology, 45(2),
microbiota have led to limitations in the pp.841-847.
use of these compounds in aquatic Adel, M., Safari, R., Pourgholam, R.,
animals. Generally, further studies are Zorriehzahra, J. and Esteban,
needed to introduce and develop M.Á., 2015b. Dietary peppermint
sustainable prevention strategies to use (Mentha piperita) extracts promote
phytogenic compounds to enhance host growth performance and increase the
immunity, stress resistance, and the main humoral immune parameters
prevention of pathogenesis in (both at mucosal and systemic level)
aquaculture. of Caspian brown trout (Salmo trutta
caspius Kessler, 1877). Fish and
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