3. Use of immunostimulants in shrimp culture: An update

Research Signpost

37/661 (2), Fort P.O. Trivandrum-695 023

Kerala, India

Biotechnological Advances in Shrimp Health Management in the Philippines, 2015: 45-71

ISBN: 978-81-308-0558-0 Editors: Christopher Marlowe A. Caipang, Mary Beth I. Bacano-Maningas and Fernand F. Fagutao

3. Use of immunostimulants in shrimp

culture: An update

Mary Jane S. Apines-Amar1 and Edgar C. Amar2 1Institute of Aquaculture, College of Fisheries and Ocean Sciences, University of the Philippines

Visayas, Miagao, Iloilo, Philippines; 2Aquaculture Department, Southeast Asian Fisheries Development Center, Tigbauan, Iloilo, Philippines

Abstract. Different approaches are used to prevent and control diseases in aquaculture. Immunostimulation is one method that is gaining popularity and is considered a promising development in aquaculture. Immunostimulants were found to be effective in enhancing parameters of non-specific immunity and resistance to diseases of fish and crustaceans. However, some issues raised on the use of immunostimulants pertains to the short-term nature of

immune indices used during efficacy evaluation, possible detrimental effects during long-term administration, or self-damage due to unregulated production of immune effectors. Further testing in large-scale production units has been recommended. This chapter presents the various types and sources of immunostimulants commonly used in aquaculture and in shrimp culture in particular. The effects of each immunostimulant vary depending on its source, dose, route of administration, length of exposure, and the species to

which it is administered.

Correspondence/Reprint request: Dr. Mary Jane S. Apines-Amar, Institute of Aquaculture, College of Fisheries

and Ocean Sciences, University of the Philippines, Visayas, Miagao, Iloilo, Philippines

E-mail: [email protected]

Mary Jane S. Apines-Amar & Edgar C. Amar 46

Introduction

Shrimp farming has been practiced in many countries for decades.

However, the increasing global demand for shrimp has led to the

intensification of shrimp culture that is one of the major contributory factors in the emergence of infectious diseases. The causative agents of infectious

diseases in shrimp are mainly viruses and bacteria. Vibrio spp. contribute to

a number of epizootic diseases causing serious problems in shrimp culture

and are responsible for shrimp mass mortalities (Nash et al 1992).

Vaccination in fish and immunostimulation both in shrimp and fish for

disease management are being increasingly appreciated in the aquaculture

industry. To fight against diseases, fish larvae and aquatic invertebrates rely

on their innate immune system (Kurtz & Franz 2003; Little & Kraaijeveld

2004) consisting of cellular and humoral components that cooperate to

recognize and eliminate foreign microorganisms and pathogens (Bachère

2003).

Approaches employed to prevent/control fish diseases include the use

of vaccines, chemotherapeutics, and immunostimulants. Immunostimulants

and vaccines are used as prophylactic interventions. They are not

recommended for use when disease is already present in the host.

Chemotherapeutants, on the other hand, are effective for teatment of

diseases that has already occurred, but they are often subject to abuse and

leave residues that affect product quality, among other issues. Vaccination

is the most reliable method, however, there are no effective vaccines

against most viral diseases. In crustaceans, vaccination is the subject of

ongoing investigations but an efficacious product is not expected to be

available for commercial application in the immediate future.

Immunostimulants may compensate for the limitations of

chemotherapeutants and vaccines. They have modulatory effects on the immunocompetence and disease resistance of fish and crustaceans. When

combined with vaccination, immunostimulation may also increase the

potency of vaccines. Thus, the use of immunostimulants for health

management is a promising new development in shrimp aquaculture (Jadhav et al 2006; Barman et al 2013).

The shrimp immune system

The immune system of shrimp is relatively primitive/less well-

developed when compared to that of fish. Invertebrates such as shrimp lack

an antibody-based vertebrate-type adaptive immune system. Thus, non-specific

Use of immunostimulants in shrimp culture: An update 47

immune responses are considered to play crucial roles in the shrimp defence

against pathogens. The induction of innate or non-specific immunity is therefore a potentially better tool to combat pathogens present in the culture

system compared to vaccination, for example. Phagocytosis, encapsulation,

nodule formation, cytotoxicity, lectins, antimicrobial proteins or peptides,

and prophenoloxidase (proPO), have been confirmed to perform essential

roles in the immune defence of shrimps (Soderhall & Cerenius 1992;

Iwanaga & Lee 2005; Amar & Almendras 2010). In recent years, many

studies conducted in crustaceans and insects provide evidence supporting the

existence of specificity and memory mediated by highly variable receptors in

the immune system in these taxonomic groups (Rowley & Powell, 2007).

However, this phenomenon was not found to be universal in the crustacean

species studied and appears to be pathogen- and host-specific. Moreover, it

is not clear at the moment how this specific immune response can provide practical benefits for health improvement in shrimp aquaculture.

What are immunostimulants?

Immunostimulants are substances that activate the immune system of

animals to make them more resistant to microbial infections (Raa 1996). The

definition has been expanded somewhat to include live organisms or their

products that have an impact on the immune system. The use of

immunostimulants does not generate a specific response to a certain antigen,

but causes an overall response that hastens recognition and elimination of a

broad range of infectious agents and foreign substances (Campos et al 1993; Secombes 1994; Sordello et al 1997). Two categories of conserved molecular

patterns are recognized by the innate immunity through the various patttern

recognition receptors (PRRs): (1) non-self or pathogen-associated molecules;

and (2) molecules generated as a result of damage to the host's own tissues

signalling danger to the immune system (Matzinger 1998; Medzhitov &

Janeway 2002). Pattern recognition is the first step in innate immunity.

Immunostimulants, like the presence of infection, are sensed by the various

PRRs. So far, 11 types of pattern recognition receptors have been identified in

shrimp namely, -1,3-glucanase-related proteins, -1,3-glucan-binding proteins, c-type lectins, scavenger receptors, galectins, fibrinogen-related

proteins, thioester-containing Down syndrome cell adhesion molecules, serine

protease homologs, trans-activation response RNA-binding protein, and Toll-

like receptors. Aside from pattern recognition, these PRRs have different binding specificities and effector functions (Wang & Wang 2013).

Immunostimulation can strengthen the immune system of farmed aquatic

animals and increase their resistance to pathogens during exposure to stress,


such as handling, crowding, sampling, transport, vaccination, during

reproduction, and also during the larval stages when high levels of mortality occur. Some commercially available immunostimulants are shown in Table 1.

Sources of immunostimulants

Bacterial preparations

Vibrio - is a curved rod-shaped gram-negative bacteria. Vibrio

anguillarum is a very efficient vaccine for salmonid fish (Johnson et al 1982;

Norqvist et al 1989; Sakai et al 1995). The immunostimulant effects of

inactivated Vibrio cells have been documented in shrimp (Itami et al 1989,

1991, 1992; Horne et al 1995; Teunissen et al 1998; Pereira et al 2009; Powell

et al 2011; Lin et al 2013). The authors reported that injection or immersion of

shrimp in Vibrio bacterin resulted in reduced mortality suggesting

immunostimulation by the ”vaccine” as invertebrates do not have an efficient

specific immune response. The immunostimulation is mediated by the PRRs

that recognize and bind stimulatory components in bacteria. Vibrio bacterin

may therefore act as an immunostimulant since non-specific immune cells such as phagocytic hemocytes are activated (Sakai 1999). A Vibrio harveyi

bacterin was also able to protect P. monodon against WSSV infection

(George et al 2006).

Lipopolysaccharide (LPS) - also known as lipoglycans or endotoxins

are large molecules consisting of a lipid and a polysaccharide joined by a

covalent bond. They are the major component of the outer membrane of

gram-negative bacteria, are responsible for the structural integrity of the

bacteria, and stimulate strong immune responses in recipient hosts. The

lipid component in association with the main polysaccharide is responsible

for the biological activities of LPS (Rietschel et al 1993). The

immunostimulant effects of LPS have been demonstrated in fish (Salati

et al 1987; Neumann et al 1995; Nya et al 2010) and shrimp (Vargas-

Albores et al 1998; Newman 2000; Felix 2005). LPS, at low doses,

improves disease resistance and acts as a prophylactic agent (Noworthy

1983). Rungrassame et al., (2013) found that shrimp fed LPS-containing

diet exhibited significantly higher survival rates when exposed to

V. harveyi than those fed the normal diet. Some crucial immune-related

transcripts such as anti-lipopolysaccharide factor 3 (ALF3), C-lectin and mucin-

like peritrophin were also induced in shrimp digestive tracts by the LPS

supplement. These findings led the authors to conclude that LPS

supplement is a promising candidate to increase disease resistance in black

tiger shrimp farming.


Live bacteria: probiotics as immunostimulants – A number of studies

revealed that the supplementation of probiotic bacteria and commercial

probiotics in feed or any sort of inclusion can boost the cellular and

humoral components of the innate immune system in several species of

fish and shellfish including salmonids and shrimps (Gullian et al 2004;

Panigrahi et al 2004, 2005, 2007; Song et al 2006; Balcazar et al 2006,

2007a, 2007b; Rodrıguez et al 2007; Pais et al 2008; Goncalves et al 2011;

Biswas et al 2013; Cerezuela et al 2013; Meena et al 2013; Perez-Sanchez

et al 2013; De et al 2014). Immunostimulation by Bacillus S11 bacteria

increased phagocytic activity in Penaeus monodon (Rengpipat et al 2000),

whereas the administration of Lactobacillus plantarum stimulated

phenoloxidase and superoxide dismutase activities leading to enhanced

clearance efficiency of Vibrio alginolyticus in Litopenaeus vannamei (Chiu

et al 2007). Complex carbohydrates

Glucans - are natural biomolecules with immunomodulatory activity. In

vertebrates, glucans modulate the immune response through the macrophage

and dendritic immune cells. The amount or dose of glucans does not

determine its effectiveness as sources, processing, size and uniformity of

glucan particles are the actual determinants of its efficacy

(www.betaglucan.com). Enhancement of immune responses and protection

against infectious agents by treatment with beta-glucans were observed in

fish (Robertsen et al 1990; Raa et al 1992; Engstad & Robertsen 1993;

Sahoo & Mukherjee 2002; Selvaraj et al 2005; Rodriguez et al 2009; Skov

et al 2012; Meena et al 2013; Vetvicka et al 2013) as well as in shrimp (Song

& Hsieh 1994; Sung et al 1994; Chang et al 2000, 2003; Wang et al 2008).

In shrimp aquaculture, the most widely used immunostimulants are glucan-

based (Nahavandi et al 2010).

Prebiotics as immunostimulants – prebiotics are indigestible fibers that

increase beneficial gut commensal bacteria resulting in improvements of the

host’s health (Song et al 2014). Prebiotics such as fructooligosaccharide

(FOS), mannan oligosaccharide (MOS), inulin, or -glucan are called

immunosaccharides bacause they directly enhance innate immune responses

including phagocytic activation, neutrophil activation, stimulation of the

alternative complement system, and increased lysozyme activity (Song et al

2014).

http://www.betaglucan.com/


Nutritional factors

Vitamins - dietary supplementation of vitamins such as A, C, and E is

effective in increasing the immunocompetence and disease resistance of

fish (Waagbo et al 1992; Mulero et al 1998; Verlhac et al 1998; Ortuno et al 1999, 2000; Cuesta et al 2001; Sahoo & Mukherjee 2002; Tewary &

Patra 2008). Vitamins A, C, and E in combination with dietary carotenoids

were found to enhance the complement, lysozyme, and phagocytic

activities in fish (Amar et al 2001). Improved immune function and

resistance to pathogens were also demonstrated in several species of

penaeid shrimp that received vitamins A, C, and E supplements (Merchie

et al 1998; Lee & Shiau 2002, 2003, 2004; Nahavandi et al 2010;

Sivakumar & Felix 2011).

Carotenoids - the role of carotenoids in the immune response of

animals has been established (Chew 1993). Carotenoids improve

lymphocyte blastogenesis, lymphocyte cytotoxicity activity and stimulate the production of certain cytokines. Carotenoids also stimulate the

phagocytic and bacterial killing ability of neutrophils and macrophages. In

fish, dietary carotenoids have been reported to heighten immune responses

and increase disease resistance (Christiansen et al 1995; Tachibana et al

1997; Amar et al 2000, 2001, 2004, 2012). Similarly in shrimp,

supplementation of dietary carotenoids resulted in increased resistance to

stress, salinity shock, and increased the antioxidant response before and

after viral infection (Merchie et al 1998; Nahavandi et al 2010; Pacheco

et al 2011).

Trace elements - deficiencies in trace elements with antioxidant

function (cofactors of numerous enzymes) such as zinc (Zn), copper (Cu),

manganese (Mn) and selenium (Se) have been reported to depress

immunity in animals. Deficiency in Zn, Mn and Cu were found to reduce

the natural killer-like activity of leukocytes and antibody production in fish

(Kiron et al 1993; Paripatananont and Lovell 1995a; Inoue et al 1998).

Dietary Zn and Se protected fish against Edwardsiella ictaluri infection

(Paripatananont and Lovell 1995b; Wang et al 1997). Enhanced lysozyme

activity and total immunoglobulin level, and improved antibody production

and survival were exhibited by rainbow trout supplemented with amino

acid-chelated trace elements (Apines-Amar et al 2004). Likewise,

supplementation of Cu in tiger shrimp resulted in improved growth, total

hemocyte count, and superoxide anion production (Lee & Shiau 2002). A

similar improvement of immune responses was observed in white shrimp

upon dietary suplementation with Zn (Lin et al 2013).


Animal sources/extracts

Chitin/Chitosan - chitin is one of the most abundant polysaccharides in

nature, and a common constituent of insects, crustacean exoskeletons, and

fungal cell walls (Esteban et al 2000). Chitosan is the product of alkaline deacetylation of chitin obtained from crustacean shells. Injection, immersion,

and oral administration of chitin and chitosan have been reported to protect

fish and shrimp against bacterial infection (Sakai et al 1992; Siwicki et al

1994; Anderson et al 1995; Wang and Chen 2005; Huxley et al 2010, 2011).

Plant sources/extracts

Seaweeds - plants including seaweeds are rich sources of safe and

inexpensive chemical compounds. Products derived from plants exhibit

various activities and are utilized as anti-stress agents, growth promoters,

appetizers, tonics, immunostimulants and antimicrobials (Citarasu et al

2002; Immanuel et al 2004). Red seaweeds contain biologically active

sulphated, galactose-based polysaccharides, and show antibacterial and

antiviral activities (Renn 1997; Rajasulochana et al 2009; Wongprasert et al 2013). Rudtanatip et al (2014) reported that sulfated galactans from

Gracilaria fisheri elicits anti-WSSV activity by binding to viral proteins

which are essential structures for viral attachment to host cells. Fucoidan, a

sulfated polysaccharide from brown algae (e.g, Fucus, Laminaria) activated

the immune system and increased the resistance to viral infection in penaeid

shrimp (Nahavandi et al 2010). An extract from Gracilaria tenuistipitata

exhibited protection in shrimp against WSSV as evidenced by the higher

survival rate and heightened immune responses (Lin et al 2011). Likewise,

white shrimp Litopenaeus vannamei immersed in seawater containing brown

seaweed Sargassum hemiphyllum var. chinense powder or its extract showed

improved immunity and resistance against Vibrio alginolyticus and WSSV infections (Huynh et al 2011).

Herbs – the benefits of herbs such as onion, ginger, and garlic on human

health are well-recognized. Enhanced immune responses and resistance to

diseases were recently demonstrated in fish and shrimp supplemented with

either onion, ginger, or garlic (Dugenci et al 2003; Nya & Austin 2009,

2011; Chang et al 2012; Apines-Amar et al 2012, 2013; Aruvasu et al 2013;

Haghighi & Rohani 2013; Talpur et al 2013; Kanani et al 2014). Elevated

expression of the immune-related genes Penaeidin, Crustin, Lysozyme,

Toll-receptor, and tumour necrosis factor was detected in kuruma shrimp

upon stimulation with garlic (allicin) extract (Tanekhy and Fall 2015). The

methanolic extracts of different herbal medicinal plants like Cyanodon


dactylon, Aegle marmelos, Tinospora cordifolia, Picrorhiza kurooa and

Eclipta alba were found to be effective against white spot syndrome virus (WSSV) infection in shrimp (Citarasu et al 2006).

Hormones/cytokines

Growth hormone (GH) – is a peptide hormone (also known as

somatotropin or somatropin) that stimulates growth and cell reproduction in

humans and other animals. Growth hormone has numerous beneficial effects

such as promotion of lipolysis, gluconeogenesis, increase in protein

synthesis and stimulation of immune responses among others. The influence

of GH on the immune responses of fish have been studied (Harris & Bird

2000; Yada et al 2002, 2004, 2007; Peterson et al 2007). A recombinant

bovine growth hormone was found to enhance growth and immunity in

shrimp larvae (Kang et al 2005).

Lactoferrin (LF) - formerly known as lactotransferrin (LTF), is a

glycoprotein and a component of the innate immune system. Lactoferrin

influences the growth and proliferation of various pathogens such as

bacteria, viruses, protozoa, or fungi (Kirkpatrick et al 1971). LF affects

mainly the respiratory burst and natural cytotoxic activities in fish (Esteban

et al 2005).The antimicrobial activities of lactoferrin have been reviewed by

Adlerova et al (2008). In crustaceans, dietary administration of bovine

lactoferrin enhanced immune indices and resistance against Aeromonas

haydrophila challenge in Macrobrachium rosenbergii (Chand et al 2006).

Synthetic sources

Levamisole - known under the tradename Ergamisol, was originally

synthesized as an anti-helminthic and has been widely used as an

immunomodulator belonging to imidazothiazole derivatives. Levamisole has

been used in humans to treat parasitic worm infections, and has been studied in

combination with other forms of chemotherapy for colon cancer, melanoma,

and head and neck cancer. Oral administration of levamisole resulted in

enhanced immunity and improved resistance to diseases in fish (Siwicki 1987,

1989; Siwicki et al 1990; Kajita et al 1990; Sivakumar & Felix 2011). Oral

administration of levamisole likewise resulted in increased protection against

bacterial infection in tiger shrimp (Huxley et al 2010, 2011). CpG Oligodeoxynucleotide (CpG ODN) – are short single-stranded

synthetic DNA molecules containing cytosine triphosphate deoxynucleotide


"C" followed by a guanine triphosphate deoxynucleotide "G" with phosphodiester "p" linking the two nucleotides. CpG motifs are considered pathogen-associated molecular patterns (PAMPs). CpG motifs are more

prevalent in bacterial DNA, and when unmethylated, function as

immunostimulants (Krieg et al 1995; Weiner et al 1997). In contrast, the DNA

of vertebrates are deficient in CpG motifs and highly methylated. Recently,

nucleotides have received much attention as potential immunomudulators. Li

& Gatlin (2006) has reviewed nucleotide nutrition in fish. The beneficial

influences of oral administration of nucleotides on immune functions, vaccine

efficiency or disease resistance have been demonstrated in fish (Ramadan et al

1994; Burrells et al 2001; Sakai et al 2001; Li & Gatlin 2006). It must be

pointed out that the nucleotides in the diets of farmed aquatic animals are

added to provide the supply of nucleotides (as nutrient) necessary to enhance

growth and survival especially under conditions of high requirement or stressful events, whereas CpG is a PAMP and is a non-nutrient nucleotide.

Nevertheless, even nucleotides without CpG motifs can be sensed as non-self

molecules, such as in cases of autoimmune reactions. Increased immune

indices have been reported in shrimp injected with ODNs with or without CpG

motifs (Amar & Faisan 2012).

Table 1. Some currently available commercial immunostimulants.


Effects of immunostimulants

Upregulated immune indices such as total hemocyte count, respiratory

burst, phenoloxidase activity, phagocytic activity, agglutination titer, lysozyme

and SOD activities, etc. have been reported in many immunostimulation

studies (Table 2). Growth-promoting activity was also found with some

immunostimulants (Song & Hsieh 1994). Growth enhancement could result from improved disease resistance due to immunostimulant supplementation.

Shrimp fed with peptidoglycan-supplemented feed also showed better growth

and feed conversion rates than those fed a normal diet (Boonyaratpalin et al.,

1995). Sung et al (1994) demonstrated that black tiger shrimp grew faster with

glucan immersion which could be attributed to the higher activity of glucan

delivered by immersion compared to oral administration.

Table 2. Various types of immunostimulants studied in shrimp.


Table 2. Continued


Table 2. Continued

Methods and strategies in using immunostimulants

Immunostimulants can be administered through injection, immersion, or

oral administration. Injection and immersion require handling of fish/shrimp

or confining them in a small area during application. However, these methods are laborious, time-consuming, and stressful. Injection method is

the most cost-effective method for large fish (>10g). Immersion on the other

hand, is not as effective as injection but allows mass immunostimulation and

is the most cost-effective method for smaller fish (<5g). Oral

immunostimulation is a non-stressful method that can be used with any size

of fish but requires a large amount of immunostimulant to provide

protection. Furthermore, this method is applicable only for fish fed artificial

diet.


The outcome of using an immunostimulant is usually determined by the

strategy by which it is applied (Bricknell & Dalmo 2005). Continuous use of an immunostimulant may up-regulate the immune system and maintain this

status until the immunostimulant is withdrawn, or it may cause adverse

effects such as tolerance or immunosuppression. On the other hand, pulse

administration (administering immunostimulant-supplemented and

non-supplemented diets alternately) oscillate the immune response from a

resting level to a heightened response then back to resting, and has been

shown to be a better strategy of immunostimulant application.

Some issues in the use of immunostimulants in shrimp

Lack of correlation of in vitro and in vivo studies. Some

immunostimulants may enhance the non specific immune response in vitro but this does not always result in improved health or increased survival.

Some immunostimulants do not show a linear dose/effect relationship; they

could be effective at a certain optimum concentration but have no effect or

exhibit toxicity at higher concentrations. Consequently, doses determined

in vitro cannot be directly extrapolated to large-scale production systems.

Hence, these immunostimulants may end up being fed at high doses or for

long durations resulting in chronic overstimulation and exhaustion of the

immune system.

There is lack of unequivocal evidence on the effficacy of some products.

Most studies on immune stimulation by microbial polysaccharides claim

beneficial effects by improving growth and resistance to pathogen challenge, and/or stimulation of immune responses such as prophenoloxidase,

antibacterial, antioxidant, and agglutinaton activity, and reactive oxygen

production. However, these effects are short term, and there are very few

studies conducted in large-scale production units on a longer duration. With

particular immunostimulants, some studies reported beneficial effects,

whereas no positive effects were found by others.

Some immune responses are detrimental. Essentially, the haemocytes

perform inflammatory-type reactions such as phagocytosis, haemocyte

clumping, production of reactive oxygen metabolites, and the release of

microbicidal proteins. Under normal conditions, the inactive form of effector

molecules are stored in the hemocytes but are released into the hemolymph

through exocytosis and activated upon stimulation by non-self molecules. In the open circulatory system of crustaceans, immune reactions must be

localized to avoid self-damage. Some of the responses and reactions that are

potentially self-harming include degranulation of hemocytes, cell clumping

and hemacytopenia, cytotoxicity at higher doses, depletion of immune


effectors, immune exhaustion by repeated immunostimulation, and high

energetic cost of regenerating immune components (Smith 2008). With these possible adverse consequences, a rigorous product testing on a large scale

over a duration spanning the whole crop cycle is essential. The capacity of

the products to upregulate immunity genes should also be considered with

the objective of correlating in vitro and in vivo results. Lastly, stimulation

that elicits alternative molecules that have no self-harming potential but have

direct effect on the pathogens (such as antimicrobial peptides) should be

pursued.

References

1. Adlerova L., Bartoskova A., Faldyna M., 2008 Lactoferrin: a review. Vet Med 53:457–468.

2. Amar E. C., Almendras J.M., 2010 Immunity and biological methods of disease prevention and control. In: G. D. Lio-Po and Y. Inui (eds). Health Management and Aquaculture, 2nd Edition, pp. 229-258. Southeast Asian Fisheries Development Center, Aquaculture Department, Tigbauan, Iloilo, Philippines.

3. Amar E. C., Faisan Jr J. P., 2012 Induction of immunity and disease resistance to white spot syndrome virus (WSSV) in shrimp, Penaeus monodon (Fabricius) by

synthetic oligodeoxynucleotide and bacterial DNA. Phil Agri Sci 95:169-174. 4. Amar E. C., Kiron V., Akutsu T., Satoh S., Watanabe T., 2012 Resistance of

rainbow trout, Oncorhynchus mykiss to infectious hematopoietic necrosis virus (IHNV) experimental infection following ingestion of natural and synthetic carotenoids. Aquaculture, 330-333:148-155.

5. Amar E. C., Kiron V., Satoh S., Watanabe T., 2001 Influence of various dietary synthetic carotenoids on bio-defense mechanisms in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquacult Res 32:162-173.

6. Amar E. C., Kiron V., Satoh S., Watanabe T., 2004 Enhancement of innate immunity in rainbow trout, Oncorhynchus mykiss associated with dietary intake of carotenoids from natural products. Fish Shellfish Immunol 16:527-537.

7. Amar E. C., Kiron V., Satoh S., Okamoto N., Watanabe T., 2000 Effects of dietary beta-carotene on the immune response of rainbow trout, Oncorhynchus mykiss. Fish Sci 66:1068-1075.

8. Anderson D. P., Siwicki A. K., 1994 Duration of protection against Aeromonas salmonicida in brook trout immunostimulated with glucan or chitosan by

injection or immersion. Progressive Fish-Culturist 56:258-261. 9. Anderson D. P., Siwicki A. K., Rumsey G. L., 1995 Injection or immersion

delivery of selected immunostimulants to trout demonstrate enhancement of nonspecific defense mechanisms and protective immunity. In: Shariff M., Subasinghe R. P., Arthur J. R. (eds). Diseases in Asian aquaculture, vol. 11. Manila, Philippines: Fish Health Section, Asian Fisheries Society p. 413-426.

10. Apines-Amar M. J. S., Amar E. C., Faisan Jr. J. P., 2013 Growth, plasma cortisol, liver and kidney histology, and resistance to vibriosis in brown-marbled


grouper, Epinephelus fuscoguttatus fed onion and ginger. AACL Bioflux 6(6):530-538.

11. Apines Amar M. J. S., Amar E. C., Faisan Jr. J. P., Pakingking Jr. R. V., Satoh S., 2012 Dietary onion and ginger enhance growth, hemato-immunological responses, and disease resistance in brown-marbled grouper, Epinephelus fuscoguttatus. AACL Bioflux 5(4):231-239.

12. Apines-Amar M. J. S., Satoh S., Kiron V., Watanabe T., 2004 Effects of

supplemental amino acid–chelated trace elements on the immune response of rainbow trout subjected to bacterial challenge. J Aquat Anim Health 16:53–57.

13. Apines-Amar M. J. S., Andrino K. G. S., Amar E. C., Cadiz R. E., Corre Jr. V. L., 2014 Improved resistance against White Spot Virus (WSV) infection in tiger shrimp, Penaeus monodon by combined supplementation of peptidoglycan and mannan oligosaccharide (MOS). ELBA Bioflux 6(1):1-9.

14. Arulvazu C., Mani K., Chandhirasekar D., Prabhu D., Sivignanam S., 2013 Effect of dietary administration of Zingiber officinale on growth, survival and immune response of Indian major carp, Catla catla (Ham). Int J Pharm Pharm

Sci 5(Suppl 2):108-115. 15. Bachère E., 2003 Anti-infectious immune effectors in marine invertebrates:

Potential tools for disease control in larviculture. Aquaculture 227:427-438. 16. Balcazar J. L., de Blas I., Ruiz-Zarzuela I., Cunningham D., Vendrell D.,

Muzquiz J. L., 2006 The role of probiotics in aquaculture. Vet Microbiol 114:173–186.

17. Balcazar J. L., de Blas I., Ruiz-Zarzuela I., Vendrell D., Girones O., Muzquiz J. L. 2007a Enhancement of the immune response and protection induced by

probiotic lactic acid bacteria against furunculosis in rainbow trout (Oncorhynchus mykiss). FEMS Immunol Med Microbiol 51: 185–193.

18. Balcazar J. L., Rojas-Luna T., Cunningham D. P. 2007b Effect of the addition of four potential probiotic strains on the survival of pacific white shrimp (Litopenaeus vannamei) following immersion challenge with Vibrio parahaemolyticus. J Invert Pathol 96:147–150.

19. Barman D., Nen P., Mandal S.C., Kumar V., 2013 Immunostimulants for Aquaculture Health Management. J Mar Sci Res Dev 3:134. doi: 10.4172/2155-

9910.1000134. 20. Biswas G., Korenaga H., Nagamine R., Takayama H., Kawahara S., Takeda S.,

Kikuchi Y., Dashnyam B., Kono T., Sakai M., 2013 Cytokine responses in the Japanese pufferfish (Takifugu rubripes) head kidney cells induced with heat-killed probiotics isolated from the Mongolian dairy products. Fish Shellfish Immunol 34(5):1170–1177.

21. Boonyaratpalin S., Boonyaratpalin M., Supamattaya K., Toride Y., 1995 Effects

of peptidoglucan PG on growth, survival, immune responses, and tolerance to

stress in black tiger shrimp, Penaeus monodon. In: Shariff M., Subasighe R.P.,

Arthur J.R. Eds.., Diseases in Asian Aquaculture Vol. 11. Fish Health Section,

Asian Fisheries Society, Manila, Philippines, pp. 469–477.

22. Bricknell I., Dalmo R. A., 2005 The use of immunostimulants in fish larval

aquaculture. Fish Shellfish Immunol 19:457-472.


23. Burrells C., William P. D., Forno P. E., 2001 Dietary nucleotides: a novel supplement in fish feeds. 1. Effects on resistance to disease in salmonids. Aquaculture 199:159-169.

24. Campos M., Godson D., Hughes H., Babiuk L., Sordillo L., 1993 The role of biological response modifiers in disease control. J Dairy Sci 76:2407-2417.

25. Cerezuela R, Meseguer J, Esteban M A (2013) Effects of dietary inulin, Bacillus subtilis and microalgae on intestinal gene expression in gilthead seabream

(Sparus aurata L.). Fish Shellfish Immunol 34:843–848. 26. Chand R. K., Sahoo P. K., Kumari J., Pillai B. R., Mishra B. K., 2006. Dietary

administration of bovine lactoferrin influences the immune ability of the giant freshwater prawn Macrobrachium rosenbergii (de Man) and its resistance against Aeromonas hydrophila infection and nitrite stress. Fish Shellfish Immunol 21:119-121.

27. Chang C. F., Chen H. Y., Su M. S., Liao I. C., 2000 Immunomodulation by dietary ß-1,3-glucan in the brooders of the black tiger shrimp Penaeus monodon. Fish Shellfish Immunol 10:505-514.

28. Chang C. F., Su M. S., Chen H. Y., Liao I. C., 2003 Dietary ß-1,3-glucan effectively improves immunity and survival of Penaeus monodon challenged with white spot syndrome virus. Fish Shellfish Immunol 15:297-310.

29. Chang Y-P., Liu C-H., Wu C-C., Chiang C-M., Lian J-L., Hsieh S-L., 2012 Dietary administration of zingerone to enhance growth, non-specific immune response, and resistance to Vibrio alginolyticus in Pacific white shrimp (Litopenaeus vannamei) juveniles. Fish Shellfish Immunol 32:284-290.

30. Chang M-X., Zou J., Nie P., Huang B., Yu Z., Collet B., Secombes C. J., 2013

Intracellular interferons in fish: a unique means to combat viral infection. PLoS Pathog 9(11): e1003736. doi:10.1371/journal.ppat.1003736.

31. Chen X., Lin H. Z., Jiang S. G., Wu K. C., Liu Y. J., Tian L. X., Zhang Y. Q., Niu J., 2013 Dietary supplementation of honeysuckle improves the growth, survival and immunity of Penaeus monodon. Fish Shellfish Immunol 35(1):161-169.

32. Cheng W., Liu C. H., Yeh S. T., Chen J. C., 2004 The immune stimulatory effect of sodium alginate on the white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Fish Shellfish Immunol 17(1):41-51.

33. Cheng W., Liu C. H., Kuo C. M., Chen J. C., 2005 Dietary administration of sodium alginate enhances the immune ability of white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus.

34. Chew B. P., 1993 Role of carotenoids in the immune response. J Dairy Sci

76:2804-2811.

35. Chiu C. H., Guu Y. K., Liu C. H., Pan T. M., Cheng W., 2007 Immune responses and gene expression in white shrimp Litopenaeus vannamei, induced by Lactobacillus plantarum. Fish Shellfish Immunol 2:364-377.

36. Citarasu T., Sekar R. R., Babu M. M., Marian M.P., 2002 Developing Artemia

enriched herbal diet for producing quality larvae in Penaeus monodon. Asian

Fish Sci 15:21-32. 37. Citarasu T., Sivaram V., Immanuel G., Rout N., Murugan V., 2006 Influence of

selected Indian immunostimulant herbs against white spot syndrome virus


(WSSV) infection in black tiger shrimp, Penaeus monodon with reference to haematological, biochemical and immunological changes Fish Shellfish Immunol 21: 372-384.

38. Christiansen R., Glette J., Lie Ø., Torrissen, O. J., Waagbø R., 1995 Antioxidant

status and immunity in Atlantic salmon, Salmo salar L., fed semi-purified diets

with and without astaxanthin supplementation. J Fish Dis 18:317–328.

39. Cuesta A., Esteban M. A., Ortuño J., Meseguer J., 2001 Vitamin E increases

natural cytotoxic activity in sea bream (Sparus aurata L.). Fish Shellfish

Immunol 11: 293-302.

40. De B. C., Meena D. K., Behera B. K., Das P., Mohapatra P.K.D., Sharma A. P.

2014 Probiotics in fish and shellfish culture: immunomodulatory and

ecophysiological responses. Fish Physiol Biochem 40(3):921-971.

41. Devaraja T. N., Otta S. K., Shubha G., Karunasagar I., Tauro P., Karunasagar I.,

1998 Immunostimulation of shrimp through oral administration of Vibrio

bacterin and yeast glucan. In Flegel T. W. (ed) Advances in shrimp

biotechnology. National Center for Genetic Engineering and Biotechnology,

Bangkok.

42. Dugenci S. K., Arda N., Candan A., 2003 Some medicinal plants as

immunostimulant for fish. J Ethnopharmacol 88:99-106.

43. Engstad R. E., Robertsen B., 1993 Recognition of yeast cell wall glucan by

Atlantic salmon (Salmo salar L.) macrophages. Dev Comp Immunol 17:319-330.

44. Esteban M. A., Mulero V., Cuesta A., Ortuño J., Meseguer J., 2000 Effects of

injecting chitin particles on the innate immune response of gilthead seabream

(Sparus aurata L.). Fish Shellfish Immunol 10:543-554.

45. Esteban M. A., Rodríguez A., Cuesta A., Meseguer J., 2005 Effects of lactoferrin on non-specific immune responses of gilthead seabream (Sparus auratus L.). Fish Shellfish Immunol 18(2):109-124.

46. Felix S., 2005 Pro-PO based immunomodulatory effect of glucan and LPS on

tiger shrimp, Peneaus monodon (Fabricus). In: Walker P., Lester R., Bondad-

Reantaso M.G. (eds). Diseases in Asian Aquaculture V, pp. 477-482. Fish

Health Section, Asian Fisheries Society, Manila.

47. Felix S., Herald Robins P., Rajeev A., 2004 Immune enhancement assessment

of dietary incorporated marine algae Sargassum wightii

(Phaeophyceae/Punctariales) in tiger shrimp Penaeus monodon

(Crustacea/Penaeidae) through prophenoloxidase (proPO) systems. Indian J Mar

Sci 33(4):361-364.

48. George M. R., Maharajan A., Riji John K., Prince Jeyaseelan M. J., 2006

Shrimps survive white spot syndrome virus challenge following treatment with

vibrio bacterin. Indian J Expt Biol 44:63-67.

49. Gonçalves A. T., Maita M., Futami K., Endo M., Katagiri T., 2011 Effects of a

probiotic bacterial Lactobacillus rhamnosus dietary supplement on the crowding

stress response of juvenile Nile tilapia Oreochromis niloticus. Fisheries Science

77(4):633-642.


50. Gullian M., Thompson F., Rodriguez J., 2004 Selection of probiotic bacteria and study of their immunostimulatory effect in Penaeus vannamei. Aquaculture 233:1–14.

51. Haghighi M., Rohani M. S., 2013 The effects of powdered ginger (Zingiber officinale) on the haematological and immunological parameters of rainbow trout Oncorhynchus mykiss. J Med Plant Herbal Ther Res 1:8-12.

52. Harris J., Bird D. J., 2000 Modulation of the fish immune system by hormones.

Vet Immunol Immunopathol 77(3-4):163-176. 53. Horne M. T., Poy M., Pranthanpipat P., 1995 Control of vibriosis in black tiger

shrimp, Penaeus monodon, by vaccination. In: Chou et al eds., The Third Asian Fisheries Forum. Asian Fisheries Society, Manila, Philippines, pp. 459–467.

54. Huang C. C., Song Y. L., 1999 Maternal transmission of immunity to white spot syndrome associated virus (WSSV) in shrimp (Penaeus monodon). Dev Comp Immunol 23:545-552.

55. Huxley V. A. J., John J., Suthan P., Lipton A. P., 2010 Chitosan and levamisole

induced survival and bacterial disease resistance in tiger shrimp, Penaeus

monodon (Fabricus). Asian J of Anim Sci 5(2):164-167.

56. Huxley V. A. J., Suthan P., Joseph M. V., Lipton A.P., 2011 Immunomodulatory

potential of Chitosan and Levamisole against bacterial diseases of Penaeus

monodon. Asian J of Anim Sci 6(1):33-40.

57. Huynh T-G., Yeh S-T., Lin Y-C., Shyu J-F., Chen L-L., Chen J-C., 2011 White

shrimp Litopenaeus vannamei immersed in seawater containing Sargassum

hemiphyllum var. chinense powder and its extract showed increased immunity

and resistance against Vibrio alginolyticus and white spot syndrome virus. Fish

Shellfish Immunol 31:286-293.

58. Immanuel G., Sivagnanavelmurugan M., Marudhupandi T., Radhakrishnan S.,

Palavesam A., 2012 The effect of fucoidan from brown seaweed Sargassum

wightii on WSSV resistance and immune activity in shrimp Penaeus monodon

(Fab). Fish Shellfish Immunol 32(4):551-564. DOI:10.1016/j.fsi.2012.01.003.

59. Immanuel G., Vincybai V. C., Sivaram V., Palavesam A., Marian M. P., 2004

Effect of butanolic extracts from terrestrial herbs and seaweeds on the survival,

growth and pathogen (Vibrio parahaemolyticus) load on shrimp Penaeus

indicus juveniles. Aquaculture 236(1-4):53-65.

60. Inoue M., Satoh S., Maita M., Kiron V., Okamoto N., 1998 Recovery from

derangement of natural killer-like activity of leucocytes due to Zn or Mn

deficiency in rainbow trout, Oncorhynchus mykiss (Walbaum), by the oral

administration of these elements. J Fish Dis 21:233–236.

61. Itami T., Takahashi Y., Nakamura Y., 1989 Efficacy of vaccination against vibriosis in cultured kuruma prawns Penaeus japonicus. J Aquat Anim Health 1:238–242.

62. Itami T., Takahasi Y., Voneoka K., Yau Y., 1991 Survival of larval giant tiger prawns, Penaeus monodon after addition of killed vibrio cells to a microencapsulated diet, J. Aquat Anim Health 3(2):151-152.

http://www.sciencedirect.com/science/article/pii/S0044848603008275




63. Itami T., Yan Y., Takahashi Y., 1992 Studies on vaccination against vibrios in cultured kuruma prawn, Penaeus japonicus. Effect of different vaccine preparations and oral vaccination efficacy. J Shimonoseki Univ Fish 40(3):139-144.

64. Iwanaga S., Lee B. L., 2005 Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 38:128-150.

65. Jadhav V. S., Khan S. I., Girkar M. M., Gitte M. J., 2006 The role of immunostimulants in fish and shrimp aquaculture. Aquacult Asia XI 3:24-27.

66. Johnson K. A., Flynn J. K., Amend D.F., 1982 Duration of immunity in salmonids vaccinated by direct immersion with Yersinia ruckeri and Vibrio anguillarum bacterins. J Fish Dis 5(3):207–213.

67. Kajita Y., Sakai M., Atsuta S., Kobayashi M., 1990 The immunomodulatory effects of levamisole on rainbow trout, Oncorhynchus mykiss. Fish Pathol 25:93–98.

68. Kanani H. G., Nobahar Z., Kakoolaki S., Jafarian H., 2014 Effect of ginger- and garlic-supplemented diet on growth performance, some hematological parameters and immune responses in juvenile Huso huso. Fish Physiol Biochem

40(2):481-490. 69. Kang W-K, Lee B-U, Chun H-J, Hwang S-D, Kim B-C, Kim H-S, 2005 Method

of enhancing growth and immunity of shrimp larvae using recombinant bovine growth hormone. International Publication Number WO 2005/115166 A1. World Intellectual Property Organization, 16pp.

70. Kawakami H., Shinohara N., Sakai M., 1998 The non-specific immunostimulation and adjuvant effects of Vibrio anguillarum bacterin, M-glucan, chitin and Freund’s complete adjuvant against Pasteurella piscicida

infection in yellowtail. Fish Pathol 33:287-292. 71. Kirkpatrick C. H., Green I., Rich R. R., Schade A. L., 1971 Inhibition of growth

of Candida albicans by iron-unsaturated lactoferrin:relation to host-defense mechanisms in chronic mucocutaneous candidiasis. J Infect Dis 124:539–544.

72. Kiron V., Gunji A., Okamoto N., Satoh S., Ikeda Y., Watanabe T., 1993 Dietary nutrient dependent variation on natural-killer activity of the leucocytes of rainbow trout. Fish Pathol 28:71–76.

73. Krieg A. M., Yi A. K., Matson S., Waldschmidt T. J., Bishop G. A., Teasdale R.,

Koretzky G. A., Klinman D. M., 1995 CpG motifs in bacterial DNA trigger direct B-cell activation . Nature 374(6522):546–549.

74. Kurtz J., Franz K., 2003 Innate defence: evidence for memory in invertebrate immunity. Nature 425:37–38.

75. Lee M. H., Shiau S. Y., 2002 Dietary copper requirement of juvenile grass shrimp, Penaeus monodon, and effects on non-specific immune responses. Fish Shellfish Immunol 13:259–270.

76. Lee M. H., Shiau S. Y., 2002 Dietary vitamin C and its derivatives affect

immune responses in grass shrimp, Penaeus monodon. Fish Shellfish Immunol 12(2):119-129.

77. Lee M. H., Shiau S. Y., 2003 Increase of dietary vitamin C improves haemocyte respiratory burst response and growth of juvenile grass shrimp, Penaeus monodon, fed with high dietary copper. Fish Shellfish Immunol 14(4):305-315.


78. Lee M. H., Shiau S. Y., 2004 Vitamin E requirements of juvenile grass shrimp, Penaeus monodon, and effects on non-specific immune responses. Fish Shellfish Immunol 16(4):475-485.

79. Li P., Gatlin D. M. III, 2006 Nucleotide nutrition in fish: Current knowledge and future applications. Aquaculture 251:141–152.

80. Li P., Burr G. S., Gatlin D. M. III, Hume M. E., Patnaik S., Castille F. L., Lawrence A. L., 2007 Dietary supplementation of short-chain

fructooligosaccharides influences gastrointestinal microbiota composition and immunity characteristics of Pacific white shrimp, Litopenaeus vannamei, cultured in a recirculating system. J Nutr 137(12):2763-2768.

81. Lin Y-C., Chen J-C., Morni W. Z. W., Putra D. F., Huang C-L., Li C-C., Hsieh J-F., 2013 Vaccination enhances early immune responses in white shrimp Litopenaeus vannamei after secondary exposure to Vibrio alginolyticus. PLoS ONE 8(7): e69722. doi:10.1371/journal.pone.0069722

82. Liu C. H., Yeh S. P., Kuo C. M., Cheng W., Chou C. H., 2006 The effect of sodium alginate on the immune response of tiger shrimp via dietary

administration: activity and gene transcription. Fish Shellfish Immunol 21(4):442-452.

83. Lin S., Lin X., Yang Y., Li F., Luo L., 2013 Comparison of chelated zinc and zinc sulfate as zinc sources for growth and immune response of shrimp (Litopenaeus vannamei). Aquaculture 406–407:79–84.

84. Lin Y-C., Yeh S-T., Li C-C., Chen L-L, Cheng A-C., Chen J-C., 2011 An immersion of Gracilaria tenuistipitata extract improves the immunity and survival of white shrimp Litopenaeus vannamei challenged with white spot

syndrome virus. Fish Shellfish Immunol 31(6):1239-1246. 85. Little T. J., Kraaijeveld A. R., 2004 Ecological and evolutionary implications of

immunological priming in invertebrates. Trends Ecol Evol 19 (2): 58–60. 86. Matzinger P., 1998 An innate sense of danger. Sem Immunol 10(5):399–415. 87. Medzhitov R., Janeway C. A., 2002 Decoding the Patterns of Self and Nonself

by the Innate Immune System. Science 296(5566):298-300. 88. Meena D. K., Das P., Kumar S., Mandal S. C., Prusty A. K., Singh S. K., Akhtar

M. S., Behera B. K., Kumar K., Pal A. K., Mukherjee S. C., 2013 Beta-glucan:

an ideal immunostimulant in aquaculture (a review). Fish Physiol Biochem 39(3):431-457. doi: 10.1007/s10695-012-9710-5.

89. Merchie G., Kontara E., Lavens P., Robles R., Kurmaly K., Sorgeloos P., 1998 Effect of vitamin C and astaxanthin on stress and disease resistance of postlarval tiger shrimp, Penaeus monodon (Fabricius). Aquacult Res 29:579–585.

90. Mulero V., Esteban M. A., Munoz J., Meseguer J., 1998 Dietary intake of

levamisole enhances the immune response and disease resistance of the marine

teleost gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 8:49-62.

91. Nahavandi R., Nurul Amin S. M., Hafezamini P., Javanmard A., 2010

Evaluation of nutritional genomes approach for controlling of disease in shrimp

farming. J Anim Vet Advance 9(20):2613-2619. 92. Nash G., Nithimathachoke C., Tungamandi C., Arkarjamorn A., Prathanpipat P.,

Ruramthaveesub P., 1992 Vibriosis and its control in pond reared Penaeus

http://scialert.net/asci/author.php?author=Reza&last=Nahavandi

http://scialert.net/asci/author.php?author=S.M.%20Nurul&last=Amin

http://scialert.net/asci/author.php?author=Parivash&last=Hafezamini

http://scialert.net/asci/author.php?author=Arash&last=Javanmard


monodon in Thailand. In: Shariff M., Subasinghe R. P., Arthur J. R. (Eds.) Disease in Asian Aquaculture I, Asian Fisheries Society, Manila, Philippines. p. 143 - 155.

93. Neumann N. F., Fagan D., Belosevic M., 1995 Macrophage activating factors secreted by mitogen stimulated goldfish kidney leucocytes synergies with bacterial lipopolysaccharide to induce nitric oxideproduction in teleost macrophages. Dev Comp Immunol 19:475-482.

94. Newman S. G., 2000 Proactive Disease management in shrimps. Infofish International 2:74-75.

95. Nonwachai T., Purivirojkul W., Limsuwan C., Chuchird N., Velasco M., Dhar

A. K., 2010 Growth, nonspecific immune characteristics,and survival upon challenge with Vibrio harveyi in Pacific white shrimp (Litopenaeus vannamei) raised on diets containing algal meal. Fish Shellfish Immunol 29:298-304.

96. Norqvist A., Hagstrom A., Wolf-Watz H., 1989 Protection of rainbow trout against vibriosis and furunculosis by the use of attenuated strains of Vibrio anguillarum. Appl Environ Microbiol 55:1400–1405.

97. Noworthy A., 1983. Beneficial effects of endotoxins. New York, Plenum Press. 98. Nya E. J., Austin B., 2009 Use of dietary ginger, Zingiber officinale Roscoe as

an immunostimulant to control Aeromonas hydrophila infections in rainbow

trout, Oncorhynchus mykiss (walbaum). J Fish Dis 32:971-977. 99. Nya E. J., Austin B., 2010 Use of bacterial lipopolysaccharide (LPS) as an

immunostimulant for the control of Aeromonas hydrophilla infections in rainbow trout, Oncorhynchus mykiss (Walbaum). J Appl Microbiol 108:686-694.

100. Nya E. J., Austin B., 2011 Development of immunity in rainbow trout

(Oncorhynchus mykiss, Walbaum) to Aeromonas hydrophila after the dietary

application of garlic. Fish Shellfish Immunol 30:845-850.

101. Ortuno J., Esteban M. A., Meseguer J., 1999 Effect of high dietary intake of vitamin C on non-specific immune response of gilthead sea bream, Sparus aurata L., Fish Shellfish Immunol 9:429-443.

102. Ortuno J., Esteban M. A., Meseguer J., 2000 High dietary intake of α-tocopherol

acetate enhances the non-specific immune response of gilthead seabream

(Sparus aurata L.). Fish Shellfish Immunol 10:293-307.

103. Pacheco R., Ascencio F., Zarain M., Gómez G., Campa A., 2011 Enhancement

of superoxide dismutase and catalase activity in juvenile brown shrimp,

Farfantepenaeus californiensis (Holmes, 1900), fed β-1.3 glucan vitamin E, and

β-carotene and infected with white spot syndrome virus. Lat Am J Aquat Res

39(3): 534-543.

104. Pais R., Khushiramani R., Karunasagar I., Karunasagar I., 2008 Effect of

immunostimulants on the haemolymph haemagglutinins of tiger shrimp Penaeus

monodon. Aquacult Res 39(12):1339-1345.

105. Panigrahi A., Kiron V., Kobayashi T., Puangkaew J., Satoh S., Sugita H., 2004

Immune responses in rainbow trout Oncorhynchus mykiss induced by a potential

probiotic bacteria Lactobacillus rhamnosus JCM 1136. Vet Immunol

Immunopathol 102:379–388.


106. Panigrahi A., Kiron V., Puangkaew J., Kobayashi T., Satoh S., Sugita H., 2005 The viability of probiotic bacteria as a factor influencing the immune response in rainbow trout Oncorhynchus mykiss. Aquaculture 243:241–254.

107. Panigrahi A., Kiron V., Satoh S., Hirono I., Kobayashi T., Sugita H., 2007 Immune modulation and expression of cytokines genes in rainbow trout Oncorhynchus mykiss upon probiotic feeding. Dev Comp Immunol 31: 372–382.

108. Paripatananont T., Lovell R. T., 1995a Chelated zinc reduces the dietary zinc

requirement of channel catfish, Ictalurus punctatus. Aquaculture 133:73–82. 109. Paripatananont T., Lovell R. T., 1995b Responses of channel catfish fed organic

and inorganic sources of zinc to Edwardsiella ictaluri challenge. J Aquat Anim Health 7:147–154.

110. Pereira J., Shanmugam S. A., Mazher Sulthana, Sundaraj V., 2009 Effect of vaccination on vibriosis resistance of Fenneropenaeus indicus. Tamilnadu J Vet Anim Sci 5(6):246-250.

111. Perez-Sanchez T., Ruiz-Zarzuela, I., de Blas, I., Balcazar, J. L., 2013 Probiotics in aquaculture: a current assessment. Rev Aquacult 5:1–14.

112. Peterson B. C., Small B. C., Bilodeau L., 2007 Effects of GH on immune and endocrine responses of channel catfish challenged with Edwardsiella ictaluri. Comp Biochem Physiol Part A 146:47–53.

113. Pholdaeng K., Pongsamart S., 2010 Studies on the immunomodulatory effect of polysaccharide gel extracted from Durio zibethinus in Penaeus monodon shrimp against Vibrio harveyi and WSSV. Fish Shellfish Immunol 28(4):555-561.

114. Powell A., Pope E.A., Eddy F. E., Roberts E. C., Shields R. J., Francis M. J., Smith P., Topps S., Reid J., Rowley A.F., 2011 Enhanced immune defences in

Pacific white shrimp (Litopenaeus vannamei) post-exposure to a vibrio vaccine. J Invert Pathol 107(2):95–99.

115. Raa J., Rostad G., Engstad R., Robertsen B., 1992 The use of immunostimulants to increase resistance of aquatic organisms to microbial infections. In: Shariff I. M., Subasinghe R. P., Arthus J. R. (eds). Diseases in Asian Aquaculture. Fish Health Section, Asian Fisheries Society 1992, pp. 39-50, Manila, Philippines.

116. Raa J., 1996 The use of immunostimulatory substances in fish and shellfish farming. Rev Fish Sci 4(3):229-288.

117. Rajasulochana P., Dhamotharan R., Krishnamoorthy P., Murugesan S., 2009 Antibacterial activity of the extracts of marine red and brown algae. J Am Sci 5:20-25.

118. Ramadan A., Afifi N. A., Moustafa M. M., Samy A. M., 1994 The effect of ascogen on the immune response of Tilapia fish to Aeromonas hydrophila vaccine. Fish Shellfish Immunol 4(3):159–165.

119. Rengpipat S., Rukpratanporn S., Piyatiratitivorakul S., Menasaveta P., 2000 Immunity enhancement in black tiger shrimp (Penaeus monodon) by a probiotic bacterium (Bacillus S11). Aquaculture 191:271–288.

120. Renn D., 1997 Biotechnology and the red seaweed polysaccharide industry: status, needs and prospects. Trends Biotechnol 15:9-14.

121. Rietschel E. T., Kirikae T., Schade F. U., Ulmer A. J., Holst O., Brade H., Schmidt G., Mamat U., Grimmecke H. D., Kusumoto S., Zahringer U., 1993 The


chemical structure of bacterial endotoxin in relation to bioactivity. Immunobiol 187:169-180.

122. Robertsen B., Rorstad G., Engstad R., Raa J., 1990 Enhancement of non-specific resistance in Atlantic salmon, Salmo salar L., by a glucan from Saccharomyces cerevisiae cell walls. J Fish Dis 13:391-400.

123. Rodríguez I., Chamorro R., Novoa B., Figueras A., 2009 Beta-Glucan administration enhances disease resistance and some innate immune responses in

zebrafish (Danio rerio). Fish Shellfish Immunol 27(2):369-373. doi: 10.1016/j.fsi.2009.02.007.

124. Rodríguez J., Espinosa Y., Echeverría F., Cárdenas G., Román R., Stern S., 2007 Exposure to probiotics and β-1,3/1,6-glucans in larviculture modifies the immune response of Penaeus vannamei juveniles and both the survival to White Spot Syndrome Virus challenge and pond culture. Aquaculture 273(4):405-417.

125. Rowley A. F., Powell A., 2007 Invertebrate immune systems–specific, quasi-specific, or nonspecific? J Immunol 179(11):7209-7214.

126. Rudtanatip T., Asuvapongpatana S., Withyachumnarnkul B., Wongprasert K.,

2014 Sulfated galactans isolated from the red seaweed Gracilaria fisheri targeted the envelope proteins of white spot syndrome virus and protected against viral infection in shrimp haemocytes. J Gen Virol doi: 10.1099/vir.0.062919-0.

127. Rungrassamee W., Maibunkaew S., Karoonuthaisiri N., Jiravanichpaisal P., 2013 Application of bacterial lipopolysaccharide to improve survival of the black tiger shrimp after Vibrio harveyi exposure. Dev Comp Immunol 41(2):257-262.

128. Sahoo P. K., Mukherjee S. C., 2002 The effect of dietary immunomodulation upon Edwardsiella tarda vaccination in healthy and immunocompromised Indian major carp (Labeo rohita). Fish Shellfish Immunol 12(1):1-16.

129. Sajeevan T. P., Philip R., Bright Singh I. S., 2009 Dose/frequency: A critical factor in the administration of glucan as immunostimulant to Indian white shrimp Fenneropenaeus indicus. Aquaculture 287:248–252.

130. Sakai M., 1999 Current research status of fish immunostimulants. Aquaculture 172:63-92.

131. Sakai M., Atsuta S., Kobayashi M., 1995 Efficacies of combined vaccine for Vibrio anguillarum and Streptococcus sp. Fisheries Sci 61:359–360.

132. Sakai M., Kamiya H., Ishii S., Atsuta S., Kobayashi M., 1992 The

immunostimulating effects of chitin in rainbow trout, Oncorhynchus mykiss. In:

Shariff M., Subasinghe R. P., Arthur J. R., (eds). Diseases in Asian aquaculture

I. Manila, Philippines: Fish Health Section, Asian Fish Soc 1992. p. 413-417.

133. Sakai M., Taniguchi K., Mamoto K., Ogawa H., Tabata M., 2001 Immunostimulant effects of nucleotide isolated from yeast RNA on carp Cyprinus carpio L. J Fish Dis 24:433-438.

134. Salati F., Hamaguchi M., Kusuda R., 1987 Immune response of red sea bream to

Edwardsiella tarda antigens. Fish Pathol 22:93-98.

135. Secombes C. J., 1994 Enhancement of fish phagocytic activity. Fish Shellfish

Immunology. 4: 421-436.


136. Selvaraj V., Sampath K., Sekar V., 2005 Administration of yeast glucan enhances survival and some non-specific and specific immune parameters in carp (Cyprinus carpio) infected with Aeromonas hydrophila. Fish Shellfish Immunol 19(4):293-306.

137. Sirirustananun N., Chen J-C., Lin Y-C., Yeh S-T., Liou C-H., Chen L-L., Sim S. S., Chiew S.L., 2011 Dietary administration of a Gracilaria tenuistipitata extract enhances the immune response and resistance against Vibrio alginolyticus and

white spot syndrome virus in the white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 31(6):848-855.

138. Sivakumar K., Felix, 1. S., 2011 Immunostimulants in the immune response of Penaeus monodon (Fabricius). J Mar Biol Ass India 53(1):58–67.

139. Siwicki A. K., 1987 Immunomodulating activity of levamisole in spawners carp (Cyprinus Carpi o L.). J Fish Biol 31:245–246.

140. Siwicki A. K., 1989 Immunostimulating influence of levamisole on nonspecific immunity in carp (Cyprinus carpio). Dev Comp Immunol 13:87–91.

141. Siwicki A. K., Anderson D. P., Dixon O. W., 1990 In vitro immunostimulation

of rainbow trout (Oncorhynchus mykiss) spleen cells with levamisole. Dev Comp Immunol 14: 231–237.

142. Siwicki A. K., Anderson D. P., Rumsey G. L., 1994 Dietary intake of

immunostimulants by rainbow trout affects non-specific immunity and

protection against furunculosis. Vet Immunol Immunopathol 41:125-139. 143. Skov J., Kania P. W., Holten-Andersen L., Fouz B., Buchmann K., 2012

Immunomodulatory effects of dietary β-1,3-glucan from Euglena gracilis in

rainbow trout (Oncorhynchus mykiss) immersion vaccinated against Yersinia ruckeri. Fish Shellfish Immunol 33(1):111-120. doi: 10.1016/j.fsi.2012.04.009.

144. Smith V., 2008 Immunostimulants for shrimp require further testing. Global Aquaculture Advocate Jan-Feb: 72 & 74.

145. Soderhall K., Cerenius L., 1992 Crustacean immunity. Annu Rev Fish Dis 2:3-23. 146. Sordello L. M., Shafer W. K., De Rosa D., 1997 Immunobiology of the

mammary gland. J Dairy Sci 80:1851-1865.

147. Song, S. K., Beck, B. R., Kim, D., Park, J., Kim, J., Kim, H. D., Ringø, E., 2014

Prebiotics as immunostimulants in aquaculture: A review. Fish Shellfish

Immunol 40:40-48.

148. Song Y-L., Hsieh Y-T., 1994 Immunostimulation of tiger shrimp Penaeus monodon hemocytes for generation of microbicidal substances: analysis of reactive oxygen species. Dev Comp Immunol 18:201–209.

149. Song Z-f., Wu T-x., Cai L-s., Zhang L-j., Zheng X-d., 2006 Effects of dietary supplementation with Clostridium butyricum on the growth performance and

humoral immune response in Miichthys miiuy. J Zhejiang Univ SCI B 7(7): 596-602.

150. Sung H. H., Kou G. H., Song Y. L., 1994 Vibriosis resistance induced by glucan treatment in tiger shrimp (Penaeus monodon). Fish Pathol 29:11-17.

151. Tachibana K., Yagi M., Hara K., Mishima T., Tsuchimoto M., 1997 Effects of

feeding -carotene supplemented rotifers on survival and lymphocyte

proliferation reaction of fish larvae of Japanese parrotfish (Oplegnathus


fasciatus) and spotted parrotfish (Oplegnathus punctatus): preliminary trials.

Hydrobiol 358:313-316.

152. Talpur A. D., Ikhwanuddin Mhd., Bolong A-M. A., 2013 Nutritional effects of

ginger (Zingiber officinale Roscoe) on immune response of Asian sea bass,

Lates calcarifer (Bloch) and disease resistance against Vibrio harveyi.

Aquaculture 400–401:46–52.

153. Tanekhy M., Fall J., 2015 Expression of innate immunity genes in kuruma shrimp Marsupenaeus japonicus after in vivo stimulation with garlic extract (allicin). Vet Med 60:39-47

154. Teunissen O. S. P., Faber R., Booms G. H. R., Latscha T., Boon J. H., 1998 Influence of vaccination on vibriosis resistance of the giant black tiger shrimp Penaeus monodon (Fabricius). Aquaculture 164:359-366.

155. Tewary A., Patra B. C., 2008 Use of vitamin C as an immunostimulant. Effect

on growth, nutritional quality, and immune response of Labeo rohita (Ham.). Fish Physiol Biochem 34(3):251-259.

156. Yeh S-T., Chen J-C., 2008 Immunomodulation by carrageenans in the white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Aquaculture 276:22–28.

157. Vargas-Albores F., Hernandez-Lopez J., Gollas-Galvan T., Montano-Perez K., Jimenez-Vega F., Yepiz-Plascencia G., 1998 Activation of shrimp cellular defence functions by microbial products. In Flegel, T.W. (ed.). Advances in Shrimp Biotechnology, National Centre for Genetic Engineering and

Biotechnology, Bangkok. p. 161-166. 158. Verlhac V., Obach A., Gabaudan J., Schuep W., Hole R., 1998

Immunomodulation by dietary vitamin C and glucan in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 8:409-424.

159. Vetvicka V., Vannucci L., Sima P., 2013 The Effects of β – glucan on fish immunity. N Am J Med Sci 5(10):580–588. doi: 10.4103/1947-2714.120792.

160. Waagbo R., Glette J., Raa-Nilsen E., Sandnes K., 1992 Dietary vitamin B6 and vitamin C. Influence on immune response and disease resistance in Atlantic salmon (Salmo Salar). Ann N Y Acad Sci 669:379-382.

161. Wang S-H., Chen J-C., 2005 The protective effect of chitin and chitosan gainst

Vibrio alginolyticus in white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 19: 191-204.

162. Wang Y. C., Chang P S., Chen H. Y., 2008 Differential time-series expression of

immune-related genes of Pacific white shrimp Litopenaeus vannamei in response

to dietary inclusion of ß-1,3-glucan. Fish Shellfish Immunol 24:113-121.

163. Wang C., Lovell R. T., Klesius P. H., 1997 Response to Edwardsiella ictaluri

challenge by channel catfish fed organic and inorganic sources of selenium. J

Aquat Anim Health 9:172–179.

164. Wang X. W., Wang J. X., 2013 Pattern recognition receptors acting in innate

immunity of shrimp against pathogen infections. Fish Shellfish Immunol

34:981-989. 165. Weiner G. J., Liu H. M., Wooldridge J. E., Dahle C. E., Krieg A. M., 1997

"Immunostimulatory oligodeoxynucleotides containing the CpG motif are


effective as immune adjuvants in tumor antigen immunization". Proceedings of the National Academy of Sciences of the United States of America 94(20):10833–10837.

166. Wongprasert K., Rudtanatip T., Praiboon J., 2013 Immunostimulatory activity of sulfated galactans isolated from the red seaweed Gracilaria fisheri and development of resistance against white spot syndrome virus (WSSV) in shrimp. Fish Shellfish Immunol DOI:10.1016/j.fsi.2013.10.010.

167. Yada T., 2007 Growth hormone and fish immune system. Gen Comp Endocrinol 152: 353–358.

168. Yada T., Misumi I., Muto K., Azuma T., Schreck C. B., 2004 Effects of

prolactin and growth hormone on proliferation and survival of cultured trout leucocytes. Gen Comp Endocrinol 136:298–306.

169. Yada T., Uchida K., Kajimura S., Azuma T., Hirano T., Grau E. G., 2002 Immunomodulatory effects of prolactin and growth hormone in the tilapia, Oreochromis mossambicus. J Endocrinol 173(3):483-492.

170. Zhang J., Liu Y., Tian L., Yang H., Liang G., Xu D., 2012 Effects of dietary mannan oligosaccharide on growth performance, gut morphology and stress tolerance of juvenile Pacific white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 33(4):1027-1032.

3. Use of immunostimulants in shrimp culture: An update

Documents

Transcript of 3. Use of immunostimulants in shrimp culture: An update