Evaluation of the impact of probiotics usage in aquaculture: A systematic review

doi:10.21203/rs.3.rs-1737405/v1

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Evaluation of the impact of probiotics usage in aquaculture: A systematic review

https://doi.org/10.21203/rs.3.rs-1737405/v1

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In aquaculture, probiotics are widely used for preventing the diseases. Probiotics are live beneficial bacteria that are ingested into the gastrointestinal tract through food or water or any dietary supplement to boost immunity and internal microbial resistance. Several experimental studies have been undertaken on the effect of probiotics on the immune system of diverse aquatic animals, as well as the mechanism involved to control the harmful pathogens. As a result, the current study aims to conduct a systematic review to update the findings related to specific immunological markers. Relevant studies from PubMed, EMBASE, and Google Scholar were systematically searched until the latest issue. Experimental studies written in the English language were included in the review. The main outcome was to identify the insightful outcome about the impact of probiotics. Systemic review was performed for 12 studies. The SYRCL’S risk of bias tool for the animal study was also used to evaluate the quality of the included studies. In conclusion, the results of the current review study summarize that probiotic could boost the immune system of aquatic animals by increasing plasma immunoglobulin, cytokines, plasma lysozyme, respiratory burst, peroxidase, phagocytosis, and alternative complement activities.

Aquaculture

Probiotic

Resistance

Systemic review

Aquaculture, one of the fastest-growing food-producing sectors, accounts for 90% to global production [1]. However, when aquatic animals are exposed to stressful conditions, diseases develop, the environment deteriorates, and substantial economic losses [1]. Broad-spectrum antibiotic and chemicals destroys both harmful and beneficial bacteria in the pond, causing the issues for aquatic organisms [1, 2]. Furthermore, the utility of antimicrobial agents results in the evolution of antimicrobial resistance among pathogenic bacteria [3]. Therefore, an alternative approach has been emerged i.e., probiotics to control only the potential pathogens in the water [4].

Probiotics are live beneficial bacteria that are given into the gastrointestinal tract via food or water or any dietary supplement that boost immunity and internal microbial resistance [1, 5]. Probiotics increase the number of beneficial bacteria, which compete with harmful microorganisms and limit their growth [3]. Furthermore, probiotics play an essential role in the degradation of organic matter, which helps to decrease the production of sludge and slime [1]. Therefore, water quality would improve by reducing the disease incidence, increasing zooplankton numbers, decreasing odors, and ultimately improving aquacultural productivity [6]. Additionally, probiotics are utilized in aquaculture to stimulate growth, nutrient absorption, and stress reduction in aquatic organisms to boost the overall production [7].

Experimental studies confirmed that commercial probiotic products prepared from bacterial species such as Bacillus sp., Lactobacillus sp., Clostridium spp., Enterococcus sp., and Staphylococcus sp., stimulated innate immunity and growth in aquatic animals [1, 5]. Hence, we performed a systemic review to update the knowledge regarding bacterial probiotic sources, probiotic use in fish diets against pathogenic bacteria, probiotic mode of action, and beneficial aspects of probiotics in fish. Furthermore, this review study provides valuable information for for future research for scientists, researchers, pharmacists, nutritionists, pharmaceutical industries, agricultural engineers, and veterinarians.

Search strategy and study selection

A systematic literature search using PubMed, EMBASE, and Google Scholar yielded relevant studies. The articles were screened from the databases using MeSH terms with boolean operators such as (“fish” OR “fish*” OR “aquaculture” OR “fish culture” OR “Fish farming”) AND (“probiotics” OR “bacteria”). Only the experimental studies written in the English language were included in the review. Other studies such as case reports, laboratory studies, and uncontrolled trials were excluded. The publication time of the retrieved articles is from the available date of inception until the latest issue. Reference lists from relevant articles selected were hand-searched to screen potentially eligible studies (Figure 1).

Type of studies and outcome

Only experimental studies were included in the review. The following comparisons were considered: placebo and any other control except probiotics. The main outcome of the study was any insightful outcome about the effects of probiotics.

Data extraction and collection

A total of 481 articles were found in the literature search, with 45 duplicates were removed. The remaining 436 records were subjected to a title/abstract level screening, with 380 articles being excluded. A total of 56 full-text articles were then reviewed for eligibility based on the inclusion criteria. However, 44 articles were excluded as they were not relevant to the study. Hence, a total of 12 studies were included for systemic review and discussion. Using a pre-designed data collection form, two reviewers independently extracted relevant data from the included studies, and any discrepancies encountered were resolved through discussion between the reviewers. The main contents of the data collection form include basic information of studies (study ID, title, authors, aim, methods); reporting quality; intervention (specific information of fishes, probiotic); control, results (changes after the probiotic supplementation).

Assessment of risk of bias and relevance in included studies

Risk of bias and studies included were assessed by reviewers independently. SYRCLE's risk of bias tool was used to assess the quality of animal studies [8].

Assessment of study risk of bias

Table 1 shows the results of SYRCLE's risk of bias tool. Overall, there is a high level of certainty in the quality of studies as critical details about the study designs were included in studies [9]. In terms of selection bias, none of the studies (n = 12) provided a complete description of sequence generation process. In terms of animals' characteristics, all the studies found that the animals were similar to one another. Information about the allocation concealment was not clearly reported in few studies (n = 3). All the studies reported random housing and random outcome assessment. However, none of the studies described the blinding. None of the studies reported blinding of personnel. Incomplete outcome data were addressed in all the studies. Selective reporting and other important sources of bias were absent in all the studies included (Table 1).

Table 1: Cochrane Collaboration's tool for assessing the risk of bias

Studies	Random sequence generation	Baseline characteristics	Allocation concealment	Random housing	Blinding	Random outcome assessment	Blinding	Incomplete outcome	Selective outcome reporting	Other source bias
Studies	Was the allocation sequence adequately generated and applied?	Were the groups similar at baseline or were they adjusted for confounders in the analysis?	Was the allocation adequately concealed?	Were the animals randomly housed during the experiment?	Were the caregivers and/or investigators blinded from knowledge which intervention each animal received during the experiment?	Were animals selected at random for outcome assessment?	Was the outcome assessor blinded?	Were incomplete outcome data adequately addressed?	Are reports of the study free of selective outcome reporting?	Was the study apparently free of other problems that could result in high risk of bias?
Standen BT 2013[10]	No	Yes	Yes	Yes	Unclear	Yes	Unclear	Yes	Yes	Yes
Fuchs VI_2017[11]	No	Yes	Yes	Yes	No	Yes	Yes	Yes	Yes	Yes
Salinas I_2018[12]	No	Yes	Yes	Yes	No	Yes	Unclear	Yes	Yes	Yes
Gupta A_2014[13]	No	Yes	Yes	Yes	No	Yes	Yes	Yes	Yes	Yes
Pirarat N_2011[14]	No	Yes	Unclear	Yes	Unclear	Yes	Yes	Yes	Yes	Yes
Balcázar JL_2007[15]	No	Yes	Yes	Yes	Unclear	Yes	Yes	Yes	Yes	Yes
Ljubobratovic U_2017[16]	No	Yes	Yes	Yes	No	Yes	Unclear	Yes	Yes	Yes
Nayak SK_2007[17]	No	Yes	Yes	Yes	No	Yes	Unclear	Yes	Yes	Yes
Selim KM_2015[18]	No	Yes	Unclear	Yes	Unclear	Yes	Yes	Yes	Yes	Yes
Cerezuela R_2013[19]	No	Yes	Yes	Yes	No	Yes	Unclear	Yes	Yes	Yes
Liu W_2013[20]	No	Yes	Yes	Yes	No	Yes	Yes	Yes	Yes	Yes
Xing CF_2013[21]	No	Yes	Unclear	Yes	Unclear	Yes	Yes	Yes	Yes	Yes

Table 2 summarises the included studies. The studies were categorised with respect to fish type/breed, intervention and control arms, and main outcome.

Table 2. : The studies were categorised according to fish type/breed, intervention and control arms, and main outcome.

Studies	Fish type or breed	Intervention arm (n)	Control arm (n)	Outcomes
Standen BT 2013 [10]	Genetically male red Nile tilapia O. niloticus (GMT, Fishgen UK)	P. acidilactic	o iso-nitrogenous and iso-lipidic diets without probiotics	Probiotic treatment potentiated the immune-responsiveness of the intestine as upregulation of the gene expression of the pro-inflammatory cytokine TNFa was observed in the probiotic fed fish (P<0.05). Intraepithelial leucocyte levels (IELs) also elevated in the intestine of P. acidilactici fed tilapia after six weeks (P<0.05) of feeding and a trend towards elevated goblet cells was also observed after six weeks (P=0.08). Concomitantly at week six, along with elevated IELs and elevated TNFa mRNA levels in the intestine, an increased abundance of circulating neutrophils and monocytes were observed in fish fed the probiotic supplemented diet (P<0.05).
Fuchs VI_2017 [11]	Turbots (Scophthalmus maximus)	Four diets: a) Saccharomyces cerevisiae, b) alginic acid product of brown algal extracts c) purified yeast nucleotides (cytidine-5V-monophosphate (CMP), disodium uridine-5V-monophosphate (UMP), adenosine-5V-monophosphate (AMP), disodium inosine-5V-monophosphate (IMP), disodium guanidine-5V-monophosphate (GMP)) and ribosomal RNA, c) probiotic product of bacteria strains B. subtilis and B. licheniformis	FM-based diet (C-HF; 585 g FM protein kg−1 feed) and a FM reduced diet (C-LF; 320 g FM kg−1 feed)	Plasma lysozyme activity, neutrophil reactive oxygen species production, and total plasma protein levels did not significantly differ between treatment groups; however, plasma cholesterol increased significantly in fish fed β-glucan/MOS (GM), alginic acid (AC), nucleotides/RNA (NR) and C-HF compared to C-LF (I). Plasma glucose and triglyceride levels significantly increased with GM and NR treatments, while glucose levels were significantly higher in C-HF compared to C-LF. Immunostimulant-supplemented diets exhibited significantly lower cortisol levels compared to controls C-LF (at 0.5 h) and C-HF (at 1 h) post stress, respectively (II). FM substitution did not modulate the innate immune response but was associated with reduced levels of cholesterol.
Salinas I_2008 [12]	Seawater teleost Sparus aurata L. (a protandrous hermaphrodite species) obtained from Culmarex S.A. (Murcia, Spain)	Heat-inactivated 1 X 10^7 CFU g ^-1 Lactobacillus; (III) diet supplemented with heat-inactivated 1 X 10^7 CFU g ^-1 Bacillus; (IV) diet supplemented with heat-inactivated 0.5 X 10^7 CFU g ^-1 Lactobacillus and 0.5 X 10^7 CFU g ^-1 Bacillus	Non-supplemented commercial pelleted diet	Feeding the mixture of the two killed bacteria species significantly increased natural complement, serum peroxidase and phagocytic activities compared with controls.
Gupta A_2014 [13]	Cyprinus carpio	Three bacterial strains viz. Bacillus coagulans (B1), B. licheniformis (B2) and Paenibacillus polymyxa (B3)	Without probiotic	Fish fry were fed these diets and growth performance, various non-specific immune parameters and disease resistance study were conducted at 80 days post-feeding. The antagonism study showed inhibition zone against Aeromonas hydrophila and Vibrio harveyi. The growth-promoting influences of probiotic supplemented dietary treatments were observed with fish fry and the optimum survival, growth and feed utilization were obtained with P. polymyxa (B3) supplemented diet. Study of different non-specific innate immunological parameters viz. lysozyme activity, respiratory burst assay and myeloperoxidase content showed significant (p < 0.05) higher values in fish fry fed B3 diet at 109 CFU/g. Dietary supplementation of B. coagulans, B. licheniformis and P. polymyxa significantly (p < 0.05) enhanced the resistance of fish fry against bacterial challenge
Pirarat N_2011 [14]	tilapia (Oreochromis niloticus)	L. rhamonsus GG (ATCC 53103), was cultured in MRS broth at 30⁰C for 48 h, centrifuged and washed with sterile PBS three times	wihtout probiotic	Supplementation of L. rhamnosus promoted the intestinal structure and the mucosal immunity of tilapia. Probiotic fish had a greater villous height in all parts of the intestines and, significantly, in the proximal and middle part. The population of intraepithelial lymphocytes was significantly higher in the probiotic group than in the control group in all parts of the intestines. The population of acidophilic granulocyte in the probiotic group was significantly higher at the proximal and distal parts when compared with the control group. The higher serum complement activity as well as the enhanced phagocytosis and killing ability of the head kidney leukocytes in the probiotic supplemented fish corresponded with the higher level of TNF alpha and IL-1 gene expression, suggested the induction of IL-1 and TNF alpha cytokines by L. rhamnosus indicating an important regulator of gut associated immune systems
Balcázar JL_2007 [15]	brown trout (Salmo trutta)	Three bacterial strains, Lc. lactis ssp. lactis CLFP 100, Leu. mesenteroides CLFP 196 and Lb. sakei CLFP 202, isolated from salmonids and genetically identified by 16S rRNA gene sequencing, were selected from a pool of 246 strains obtained from the intestinal content of healthy salmonids.	Unsupplemented food	Only Lb. lactis ssp. lactis and Leu. mesenteroides were detected at levels above 1 £ 102 colony-forming units/g at the end of the fourth week. In comparison to untreated control fish, the alternative complement activity in the serum was found to be significantly greater in all LAB groups at the alternative complement activity in the serum the end of the second week. Groups supplemented with Lc. lactis ssp. lactis and Leu. mesenteroides exhibited an elevated level of lysozyme activity at the end of the third week, but the group supplemented with Lb. sakei did not exhibit any significant change in lysozyme activity. Serum immunoglobulin levels were higher compared with the control group, but there was no significant difference between the LAB and control groups.
Ljubobratovic U_2017 [16]	Juvenile pike-perch (Sander lucioperca)	Two groups received the combination of OTOHIME and nauplii enriched either with Lactobacillus paracasei BGHN14+ Lactobacillus rhamnosus BGT10 or with Lactobacillus reuteri BGGO6–55 +Lactobacillus salivarius BGHO1, and one group received OTOHIME hydrolyzed by BGHN14 +BGT10 and non-enriched nauplii	Control group received non-enriched nauplii and non-hydrolyzed OTOHIME	There was positive effect of Artemia enriched with BGGO6–55 +BGHO1 on fish growth, skeletal development and trypsin to chymotrypsin activity ratio (T/C), as an indicator of protein digestibility. Hydrolysis of OTOHIME was also associated with better skeletal development, higher T/C values and lower levels of Aeromonas and Mycobacterium spp., which are important fish pathogens
Nayak SK_2007 [17]	Rohu (Labeo rohita Ham.)	B. subtilis isolated from the gastrointestine, a vitamin C treated feed contained ascorbyl polyphosphate (Hi- Media, India) at 100 mg/kg diet. A probiotic and vitamin C combined feed was prepared by mixing both B. subtili at 108 CFU/g and ascorbyl polyphosphate at 100 mg/kg diet	no additional supplement	The total serum protein and globulin content was significantly higher (p < 0.05) in probiotic (B. subtilis at 108 CFU/g of the feed) fed group while the respiratory burst activity of blood neutrophils was significantly high in vitamin C fed group. The antibody level was significantly high in Bacillus subtilis treated group followed by the probiotic (B. subtilis at 108 CFU/g of the feed) and ascorbyl polyphosphate combined group. The least percentage of mortality was recorded in B. subtilis treated group (25%) followed by 35 and 40% in ascorbyl polyphosphate treated and B. subtilis and ascorbyl polyphosphate combined groups, respectively
Selim KM_2015 [18]	Nile Tilapia, Oreochromis niloticus	Bacillus amyloliquefaciens was added to the basal diets at levels of 1×104 CFU/g (G2) and 1×10^6 CFU/g (G3)	-	After 15d of treatment, the serum killing percentages and phagocytic activities were significantly higher in G3 than in G1 and G2, whereas the same parameters had significantly higher values in G3 and G2 than in G1 after 30 d. After both 15d and 30d, the lysozyme activities and nitric oxide assay results (mmo/l) were significantly higher in G3 than G2, and the lowest values were observed in G1. The percentage of serum killing, serum nitric oxide and serum lysozyme activity were significantly increased by the time of Bacillus amyloliquefaciens administration independently of the probiotic dose, and the phagocytic activity percentage was significantly decreased at the end.
Cerezuela R_2013 [19]	Seawater teleost gilthead sea bream (S. aurata L.), obtained from CULMAREX S.A. (Murcia, Spain),	B. subtilis (CECT 35, Valencia, Spain) were grown in nutrient agar (pH 6.8; 30 degree C) plates for 2-3 days. Colonies recovered from plates were then inoculated in 750 ml nutrient broth in continuous gentle agitation for 15 h	Without probiotic	Intestinal morphometric study revealed no effect of inulin or B. subtilis on the intestinal absorptive area. Experimental diets cause important alterations in the intestinal microbiota by significantly decreasing bacterial diversity, as demonstrated by the specific richness, Shannon, and range-weighted richness indices. The observed alterations demonstrate that fish fed experimental diets had different signs of gut oedema and inflammation that could compromise their body homeostasis, which is mainly maintained by the epithelial lining of the gastrointestinal tract.
Liu W_2013 [20]	juvenile hybrid tilapia	The LALB and HALB strains were used. The pathogenic strain A. hydrophila NJ-1 was used in the challenge test.	Basal diet without probiotic	The adhesive gut bacterial communities were altered in the fish fed either the HALB or the LALB, but the response was more rapid and substantial with the adhesive strain. The two strains induced similar changes in the patterns (upregulation or downregulation) of intestinal, splenic or kidney cytokine expression, but they differed in the degree of response for these genes. Changes in intestinal HSP70 expression levels coincided with changes in the similarity coefficient of the adhesive gut bacterial communities between the probiotic treatments. The highest dose of the HALB appeared to protect against the toxic effects of immersion in A. hydrophila (P < 0.05)
Xing CF_2013 [21]	cobia (Rachycentron canadum)	Pdp strain P40, cultured in brain heart infusion (BHI) broth with 20⁰C & salinity at 28⁰C. The LAB 4012 was isolated from the intestine of a 3-day fasted adult cobia, and cultured in MRS broth (Fluka) at 37⁰C, and was proved to be able to resist the treatments of gastric acid (pH 2.0) and 0.3% bile salt	LAB unfed group	After a 2-week feeding of LAB 4012, the growth rate of the fed cobia was 12% higher than that of the non-fed group, and the relative percentage of survival of the fed cobia was found to be 74.4 in Pdp immersion challenge. Respiratory burst of peripheral blood leukocytes in the LAB 4012-fed group was significantly higher than that of the non-fed group. LAB 4012 did not improve specific antibody response in cobia after immunization with Pdp vaccine, it still significantly raised the survival rate by 22% over that of the non-fed group after Pdp immersion challenge

Probiotics modulate immune responses in aquatic animals by increasing lysozyme and complement activity, inducing proinflammatory cytokines, increasing mucosal and systemic antibody production, increasing respiratory burst activity, stimulating natural killer cell activity and activating phagocytic activity. The present review study covers the effects of various probiotics on innate immune responses in various fish strains.

Probiotic impact on serum lysozyme activity

Lysozyme, a bactericidal cationic enzyme is produced by leucocytes (mainly neutrophils and macrophages) and reacts against gram-positive and few gram-negative bacteria [18, 22]. When infected with microorganisms, it attacks the peptidoglycan layers in the cell walls of bacteria, lyzes them, and increases the sera of fish [22]. In Selim et al. study, Bacillus amyloliquefaciens activated serum lysozyme in tilapia when supplemented at 104 and 106 CFU/g [18]. In rainbow trout, olive flounder, and paralichthys olivaceus, Bacillus strains supplementation boosted lysozyme activity [23–26]. These results imply that probiotics enhances the innate immune system in aquatic amimals via serum lysozyme activity.

Probiotic impact on plasma lysozyme activity

Tretament of Nile tilapia with probiotic bacteria, B. subtilis, at a concentration of 5 × 10⁶ CFU g feed⁻¹ promoted the innate immune system by increasing the mean corpuscular hemoglobin and improving macrophages plasma lysozyme activity [26]. Supplementation of commercial bacillus probiotic significantly increased the plasma lysozyme activity in rainbow trout [27]. A few former studies have found that administration of probiotic diet for 8 weeks controlled multiple bacterial diseases via plasma lysozyme activity [28,29]. In a meta-analysis review study, probiotics had no effect on plasma lysozyme activity, and the effect slightly declined with an increase in duration of the experiment [22].

Probiotic impact on plasma immunoglobulin

Probiotics interact with immune cells such as monocytes, macrophages, neutrophils, and natural killers cells, and enhance their natural immune responses in different fish.[17] Immunoglobulins (Ig) are known to have a protective function against disease in humans and animals. Administration of three bacterial strains of Lc. lactis ssp. (lactis CLFP 100, Leu. mesenteroides CLFP 196 and Lb. sakei CLFP) at 106 CFU/g feed for two weeks elevated the serum immunoglobulin levels in brown trout (Salmo trutta), but not at a significant level [15]. Similarly, probiotics tretament boosted the plasma Ig levels in rainbow trout, however, the levels decreased as increase in duration of the experiments [22]. Other similar study conducted on rainbow trout found that probiotics increased the Ig levels in a transient manner and the levels declined after stopping the probiotics [30].

Probiotic impact on cytokine

Cytokines, including chemokines, interferons, interleukins, lymphokines, and tumor necrosis factor, are released by cells and influence the behavior of other cells and even sometimes produces other cells [31]. Lb. plantarum supplementation upregulated the expression of IL-1b, IL-10, and TNF in the head kidney [32]. In another study, feeding to Nile tilapia with Pediococcus acidilactici upregulated the expression of proinflammatory cytokine TNF-a [10]. In a study by Kim et al., after feeding with Lactococcus lactis upregulated the IL-1, and IFN- c expression in olive flounder (Paralichthys olivaceus) [33]. This indicates diverse microorganisms can be used as probiotics in aquaculture to stimulate or modulate immune responses.

Probiotic impact on peroxidase activity

The peroxidase enzyme, which produces hypochlorous acid using oxidizing radicals kills pathogens. The peroxidase is released from the azurophilic granules of neutrophils during the oxidative respiratory burst. Supplementation of probiotics such as B. subtilis, alone or in combination with N. delbrueckii spp. Lactis for three weeks stimulated the serum protease activity but did not increases the peroxidase activity of head kidney leukocytes from S. aurata [12]. Similarly, in a Wang et al.study., treatment of E. faecium at a concentration of 107 CFU/Ml for every 4-40 days significantly increased the serum peroxidase activity in O. niloticus [4].

Probiotic impact on serum alternative hemolytic complement pathway

The activity of alternative hemolytic complement pathway activity in fish is another most crucial component of the innate immune system. The bacterial strains of Lc. lactis ssp. at 106 CFU/g feed for 2 weeks increased the serum alternative complement activity in all the LAB groups when compared to control [15]. Meta-analysis also demonstrated that probiotics could increase the immunity of rainbow trout via stimulating serum alternative hemolytic complement pathway [22]. While other studies reported that the results may varies concerning the type of bacteria [34] and duration of experiment [35].

Probiotic impact on serum total protein

Blood protein levels have been found to be a good indicator of fish health. A meta-analysis review study also reported that probiotics increase the serum total protein in rainbow trout [22]. Several previous studies have found that probiotics have increasing effects on serum total protein in fish [17,36]. Other studies reported probiotic treatment had no effect on serum total protein [11,37]. However, high levels of serum total protein, on the other hand, seems to stimulate an innate immunological response in fish.

Probiotic impact on serum complement activity

The complement system is another essential serum compound that play a vital role in cellular defense mechanism of fish by directly killing microorganisms either through lysis, phagocytosis, chemical adsorption and activation of leukocytes, and other immune compounds or modulation of specific antibody responses by localization of antigens for B lymphocytes [38,39]. A recent meta-analysis study demonstrated that probiotic treatment in rainbow trout increased the activity of the complement system and the activity elevated in response to higher concentrations of probiotics [22]. In Pirarat et al., treatment to tilapia with L. rhamnosus improved the serum complement activity [14].

Probiotic impact on phagocyte activity

Phagocytes are white blood cells (neutrophils and macrophages), which engulf foreign bacteria and kill them via the production of reactive oxygen species such as hydrogen peroxide, superoxide anion, and hydroxyl radicals during respiratory burst [31]. In a Salinas et al., heat inactivated lactobacillus bacteria significantly increased the phagocytic activities in seawater teleost Sparus aurata L when compared with controls [12]. Similarly in a meta-analysis review study, probiotics increased the phagocytic activity in rainbow trout [22]. In a comparable study conducted by Pirarat et al., a two weeks supplementation of L. rhamnosus in tilapia (Oreochromis niloticus) significantly stimulated the phagocytosis activity [40].

Probiotic impact on respiratory burst

Respiratory burst activity is the other strong defense mechanism of fish against pathogens, where the probiotics improve the respiratory burst of phagocytic cells and protect the cells [31]. Xing et al. study, demonstrated that treatment with lactic acid bacteria (LAB 4012) for two weeks significantly improved the respiratory burst of peripheral blood lymphocytes and stimulated the protection of Cobia (Rachycentron canadum) from photobacteriosis challenge [21]. Rahimi et al. reported that probiotics had no affect the respiratory burst activity [22]. Furthermore, an increase in the duration of experiment and the growth of fish reduced the respiratory burst activity [22]. Therefore, further studies are needed to reach a definite conclusion on the effects of the probiotics on respiratory burst activity.

Despite the fact that systematic reviews are the gold standard and preferred technique for conducting experimental studies, they are not exclusive. Scoping reviews, which are commonly used to uncover knowledge gaps, are allowed. We recongnize that the number of studies included was inadequate when compared to a broad topic. Furthermore, the inclusion of only a few databases might have overlooked other publications that are not included in these databases. Furthermore, although we did not assign a time frame to the publications obtained in this study; the earliest article published was in the year 2007 in the included studies. Hence, older articles that did not use the searched term in the titles or abstracts may be overlooked. Another limitation encountered is the exclusion of journals published in languages other than English. Neverthless the low risk of bias identified in most studies is the main strength of this review.

In conclusion, the current review summarizes probiotics could improve the immune system of aquatic animals by increasing plasma immunoglobulin, cytokine activity, plasma lysozyme activity, respiratory burst activity, peroxidase activity, phagocytosis activity, and alternative complement activity. However, additional high-quality, large-scale trials might require to be performed to substantiate the view of the study.

Acknowledgments

All the authors have contributed equally to the development of the review article. Dr. David Elisha Henry would like to thank the vice-chancellor, M S Ramaiah University of Applied Sciences for the support and for providing the seed grant.

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No competing interests reported.

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Evaluation of the impact of probiotics usage in aquaculture: A systematic review

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