i An update to this article is included at the end

Fish and Shellfish Immunology 77 (2018) 194–199

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Fish and Shellfish Immunology

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Full length article

The effects singular or combined administration of fermentable fiber and T

probiotic on mucosal immune parameters, digestive enzyme activity, gut
microbiota and growth performance of Caspian white fish (Rutilus frisii
kutum) fingerlings
Ali Taheri Mirghaeda,∗, Peyman Yarahmadia, Seyed Hossein Hosseinifarb, Davood Tahmasebib,
Nahid Gheisvandib, Alireza Ghaedic
a
Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
b
Department of Fisheries, Faculty of Fisheries and Environmental Sciences, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran
c
Iranian Fisheries Research Organization, Iran

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

Keywords: The aim of the present study was to investigate the effects of single or combined administration of dietary
Fermentable fiber fermentable fiber (Vitacel®) and probiotic PrimaLac® on mucosal immune parameters, digestive enzyme activity,
Probiotic gut microbiota and growth performance of Caspian white fish (Rutilus frisii kutum) fingerlings. Fish were
Mucosal immunity transferred to laboratory, acclimatized for two weeks and then fish (0.56 ± 0.026 g) were allocated into 12
Gut microbiota
tanks (30 fish per tank). Triplicate groups were fed a basal diet (Control) or basal diet supplemented with
Digestive enzyme
Rutilus frisii kutum
fermentable fiber [Vitacel®] (FF), probiotic [PrimaLac®] (P) and combined fermentable fiber and probiotic
(FF + P). At the end of feeding trial, growth performance and feed utilization parameters were significantly
(P < 0.05) improved in FF, P and FF + P treatments compared control group. Evaluation of digestive enzyme
activity revealed significant (P < 0.05) increase of lipase activity in fish fed supplemented diet. However,
amylase, protease and alkaline phosphatase were significantly higher (P < 0.05) only in P and FF + P treat-
ments. Furthermore, total autochthonous intestinal microbiota and autochthonous LAB levels significantly in-
creased in fish fed supplemented diet (P < 0.05). Also, inclusion of FF, P and FF + P in Caspian white fish diet
remarkably increased skin mucus immune parameters compared control group (P < 0.05). These results indicate
that singular or combined administration of FF and P can be considered as a beneficial dietary supplement for
early stages of Caspian white fish (Rutilus fresii kutumn) culture.

1. Introduction in the intestinal tract, and thus improves host health” [8]. Previous
studies revealed prebiotics have positive effect on growth performance,
The Caspian white fish (Rutilus frisii kutum) is an important com- body composition, immune response, gut microbiota, haematological
mercial fish species in the Caspian Sea. Artificial culture as well as re- and serum biochemical parameters [9–16]. Similar results were also
leasing fingerlings for restocking purposes have been practiced by reported in case of dietary administration of fermentable fiber (Vi-
SHILAT organization [1]. Physio-immunological statues and stress tol- tacel®) [17,18]. However, the effects of this feed supplement as pre-
erance of fingerlings are among the key factors which determine the biotic on skin mucosal immune response and digestive has not been
success of restocking and artificial culture of fingerlings. Dietary ad- investigated. PrimaLac® is multi-strain commercial probiotic that
ministration of probiotics and prebiotics suggested as promising ap- mainly include Lactobacillus acidophilus, Lactobacillus casei, Enterococcus
proach for imporving physiological and health status in early stages of faecium, Bifidobacterium thermophilus. Previous studies have been de-
fish culture [2–7]. monstrated the beneficial effect of Lactobacillus acidophilus [19–21],
Prebiotics are fermentable ingredient defined as a “non-digestible Enterococcus faecium [22,23] and Bacillus subtilis [24,25] in aquaculture.
food ingredient that beneficially affects the host by selectively stimu- Considering limited information about effect of fermentable fiber
lating the growth and/or activity of one or a limited number of bacteria (Vitacel®) and PrimaLac® on mucosal immune response and digestive

∗
Corresponding author.
E-mail address: [email protected] (A.T. Mirghaed).

https://doi.org/10.1016/j.fsi.2018.02.007
Received 12 August 2016; Received in revised form 15 October 2017; Accepted 5 February 2018
Available online 07 February 2018
1050-4648/ © 2018 Published by Elsevier Ltd.
A.T. Mirghaed et al. Fish and Shellfish Immunology 77 (2018) 194–199

enzyme activity of fish, the present study was performed to investigate Table 1
the effect of singular or combined administration of Vitacel® and Dietary formulation and proximate composition of the basal diet (%).
PrimaLac® on mucosal immune response, digestive enzyme activity, gut ingredient
microbiota modulation and growth performance of Caspian white fish.
Fish meal 40.0
Wheat flour 21.0
2. Material and methods Soybean meal 13.5
Gluten 5.5
2.1. Fish culture and experimental design Soybean oil 6.0
Fish oil 6.0
Mineral premixa 3.0
The experiment was performed on Caspian white fish (Rutilus frisii
Vitamin premixa 2.0
kutum) under laboratory condition for 45 days. Three hundred and sixty Binderb 2.0
fish were provided from the Sijowal Caspian Sea Teleost Fish Anti fungic 0.5
Propagation & Cultivation Centre (Golestan province, Iran) and trans- Antioxidantd 0.5
ferred to Aquaculture Lab of Gorgan University of Agricultural Science
Proximate composition (% dry matter basis**)
and Natural Resources. Fish were acclimatized for two weeks and the
fish (0.56 ± 0.02 g) were randomly distributed into twelve plastic 45-L Dry matter 91.72
tanks assigned to four experimental groups includes: Control (C), fer- Crude protein** 36.88
mentable fiber (Vitacel®) suplementation (FF), probiotic (PrimaLac®) Crude lipid** 11.63
Ash** 3.50
suplementation (P) and combined administration of Vitacel® and
Fiber** 10.58
PrimaLac® (FF + P) repeated in triplicates. Water temperature, pH and NFEe 28.30
dissolved oxygen were maintained at 23.5–24.8 °C, 6.7–7.2 and Energy (MJ kg_1)f 17.87
6.9–7.7 mg l−1, respectively. The fish were hand-fed experimental diets
a
at a rate of 3% of body weight for 45 days. Vitamin contains the following (kg_1 dry weight): vitamin A:50.000
MIU; vitamin D3: 10 MIU; vitamin E: 130 g; vitamin K3: 10 g; vitamin
B1: 10 g; vitamin B2: 25 g; vitamin B6: 16 g; vitamin B12: 100 mg;
2.2. Preparation of experimental diet
niacin: 200 g; pantothenic acid: 56 g; folic acid: 8 g; biotin: 500 mg;
antioxidant: 0.2 g; anticake: 20 g. Mineral premix contains the following
Ingredient and proximate composition of basal diet are shown in
(kg_1 dry weight): calcium phosphate 397 g; calcium lactate 327 g;
Table 1. 1% Vitacel® (Commercial raw fiber concentrates; JRS Co;
ferrous sulphate 25 g; magnesium sulphate 137 g; potassium chloride
Germany) and 0.1% PrimaLac® (multi strain commercial probiotc, in-
50 g; sodium chloride 60 g; potassium iodide 150 mg; copper sulphate
clude Lactobacillus acidophilus, L. casei, Enterococcus faecium and Bifi-
780 mg; manganese oxide 800 mg; cobalt carbonate 100 mg; zinc oxide
dobacterium bifidium) was used to prepare experimental diets as de-
1.5 g; sodium selenite 20 mg.
scribed above. The ingredient were grounded, mixed and pelleted as b
Amet binder_, Mehr Taban-e- Yazd, Iran.
previously described for Caspian white fish by Hoseinifar et al. [26]. c
ToxiBan antifungal (Vet-A-Mix, Shenan-doah, IA).
Experimental diets were stored in plastic bags at 4 °C until further use. d
Butylated hydroxytoluene (BHT) (Merck, Germany).
e
Nitrogen-free extracts (NFE) = dry matter - (crude protein + crude
2.3. Growth performance parameters lipid + ash + fibre).
f
Gross energy (MJ kg-1) calculated according to 23.6 kJ g_1 for
The growth performance parameters of trout fed experimental diets protein, 39.5 kJ g_1 for lipid and 17.0 kJ g_1 for NFE.
were determined as follows:
2.5.2. Skin mucus alkaline phosphatase (ALP) activity
weight gain% = {(Final weight − initial weight) ÷ initial weight} × 100
The mucus ALP activity was determined based on a commercial kit
SGR = {(ln Final weight − lnInitial weight)/t} × 100 protocol (Pars Azmoun Co., Iran), using a spectrophotometer and the
absorbance was read at 405 nm.
FCR = Food intake ÷ Weight gain

PER = Protein intake ÷ Weight gain 2.5.3. Skin mucus protease activity
Skin mucus Protease activity was examined by azocasein hydrolysis
assays [28]. Briefly, 100 ml of skin mucus was incubated with 100 ml of
2.4. Skin mucus collection
100 mM ammonium bicarbonate (pH 7.8) buffer containing 0.7% azo-
casein. After incubation at 30 °C in shaking incubator for 19 h, tri-
The skin mucus were collected based on the method suggested by
chloroacetic acid (4.6% final concentration) was used and cooled on ice
Ross, Firth [27] with some modifications, as described by Hoseinifar,
to stop the reaction. Then, centrifuged at 13000 rpm for 5 min, and
Sharifian [1]. Briefly, ten fish were randomly selected from each tank
100 ml of supernatant was added to the micro plate well (Costar,
and anesthetized using 250 mg l−1 clove powder. Then, fish were
Corning Inc., USA) containing an equal volume of 0.5 M NaOH (Sigma).
transferred into polyethylene bags containing 10 ml of 50 mM NaCl.
The protease activity was measured as the increase in the OD values at
After 2 min, mucus was collected, transferred to 15-ml sterile tubes and
450 nm on a micro plate reader (Benchmark, BioRad, USA).
centrifuged at 1500 g for 10 min at 4 °C. The supernatant was stored at
−80 °C for further analysis.
2.5.4. Skin mucus lysozyme activity
2.5. Evaluation of skin mucus immune parameters Skin mucus lysozyme activity was measured based on turbidimetric
assay and lysis of the lysozyme-sensitive Gram-positive bacterium
2.5.1. Skin mucus protein level Micrococcus luteus (Sigma). Briefly, 25 μl of mucus were transferred to a
Skin mucus protein concentration were measured according to 96 well plate with 75 μl of lyophilized Micrococcus luteus cells (Sigma,
spectrophotometericaly method and using bovine serum albumin to 75 μg ml−1) in triplicate and then incubated or 10 min at 30 °C. A unit
obtained standard curve based on manufacture standard protocol (Pars of mucus lysozyme activity was defined as the amount of enzyme that
azmon Co, Iran). caused a decrease in absorbance (450 nm of 0.001 min−1) [29].

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A.T. Mirghaed et al. Fish and Shellfish Immunology 77 (2018) 194–199

2.6. Evaluation of digestive enzyme assay observed in case of other body composition parameters (i.e crude lipid
and ash) between treated and control group (P > 0.05).
Nine fish per each tank were anaesthetized with clove powder The effect of dietary FF, P and FF + P on the digestive enzyme
(250 mg l−1) and digestive tracts were sampled (3 samples were activities (amylase, ALP, Lipase, trypsin and chymotrypsin) is shown in
pooled) for estimating enzymatic activity. Samples were rapidly Table 2. Amylase activity was higher in groups fed dietary P and FF + P
homogenized in five volumes of 0.2 M NaCl solution (w/v) using an in comparison with other groups (P < 0.05). Also, trypsin activity
electric homogenizer (IKA T25 digital, Ultra Turrax model). were significantly higher in group fed dietary supplemented with
FF + P when compared to other groups (P < 0.05). Furthurmore, Li-
2.6.1. Amylase activity pase and chymotrypsin activity were significantly higher (P < 0.05) in
Amylase activity was estimated based on starch as substrate and fish fed treated diet compared control group.
measurement of maltose released by hydrolysis of substrate reacting The effects of FF, P and FF + P supplemented diets on total auto-
with 3, 5-dinitrosalicylic acid based on method previously described by chthonous intestinal microbiota and autochthonous LAB levels are
Wilchek and Bayer [17]. shown in Fig. 1. Our results revealed that total autochthonous intestinal
heterotrophic bacteria were significantly higher in all treatments
2.6.2. Trypsin and chymotrypsin activity compared to control group (P < 0.05) (Fig. 1. A). Interestingly, while
The trypsin (EC 3.4.21.4) activity was measured according to no autochthonous LAB were isolated from intestinal microbiota in
Erlanger et al. (1961). Benzoyl-DLarginine-p-nitroanilide (BAPNA) was control group, there were higher level of log CFU g−1 autochthonous
used as substrate and absorbance was read at 410 nm using spectro- LAB in Caspian white fish (Rutilus frisii kutum) fingerlings fed FF, P and
photometer (lightwave-S2000 UV/VIS). Chymotrypsin (EC 3.4.21.1) FF + P in compare to control group and highest level were observed in
activity was determined after Hummel (1959) with BTEE (N-benzoyl-L- fish fed FF + P supplemented diet (Fig. 1. B) (see Table 4).
tyrosine ethyl ester) as substrate and absorbance was read at 256 nm The effects of dietary administration single or combined of fer-
using spectrophotometer (lightwave-S2000 UV/VIS). manable fiber (Vitacel®) and probiotic PrimaLac® on the skin mucosal
immune parameters of Caspian white fish (Rutilus frisii kutum) finger-
2.6.3. ALP activity lings are presented in Table 5. The results indicated that skin mucosal
The digestive tract alkaline phosphatase activity was determined total protein level and protease activity increased in fish fed P and
using a commercial kit protocol (Pars Azmoun Co., Iran) and the ab- FF + P compared to other groups (P < 0.05). The lysozyme and ALP
sorbance was read at 405 nm. activity were significantly higher in treated groups compared to control
(P < 0.05); the highest level was observed in FF + P treatment
2.6.4. Lipase activity (P < 0.05).
Lipase activity was estimated as described by Borlongan [30]
through measurement of fatty acids released following enzymatic hy- 4. Discussion
drolysis of triglycerides in a stabilized emulsion of olive oil.
The results of present study showed that singular or combined ad-
2.7. Statistical analysis ministration of fermentable fiber (Vitacel®) and probiotic PrimaLac®
improved the growth performance and feed utilization of the Caspian
Prior to analysis of data the normality of data and homogeneity of white fish. This finding is in agreement with previous reports on posi-
variance were checked and confirmed. Then, One-way analysis of var- tive effects of dietary probiotic, prebiotic and synbiotic on growth
iance [31] followed by Duncan's multiple range tests was used for data performance and feed utilization of different species [32]. However,
analysis. Mean values were considered significantly different at there is limited information about dietary fermentable fiber (Vitacel®)
P < 0.05. Statistical analyses were conducted using SPSS statistical on growth performance and feed utilization of fishes. Yarahmadi, Ko-
package version 18.0 (SPSS Inc., Chicago, IL, USA). langi Miandare [17] reported that supplementation of rainbow trout
diet with fermanable fiber (Vitacel®) improved growth performance and
3. Results feed utilization. In agreement whit our results previuos study reported
that dietary supplemented with xylooligosaccharide as fermentable
Table 2, represents the growth performance parameters (weight component significantly increased growth performance and feed utili-
gain% (WG%)), specific growth rate (SGR% day−1), feed conversion zation of white fish (Rutilus frisii kutum) fry [26]. It seems that dietary
ratio (FCR) and protein efficiency ratio of the Rutilus frisii kutum fed fermentable fiber (Vitacel®) can improve feed utilization and growth
control, FF, P and FF + P supplemented diet. Our results revealed that performance through fermentation activity and producion of metabo-
administration of FF, P or their combination significantly increased lite such as short chain faty acid.
final body weight, WG%, and SGR and significantly decreased FCR (see In the present study, administration of fermentable fiber (Vitacel®),
Table 3). probiotic (PrimaLac®) and their combination increased the protein level
The study of body proximate composition showed that just crude of carcass body composition, while, other parameters such as moisture,
protein was significantly higher in fish fed P diet compared with other crude lipid and ash remained unaffected. In previous study by
groups (P < 0.05) and no statistically significant difference was Yarahmadi, Kolangi Miandare [17] documented that dietary

Table 2
Growth performance of Caspian white fish (Rutilus frisii kutum) fed diets supplemented with different experimental diets for 45 days. Values in a column with different
superscripts denote significant difference (P < 0.05). Values are presented as the mean ± SD.
Control FF P FF + P P values

Initial body weight (g) 0.58 ± 0.03 0.57 ± 0.03 0.54 ± 0.02 0.55 ± 0.02 0.41
Final body weight (g) 1.16 ± 0.03a 1.26 ± 0.01c 1.21 ± 0.01b 1.27 ± 0.03c 0.001
Weight gain (%) 101.29 ± 5.18a 123.42 ± 9.58b 122.23 ± 5.82b 131.13 ± 10.27b 0.010
SGR (% day−1) 0.67 ± 0.02a 0.77 ± 0.04b 0.77 ± 0.03b 0.81 ± 0.04b 0.008
FCR 2.68 ± 0.09b 2.36 ± 0.11a 2.37 ± 0.07a 2.28 ± 0.12a 0.005

Values are mean of triplicate determination (n=3).

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A.T. Mirghaed et al. Fish and Shellfish Immunology 77 (2018) 194–199

Table 3
Proximate body composition of Rutilus fresii kutumn fed diets supplemented with different experimental diets for 45 days. Values in a column with different
superscripts denote significant difference (P < 0.05). Values are presented as the mean ± SD.
Control FF P FF + P P values

Moisture 73.17 ± 0.51a 72.93 ± 1.57a 71.73 ± 0.82a 72.07 ± 1.17a 0.71
Crude protein 16.33 ± 0.74a 16.43 ± 0.35ab 17.47 ± 0.59b 17.30 ± 0.41ab 0.84
Crude lipid 9.73 ± 0.40a 9.97 ± 0.53a 9.67 ± 0.47a 9.73 ± 0.51a 0.07
ash 2.47 ± 0.25a 2.23 ± 0.32a 2.46 ± 0.25a 2.30 ± 0.36a 0.37

(Vitacel®) had no eeffect on amylase, alkaline phosphatase and trypsin

activity but lipase and chymotripsin activity increased in all treated
groups. Our results revealed that the effects of dietary supplementation
with probiotic PrimaLac® on digestive enzyme activity was more
prounaced compared other treatments. Previous study demonestrated
that feeding gilthead sea bream (Sparus aurata, L.) larvae with probiotic
Lactobacillus spp. significantly increased digestive enzyme activity [34].
To the best of our knowledge, there is no published data about effect of
dietary fermentable fiber on digestive enzyme activity of fish but pre-
vious studies have documented the positive effect of FOS on digestive
enzyme activity of Caspian roach fry (Rutilus rutilus) [35]. In contrast,
dietary inulin had no effect on digestive enzyme activity of common
carp (Cyprinus carpio) fry [36]. The increased digestive enzyme activ-
ities in the fish fed dietary supplemented with FF, P and FF + P might
be due to elevated exogenous microbial activities [37] which modu-
lated by the dietary fermentable fiber as prebiotic and probiotic Pri-
maLac®.
The intestinal microbiota of fish plays a key role in nutritional
function, enhances growth performance as well as stimulation of the
host immune system and resistant against pathogens [38,39]. Singular
or combined administration of fermentable fiber (Vitacel®) and pro-
biotic PrimaLac® significantly increased total autochthonous intestinal
microbiota and autochthonous LAB levels of fingerlings Rutilus fresii
kutum. To the [40]best of our knowledge, there is no published data
about the effects of fermentable fiber (Vitacel®) on fish intestinal mi-
Fig. 1. Total cultivable autochthonous bacterial (A) and autochthonous lactic
crobiota. However, previous study showed elevated TAC and LAB levels
acid bacteria (LAB) (B) levels (log CFU g−1 intestine) of Rutilus fresii kutumn fed in Caspian white fish (Rutilus frisii kutum) fry fed XOS supplemented
diets supplemented with different experimental diets for 45 days. Values in a diet [26]. Dietary fermentable fibre are components that do not hy-
column with different superscripts denote significant difference (P < 0.05). drolysed by digestive enzymes of non-ruminant animals such as fish,
Values are presented as the mean ± SD. and consequently are the main substrates for bacterial fermentation in
the gut [41]. Therefore, the increase of gut microflora of fish fed dietary
suplementation with fermentable fiber (Vitacel®) had no effect on body FF, P and FF + P may be regarded to improvement native of gut micro
composition of rainbow trout after 50 days feeding. In the present study flora [42].
dietary probiotic remarkably increased protein level of body composi- Fishes are dependent to innate immune system to combat with
tion in compare other groups which it may be regard higher level of different pathogens. The skin mucus play vital role because of providing
digestive enzyme activity. In agreement with our results previous study both physical and chemical barriers [43]. Total protein, lysozyme ac-
has shown that dietary Bacillus subtilis increased body protein deposi- tivity, alkaline phosphatase activity and protease activity are some
tion in Nile tilapia. The change of body protein deposition of fish can be important skin mucus immune parameters which can affect by phy-
relate to change in its synthesis, the rate of deposition in muscle, dif- siological and nutritional factors [43,44]. The results of present study
ferent growth rates of fish at different ages and type of prebiotic as documented that dietary fermentable fiber (Vitacel®), probiotic Pri-
suggested previously [33]. maLac® and their combination increased skin mucus immune para-
The present results showed positive effects of dietary fermentable meters. In agreement with our results, Hoseinifar, Roosta [45] reported
fiber (Vitacel®), probiotic (PrimaLac®) and their combination on diges- black swordtail (Xiphophorus helleri) fed dietary Lactobacillus acidophilus
tive enzyme activity. The results revealed that dietary fermentable fiber supplementation showed higher level of skin mucus total protein, al-
kalin phosphatase and antibacterial activity activity. Similar results

Table 4
Digestive enzyme activity of Rutilus fresii kutumn fed diets supplemented with different experimental diets for 45 days. Values in a column with different superscripts
denote significant difference (P < 0.05). Values are presented as the mean ± SD.
Control FF P FF + P P values

α-Amylase 1144.24 ± 8.36 a

1111.05 ± 45.26 a
1206.57 ± 21.53b
1245.01 ± 31.56 b
0.002
alkalin phosphatas 2604.68 ± 156.47a 2809.35 ± 129.59a 2767.1 ± 144.58a 3403.57 ± 343.30b 0.008
lipase activity 431.67 ± 32.53a 559.00 ± 24.02b 574.00 ± 27.87b 628.67 ± 26.50c 0.000
trypsin 0.05 ± 0.01a 0.05 ± 0.02a 0.07 ± 0.01ab 0.08 ± 0.02b 0.061
chymotrypsin 0.92 ± 0.06a 1.16 ± 0.17b 1.30 ± 0.12b 1.39 ± 0.14b 0.010

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A.T. Mirghaed et al. Fish and Shellfish Immunology 77 (2018) 194–199

Table 5
Skin mucosal immune parameters of Rutilus fresii kutumn fed diets supplemented with different experimental diets for 45 days. Values in a column with different
superscripts denote significant difference (P < 0.05). Values are presented as the mean ± SD.
Control FF P FF + P P values

Total protein 1.10 ± 0.20a 1.13 ± 0.21a 1.95 ± 0.23b 2.11 ± 0.18b 0.000
Lysozyme 131.4 ± 14.3a 186.1 ± 21.2b 240.4 ± 34.4c 286.1 ± 15.8d 0.000
Alkaline phosphatase 60.3 ± 35.1a 133.8 ± 32.2bc 81.9 ± 40.6ab 162.2 ± 30.6c 0.025
Protease 12.17 ± 2.36a 11.67 ± 1.53a 18.67 ± 3.06b 26.67 ± 2.52c 0.000

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 Update
Fish and Shellfish Immunology
Volume 81, Issue , October 2018, Page 445

DOI: https://doi.org/10.1016/j.fsi.2018.06.052
 Fish and Shellfish Immunology 81 (2018) 445

Contents lists available at ScienceDirect

Fish and Shellfish Immunology

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

Corrigendum

Corrigendum to ‘The effects singular or combined administration of T

fermentable fiber and probiotic on mucosal immune parameters, digestive
enzyme activity, gut microbiota and growth performance of Caspian white
fish (Rutilus frisii kutum) fingerlings’ [Fish and Shellfish Immunol. 77
(2018) 194–199]
Ali Taheri Mirghaeda,∗, Peyman Yarahmadia, Seyed Hossein Hosseinifarb, Davood Tahmasebib,
Nahid Gheisvandib, Alireza Ghaedic
a
Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
b
Department of Fisheries, Faculty of Fisheries and Environmental Sciences, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran
c
Agricultural Research, Education and Extension Organization, Iranian Fisheries Science Research Institute, Tehran, Iran

The authors regret affiliation of the last author needs to be changed Iranian Fisheries Science Research Institute, Tehran, Iran.
to: Agricultural Research, Education and Extension Organization, The authors would like to apologise for any inconvenience caused.

DOI of original article: https://doi.org/10.1016/j.fsi.2018.02.007

∗
Corresponding author.
E-mail address: [email protected] (A.T. Mirghaed).

https://doi.org/10.1016/j.fsi.2018.06.052

Available online 29 July 2018

1050-4648/ © 2018 Published by Elsevier Ltd.