Home Browse Boesenbergia pandurata application in Goldfish (Cyprinus carpio) Feed...
ALL Metrics
-
Views
-
Downloads
Get PDF
Get XML
Cite
Export
Track
▬
✚
Research Article
Revised

Boesenbergia pandurata application in Goldfish (Cyprinus carpio) Feed to Enhancing Fish Growth, Immunity System, and Resistance to Bacterial Infection

[version 2; peer review: 2 approved]
Esti Handayani Hardi
https://orcid.org/0000-0002-4660-7532
1,2, Gina Saptiani
https://orcid.org/0000-0002-2107-4856
1,2, Rudi Agung Nugroho
https://orcid.org/0000-0001-9006-7329
2,3, [...] fadlul Rahman1, Sulistyawati Sulistyawati1, Widyaningsih Rahayu1, Ali Supriansyah1, Irawan Wijaya Kusuma2,4
Esti Handayani Hardi
https://orcid.org/0000-0002-4660-7532
1,2, Gina Saptiani
https://orcid.org/0000-0002-2107-4856
1,2, [...] Rudi Agung Nugroho
https://orcid.org/0000-0001-9006-7329
2,3, fadlul Rahman1, Sulistyawati Sulistyawati1, Widyaningsih Rahayu1, Ali Supriansyah1, Irawan Wijaya Kusuma2,4
PUBLISHED 26 Nov 2021
Author details Author details
OPEN PEER REVIEW
REVIEWER STATUS

Abstract

Background: This study investigated how the inclusion of Boesenbergia pandurata extract (BPE) in goldfish feed affects fish growth, immunity, and resistance to infection by Aeromonas hydrophila and Pseudomonas fluorescens.  
Methods: Four fish feeds, were prepared by adding BPE at the concentrations of 0 (control), 2, 4, and 6 g kg-1, respectively, and 120 goldfish (Cyprinus carpio; initial weight 5 g) were separated into 12 boxes and fed with specific pellets and examined thrice. The experiment lasted 12 weeks, beginning with the different feeds, fish growth was measured at Weeks 4 and 8 after the feeding period. Moreover, a challenge test with pathogen bacteria to assay disease resistance was administered at Week 8 after the feeding period, and the survival rate and relative percentage of survival were quantified at Week 12.  
Results: At Week 8, the goldfish that were fed BPE-containing feeds were significantly heavier than the fish that received the control feed (pellet without BPE), and the highest weight gain, reaching 72.44 g, was obtained with Pellet 3; accordingly, the specific growth rate after BPE treatment (5.7%) was higher than that after control treatment. Conversely, the feed conversion ratio in the control group, 2.03, was higher than the ratios in the BPE groups, which were decreased to 0.55–0.90. Lastly, BPE treatment consistently enhanced the immunity parameters of goldfish (relative to control treatment) at weeks 4 and 8, and following BPE treatment, the rate of resistance against bacterial infection, 68.3%–77.0%, was higher than that after control treatment.  
Conclusions: BPE addition in goldfish feed clearly produces a positive effect by enhancing fish growth, immunity, and resistance to infection by pathogenic bacteria, and 4 g kg-1 is the optimal BPE concentration in feed prepared for goldfish.

Keywords

Boesenbergia pandurata, Cyprinus carpio, Phytobiotics, Aeromonas hydrophila, Pseudomonas fluorescens.

Corresponding author: Esti Handayani Hardi
Competing interests: No competing interests were disclosed.
Grant information: This study was supported by the Ministry of Education and Culture Republic of Indonesia (for laboratorial research) 2020-2022, contract No. 605/UN17.LI/PG/2021; and research funds were provided through Commercial Research from LPDP Fiscal Year 2019–2021, Contract No. PRJ-116/LPDP/2019. The head of both research grants is Esti Handayani Hardi.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Copyright:  © 2021 Hardi EH et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
How to cite: Hardi EH, Saptiani G, Nugroho RA et al. Boesenbergia pandurata application in Goldfish (Cyprinus carpio) Feed to Enhancing Fish Growth, Immunity System, and Resistance to Bacterial Infection [version 2; peer review: 2 approved]. F1000Research 2021, 10:766 (https://doi.org/10.12688/f1000research.52889.2) First published: 06 Aug 2021, 10:766 (https://doi.org/10.12688/f1000research.52889.1) Latest published: 26 Nov 2021, 10:766 (https://doi.org/10.12688/f1000research.52889.2)

Revised Amendments from Version 1

in the new version, I added some information based on Dr Abinawanto's revision. there some revision in this article (yellow bold) :
1. italic latin name (Cyprinus carpio)
2. revision in last reference.
3. method : adding the more information and literature to make more clearly about the dose. the dose or concentration was using this research come from the research before (Hardi et al., 2016;2017;2018;2019).
4. revision in discussed chapter with adding the statistic results.

See the authors' detailed response to the review by A. Abinawanto
See the authors' detailed response to the review by Angela Mariana Lusiastuti

Introduction

Over the past few years, the use of antibiotics in aquaculture has attracted considerable research attention, and enhanced public awareness of the health and safety of fishery products has led to the insistence that all involved parties concurrently prioritize quality assurance and food safety in aquaculture production, whether for export purposes or domestic consumption.1 Moreover, increasing innovation in aquaculture methods, particularly in the technology used, has been accompanied by a drastic increase in the production. Antibiotics application in aquaculture have been identified as residual materials in fish products and have emerged as the main reason for the frequent rejection of fish products.2 Conversely, the use of plant extracts as one of the ingredients in fish feed to stimulate fish growth and immunity is highly recommended because the extracts produce no resistance effects as residual wastes nor pose any threat to the environment.3–9

In aquaculture, the use of fish feed prepared from plant extracts offers certain benefits, such as stimulation of growth and immunity, enhancement of digestion and absorption, and resistance to diseases, and also allows for effective control of water quality.10–20 Notably, all reported single extracts of fingerroot (Boesenbergia pandurata) have been found to exert a strong antibacterial effect (80% inhibition) against Aeromonas hydrophila and Pseudomonas fluorescens both in vitro and in vivo, and fish feed containing plant extracts as an additive has been widely developed in aquaculture.21–28 Moreover, addition of garlic in fish feed increased fish immunity,26 and inclusion of thymol carvacrol effectively enhanced the growth and health of rainbow trout fries.29 This study comprehensively describes the effectiveness of the inclusion of B. pandurata (crude) extract (BPE) in fish feed to stimulate growth, immunity, and resistance to A. hydrophila and P. fluorescens infection in goldfish (Cyprinus carpio).

Methods

Aquarium and goldfish

Twelve aquariums (46 × 36 × 25.6 cm3) was used in this research with 25 L of water for 10 fish. There were four groups of different pellets and triplicates with the extracts added and a control. Each group used 10 goldfish, the fish were obtained from Rama Jaya Mahakam Company’s hatchery in Kutai Kartanegara regency, East Borneo, Indonesia, totalling 120 fish in this experiment.

The fish sample was collected using a fish sorting bucket of size 8 cm, fish that escaped from the 8 cm fish sorting bucket were collected. The fish species was goldfish (C. carpio), the fish sex was mixed between male and female, the developmental stage was larva size 8–9 cm, and the initial weight range was 5 ± 0.6 g.

Before the experiment, the goldfish were adapted to the natural environment for seven days and the fish were provided ad libitum access to commercial feed twice a day (at 8.00 a.m. and 4.00 p.m.). Moreover, the fish were first tested for infection by Aeromonas sp. and Pseudomonas sp. by incubating their isolated liver and kidneys with GSP (Himedia®) media; if the bacteria did not grow the fish were considered safe for use in the experiment, whereas if bacterial growth was constantly detected, the fish were soaked in 30% formalin for five minutes and the treatment was repeated for seven days until they were free from the bacteria, Aeromonas sp. and Pseudomonas sp.

Boesenbergia pandurata (BPE) preparation

The method of Hardi et al.30 was used for B. pandurata extraction; the rhizome was cleaned to remove soil and then minced into pieces (0.3–0.5 cm) by using a chopper, and the chopped fingerroot was dried at 40–45 °C for 48 h in an oven. The dried fingerroot was continuously blended and soaked in 96% ethanol for 48–72 h at a 1:10 ratio (i.e. 1 kg of fingerroot powder was soaked in 10 L of ethanol), and the process was continued to extraction for 24 h until the BPE was obtained with a viscosity of 10–11.

The dose of BPE utilized in carp feed is 2, 4, 6 g kg−1 of fish feed, which is the dose used in tilapia tests.5,6,10,30,35,48 Tilapia tests used this dose revealed an increase in growth and resistance to A. hydrophila and Pseudomonas sp. bacterial infections.

Composition of goldfish feed

BPE was used in goldfish feed as per the method of Hoseinifar et al.,31 with the following four feed pellets being applied as treatments:

Pellet 1 (control diets with BPE 0 g kg−1 fish feed).

Pellet 2 (supplemented-control diets with 2 g kg−1 fish feed of B. pandurata).

Pellet 3 (supplemented-control diets with 4 g kg−1 fish feed of B. pandurata).

Pellet 4 (supplemented-control diets with 6 g kg−1 fish feed of B. pandurata).

Goldfish feed was formulated as shown in Table 1.

Table 1. Formulated composition of fish feed (g kg−1).

IngredientsPellet 1Pellet 2Pellet 3Pellet 4
Shrimp flour400400400400
Wheat flour265265265265
Soybean flour135135135135
Soybean oil60606060
Fish oil60606060
Mineral premix30303030
Vitamin premix20202020
Binder20202020
vitamin C10864
BPE0246

Bacteria pathogen and challenges

The bacteria pathogen for challenges were A. hydrophila (EA-01) and P. fluorescens (EP-02) combination bacteria with bacterial density of 105 CFU mL−1 each bacteria and injection of as much as 0.1 mL were given to each fish. The bacteria were cultured in TSB (Merck®) medium for 24 h in 28–30 °C. Suspense bacteria was collected and centrifuged for 15 minutes in 7000 rpm and bacteria pellet was washing with sterile water twice, and then the bacteria suspense was counting density using TPC to measure 105 CFU mL−1, and bacteria had been properly prepared following the methods of Hardi et al.30

Challenge tests were carried out at week eight after feeding with different formulations, and mortality observations were checked from 24 hours after the first injection until week 12. The rate of resistance against both bacteria was measured using Relative Percent Survival (RPS).57 Eventually, the rate of protection against pathogen bacteria was also measured at week 12.

Water quality measurement

Three parameters of water quality—temperature, pH, and dissolved oxygen (DO)—were measured (twice daily, in the morning and evening) using a multi-parameter checker, whereas total ammonia nitrogen was measured using a spectrophotometer.

Examination of immunological parameters

Immunological parameters were evaluated by quantifying total leukocyte (TL) using cells mm−3 numbers and by measuring lysozyme activity (LA) according to the method of Parry et al.32 (with the results expressed using the unit μg mL−1). Subsequently, phagocytosis activity (“index phagocytic,” IP) the results expressed using percentage and respiratory burst activity (RBA) were examined as per the method of Van Doan et al.,33 with a few modifications.

Fish growth

Goldfish growth was measured according to the method of Hoseinifar et al.34 at Weeks 4 and 8 after the feeding period; growth was measured in terms of the following criteria: weight gain (WG), specific growth rate (SGR), and feed conversion ratio (FCR). These data were collected at 8 weeks after the feeding period:

WG = final weight (g) – initial weight (g);

SGR (%) = 100 × (ln final weight – ln initial weight)/duration of experiment;

FCR = feed offered (dry weight)/weight gain (wet weight).

Challenge test

The challenge test was administered by using A. hydrophila (EA-01) and P. fluorescens (EP-02); the bacteria were appropriately prepared as per the method of Hardi et al.6,35 The test was administered at Week 8, with 10 goldfish being exposed to a specific treatment; the fish were infected with the combined bacteria by means of intermuscular injection (0.1 mL each fish) of 105 CFU mL−1 of the bacteria at a 1:1 ratio. Subsequently, fish mortality was monitored from 24 h after the first injection until week 12. The rate of resistance toward both bacteria was measured by using the relative percentage of survival (RPS) value, as defined in the Amend57 method. Lastly, the rate of protection against infection with the pathogenic bacteria was measured at Week 12.

SR (%) = (final fish number/initial fish number) × 100;

RPS = 1 − (test mortality/control mortality) × 100.

Statistical analysis

The obtained data were analyzed for statistical significance by using MINITAB® 17 computer program (Minitab, RRID:SCR_014483), followed by the DUNCAN test. The average scores calculated were considered significantly different at P < 0.05.

Results

Growth performance

Goldfish growth performance was measured at Weeks 4 and 8 after the feeding period. At Week 4, WG and SGR were significantly higher (P < 0.05) after all BPE treatments than after the control treatment (no BPE) (Table 2). The highest SGR and WG were recorded in the case of the goldfish that received fish feed containing BPE at 4 g kg−1, and these values at Week 8 were considerably different from those measured for goldfish exposed to the control and others treatments.

Table 2. Growth performance (WG, SGR, FCR) at Weeks 4 and 8 of Cyprinus carpio treated with Boesenbergia pandurata extract (BPE).

ParametersWeekPellet 1Pellet 2Pellet 3Pellet 4
WG (g)410.30 ± 0.22a19.75 ± 0.2 b25.99 ± 0.4 b20.40 ± 0.1 b
819.67 ± 0.09 b47.32 ± 0.02 c72.44 ± 0.01 d44.67 ± 0.02 c
SGR (g)43.99 ± 0.02 a5.71 ± 0.01 b7.19 ± 0.01 c6.46 ± 0.04 b
85.70 ± 0.02 b8.39 ± 0.04 c10.54 ± 0.03 d8.92 ± 0.02c
FCR42.33 ± 0.11 a1.22 ± 0.08 b0.92 ± 0.09 c1.18 ± 0.1 b
82.03 ± 0.06 a0.85 ± 0.11 c0.55 ± 0.05 d0.90 ± 0.1 c

At Week 4, goldfish exposed to the control treatment grew by SGR 3.99–5.70 g; by contrast, treatment with BPE drastically enhanced growth, by 7.19–10.54 g in the case of the feed containing 4 g kg−1 BPE, and this was 2- or even 3-fold higher than that with the control treatment (Table 2). Moreover, consistent results were obtained at Week 8 after the third fish feeding, with the growth doubling relative to the initial weight and being markedly distinct from that measured after the control treatment. Furthermore, besides growth, feed efficiency also increased, as demonstrated by the FCR increase (relative to control) being substantially lower (0.55) at Week 8 in the case of goldfish that were fed Pellet 3 (BPE at 4 g kg−1), and this FCR value was also significantly different (P < 0.05) from those calculated after treatment with BPE at the two other concentrations (2 and 6 g kg−1), which produced roughly equal effects.

Immunological parameters

Next, immunological parameters were measured at Weeks 4 and 8 after the feeding period (Table 3). Activity of Lysozymes (LA) in addition to control of feed-fish in BPE was significantly higher (P < 0.05) (Table 3). Compared with other formulas, the highest value was recorded in fish fed pellet 3 (4 g kg−1). No significant difference (P > 0.05) between fish fed 2 and 6 g kg−1 has been observed (Table 3). Similarly, in additional groups the activity of index phagocytic (PI), compared with the control of fed fish, was significantly higher (P < 0.05) (Table 3). Fish fed dietary pellets 3 showed the highest values (Table 3). In relation to the activity of respiratory burst (RBA), fish supplemented diets (P < 0.05) were significantly higher than the control (no BPE). No significant difference (P > 0.05) between pellet 2 and pellet 4 was however observed. In comparison to controls after 8 weeks of feeding, and 12 weeks after challenges, significant (P < 0.05) differences in total leukocyte (TL) activity were observes in fish-feed supplements (Table 3).

Table 3. Immunological parameters (RBA, IP, LA, and TL) at Weeks 4 and 8 of goldfish treated with Boesenbergia pandurata extract (BPE).

ParametersWeekPellet 1Pellet 2Pellet 3Pellet 4
IP (%)420.7 ± 0.58a53.7 ± 0.71 b64.9 ± 1,21 b55.4 ± 0.4 b
824.9 ± 0.4 b61.3 ± 0.67 c68.4 ± 0.51 d64.7 ± 0.75 c
LA (μg mL−1)43.9 ± 0.15 a5.7 ± 0.08 b6.2 ± 0.15 c6.0 ± 0.21 b
83.9 ± 0.1 b5.8 ± 0.05 c6.54 ± 0.06 d6.0 ± 0.1 c
TL (104) (cell mm−3)42.4 ± 0.12 a5.22 ± 0.1 b7.92 ± 0.15 c5.81 ± 0.1 b
82.6 ± 0.1 a6.85 ± 0.1 c8.55 ± 0.1 d6.90 ± 0.1 c
RBA (OD)40.3 ± 0.06a0.6 ± 0.03 b0.8 ± 0.06 b0.7 ± 0.06 b
80.5 ± 0.03 b0.8 ± 0.10 c1.1 ± 0.12 d0.9 ± 0.06 c

Challenge test

The rate of survival and death and RPS were measured at Week 12 after completion of the challenge test. Unexpectedly, the results showed that treatment with BPE at all concentrations markedly increased the RPS, by >60%, relative to control, although BPE at 4 g kg−1 provided the maximal protection (99.56%) against A. hydrophila and P. fluorescens infection (Table 4).

Table 4. Rate of survival, death and relative percentage of survival of goldfish at Week 12 after challenge test against A. hydrophila and P. fluorescens bacterial infection.

ParametersPellet 1Pellet 2Pellet 3Pellet 4
SR (%)1768.37772
Mortality (%)82.331.72328
RPS (%)627266

The results of the experiment examining protection against pathogenic bacteria showed a significant increase in goldfish disease resistance, amounting to 68.3–77.0% following all BPE treatments, although no significant difference was measured between the distinct concentrations of BPE (P > 0.05); moreover, the highest RPS value (77.0%) was obtained with BPE used at 4 g kg−1 in the fish feed (Table 4). In conclusion, relative to Pellet 1, which did not contain BPE, all other pellets drastically increased the rate of survival after pathogenic bacterial infection.

Water quality

No significant differences were present in the quality of water in the goldfish aquaculture media when BPE was included in fish feed. The temperature was set at 29 ± 0.2 °C, the DO was 7.6 ± 0.6 mg L−1, the pH range was 7.2 ± 0.5, and the total ammonia nitrogen was 0.69 ± 0.24 mg L−1.

Discussion

Prebiotics prepared from plant extracts have been widely used in aquacultures. The results have shown that plant extracts added to feed enhance fish growth,36,37 maximize immunity,38 and strengthen disease resistance and thus reduce infection by pathogenic bacteria.39–43

In this study, we aimed to evaluate how BPE inclusion in fish feed affects goldfish growth, immunity, and disease resistance (i.e. resistance against infection by the bacteria A. hydrophila and P. fluorescens). The results comprehensively showed that BPE addition in feed exerted the positive effects of enhancing fish growth and strengthening the immune system. Similar results were reported by Hoseinifar et al.31,34,41 and Carbone & Faggio:44 Addition of the extract of medlar leaf (Mespilus germanica) consistently produced a large impact, with markedly enhanced performance being recorded in terms of growth, skin mucus levels, and serum concentrations of immune-response markers. Our study also showed increased growth of goldfish, particularly at Week 8, after consumption of feed containing BPE at 2, 4, and 6 g kg−1. Thus, BPE served as a growth-stimulating additive for the goldfish aquaculture here. Plant extracts included in fish feed have been reported to markedly increase WG, SGR, protein efficiency ratio, energy retention, feed efficiency, and protein retention.15,45–47 Moreover, champignon (Agaricus bisporus) powder extract included in fish feed effectively enhanced growth and acted as an immunostimulant in the case of goldfish fries.47 Our results here indicate that the growth, immune response, and disease resistance of goldfish were strongly influenced by the immunomodulatory effect of BPE.

In previous studies, BPE use at 400–900 ppm successfully strengthened the immune system and enhanced the disease resistance of Nile tilapia toward infection by A. hydrophila and P. fluorescens.10,48 Moreover, flavonoid and levamisole addition in feed potently intensified the antigen-phagocytosing effect of monocytes and macrophages,45 and inclusion of BPE alone or together with other extracts boosted leucocyte numbers and consistently accelerated pathogen elimination inside the body of Nile tilapia.4,6,11 Subsequently, BPE-containing vaccines were also found to increase the antibody levels and phagocytic index in Nile tilapia to enhance the immune system and produce accelerated and strengthened resistance against infection by pathogenic bacteria.4 An enhancement of monocyte and macrophage function in pathogen elimination, mucosal immune response, growth, and gene transcription is generally observed in fish that are fed plant-extract-containing fish feed formulated with peptin, oligosaccharides, and flavonoids,49,50 and the use of combinations of plant extracts in aquaculture is also well established. Moreover, addition of Ferula assafoetida extract to fish feed was shown to successfully enhance nonspecific immune-system response and growth in carp fish.51 The increased growth caused by fish feed-efficiency enhancement and FCR reduction in BPE-fed goldfish occurred because of the positive physiological impact that carbohydrates (oligosaccharides) and the essential nutrient pectin produced on the digestive system by reducing glucose absorbance52 and postponing gastric emptiness.53 Ho et al.54 and Naqash et al.55 reported that pectin and its derivatives are components that can potentially be used as prebiotics for aquaculture.

Conclusion

BPE addition in fish feed provided to goldfish markedly enhances fish growth, feed efficiency, FCR, immunity, and resistance against infection by the bacteria A. hydrophila and P. fluorescens. Moreover, inclusion of 4 g kg−1 BPE in the feed more strongly affects the aforementioned parameters than does BPE added at other concentrations.

Ethical approval

The Commission of Ethical Research for Health, Medical Faculty of Mulawarman University, approved this study with the number LOA 04/KEPK-FK/1/2020. The application of B. pandurata, S. ferox, and Z. Zerumbet in freshwater fish feed to improve fish growth, immune system, and resistance to bacterial infection is the research theme. Esti Handayani Hardi of Mulawarman University's Faculty of Fisheries and Marine Science chaired this study. This study lasted six months (from January to June 2020). For a period of 12 weeks, a feed composition with extracts was tested to see how well the fish grew, how well their immune systems worked, and how well they were protected from infections.

Data availability

Underlying data

Open Science Framework, OSF 2021: Underlying data for ‘Boesenbergia pandurata application in goldfish (Cyprinus carpio) feed to enhance fish growth, immunity, and resistance to bacterial infection’. https://doi.org/10.17605/OSF.IO/827EN.56

This project contains the following underlying data:

  • • Raw data of the growth Performa (Weight gain)

  • • Raw data of the growth Performa (Specific growth rate)

  • • Raw data of the growth Performa (Feed conversion ratio)

  • • Raw data of the Immunological Parameters (Index phagocytic)

  • • Raw data of the Immunological parameters (Total leukocyte)

  • • Raw data of the Immunological parameters (Lysozyme activity)

  • • Raw data of the Immunological parameters (Respiratory burst activity)

  • • Raw data of the Survival Rate

Data are available under the terms of the Creative Commons Zero “No rights reserved” data waiver (CC0 1.0 Public domain dedication).

Acknowledgements

Both the researchers and the writers thank Universitas Mulawarman, LPDP, for providing the funds to conduct this research. We are especially grateful to the students from the Faculty of Marine and Fisheries Science, Universitas Mulawarman, for their support and efforts in conducting this research.

References

  • 1.  DJPB RI: Direktur Jenderal Perikanan Budidaya No. Kep.35/DJ-PB/2012. Tata Cara Pengisian Formulir Data Teknis Obat Ikan. Direktur Jenderal Perikanan Budidaya Republik Indonesia.2012.
  • 2.  CAC: Codex Alimentarius Commission. Code of Practice for Fish and Fishery Products. CAC/RCP 52-2003, Rev. 2010. 2010.Reference Source
  • 3.  Cheng LP, Hu QP: Antibacterial activities and mechanism of action of acetone extracts from Rabdosia rubescens. Aceh Int J Sci Technol. 2015; 4(1): 1–6. Publisher Full Text
  • 4.  Hardi EH, et al.: Simultaneous Administration of Boesenbergia pandurata Extract and Vaccination to Stimulate Immune Response in Tilapia, Oreochromis niloticus. Pak J Biol Sci. 2019; 22(9): 419–426. PubMed Abstract | Publisher Full Text
  • 5.  Hardi EH, et al.: Borneo herbal plant extracts as a natural medication for prophylaxis and treatment of Aeromonas hydrophila and Pseudomonas fluorescens infection in tilapia (Oreochromis niloticus). F1000Res. 2018; 7. PubMed Abstract | Publisher Full Text | Free Full Text
  • 6.  Hardi EH, N R, Kusuma IW, et al.: Immunomodulatory effect and disease resistance from three Borneo plant extracts to Aeromonas hydrophila and Pseudomonas fluorescens in tilapia, Oreochromis niloticus. Aquacultura Indonesiana. 2019; 20(1): 41–47. Publisher Full Text
  • 7.  Harikrishnan R, et al.: Innate immune response and disease resistance in Carassius auratus by triherbal solvent extracts. Fish Shellfish Immunol. 2009; 27(3): 508–515. PubMed Abstract | Publisher Full Text
  • 8.  Raa J, et al.: The use of immunostimulants to increase resistance of aquatic organisms to microbial infections (M. Shariff, RP Subasinghe, and JR Arthur, Eds.). Diseases in Asian Aquaculture. 1990. 39(4): p. 26–29.
  • 9.  Yılmaz S, et al.: Effect of combination of dietary Bacillus subtilis and trans-cinnamic acid on innate immune responses and resistance of rainbow trout, Oncorhynchus mykiss to Yersinia ruckeri. Aquaculture Res. 2020; 51(2): 441–454. Publisher Full Text
  • 10.  Hardi EH, et al.: Uji in vitro Gabungan Ekstrak Boesenbergia pandurata, Solanum ferox, Zingimber zerumbet terhadap Bakteri Patogen pada Ikan Nila. Jurnal Veteriner. 2018; 19(1): 35–44. Publisher Full Text
  • 11.  Hardi EH, et al.:Inhibition of fish bacteria pathogen in tilapia using a concoction three of Borneo plant extracts. In: IOP Conference Series. Earth and Environmental Science:IOP Publishing;2018.
  • 12.  Hussein HA, et al.: Phytochemical screening, metabolite profiling and enhanced antimicrobial activities of microalgal crude extracts in co-application with silver nanoparticle. Bioresources & Bioprocessing. 2020; 7(1): 39. Publisher Full Text
  • 13.  Kurniasih T, et al.: Isolasi, seleksi, dan identifikasi bakteri dari saluran pencernaan ikan lele sebagai kandidat probiotik. Jurnal Riset Akuakultur. 2013; 8(2): 277–286. Publisher Full Text
  • 14.  Lananan F, et al.: Symbiotic bioremediation of aquaculture wastewater in reducing ammonia and phosphorus utilizing Effective Microorganism (EM-1) and microalgae (Chlorella sp.). Int Biodeterioration & Biodegradation. 2014; 95(A): 127–134. Publisher Full Text
  • 15.  Okey I, Gabriel U, Deekae S: The use of synbiotics (Prebiotic and probiotic) in aquaculture development. Sumerianz J Biotechnol. 2018; 1(2): 51–60.
  • 16.  Ringø E, Song S: Application of dietary supplements (synbiotics and probiotics in combination with plant products and β-glucans) in aquaculture. Aquaculture Nutr. 2016; 22(1): 4–24. Publisher Full Text
  • 17.  Torrecillas S, et al.: Feeding European sea bass (Dicentrarchus labrax) juveniles with a functional synbiotic additive (mannan oligosaccharides and Pediococcus acidilactici): An effective tool to reduce low fishmeal and fish oil gut health effects? Fish Shellfish Immunol. 2018; 81: 10–20. PubMed Abstract | Publisher Full Text
  • 18.  Van Nguyen N, et al.: Evaluation of dietary Heat-killed Lactobacillus plantarum strain L-137 supplementation on growth performance, immunity and stress resistance of Nile tilapia (Oreochromis niloticus). Aquaculture. 2019; 498: 371–379. Publisher Full Text
  • 19.  Waagbø R, Remø SC: Functional diets in fish health management. Aquaculture Health Management. Elsevier;2020. p. 187–234. Publisher Full Text
  • 20.  Zhang C-N, et al.: Combined effects of dietary fructooligosaccharide and Bacillus licheniformis on innate immunity, antioxidant capability and disease resistance of triangular bream (Megalobrama terminalis). Fish Shellfish Immunol. 2013; 35(5): 1380–1386. PubMed Abstract | Publisher Full Text
  • 21.  Amenyogbe E, et al.: The exploitation of probiotics, prebiotics and synbiotics in aquaculture: present study, limitations and future directions.: a review. Aquaculture Int. 2020: p. 1–25. Publisher Full Text
  • 22.  Brenes A, Roura E: Essential oils in poultry nutrition: Main effects and modes of action. Animal Feed Sci Technol. 2010; 158(1-2): 1–14. Publisher Full Text
  • 23.  Elala NMA, Ragaa NM: Eubiotic effect of a dietary acidifier (potassium diformate) on the health status of cultured Oreochromis niloticus. J Adv Res. 2015; 6(4): 621–629. PubMed Abstract | Publisher Full Text | Free Full Text
  • 24.  Giannenas I, et al.: Assessment of dietary supplementation with carvacrol or thymol containing feed additives on performance, intestinal microbiota and antioxidant status of rainbow trout (Oncorhynchus mykiss). Aquaculture. 2012; 350: 26–32. Publisher Full Text
  • 25.  Hassaan MS, Soltan MA: Evaluation of essential oil of fennel and garlic separately or combined with Bacillus licheniformis on the growth, feeding behaviour, hemato-biochemical indices of Oreochromis niloticus (L.) fry. J Aquaculture Res Devel. 2016. 7: p. 422–429. Publisher Full Text
  • 26.  Lee JY, Gao Y: Review of the application of garlic, Allium sativum, in aquaculture. J World Aquaculture Soc. 2012; 43(4): 447–458.
  • 27.  Puvača N, et al.: Beneficial effects of phytoadditives in broiler nutrition. World's Poult Sci J. 2013; 69(1): 27–34. Publisher Full Text
  • 28.  Ramezanzadeh S, Kenari AA, Esmaeili M: Immunohematological parameters of rainbow trout (Oncorhynchus mykiss) fed supplemented diet with different forms of barberry root (Berberis vulgaris). Comparative Clin Pathol. 2020; 29(1): 177–187. Publisher Full Text
  • 29.  Ahmadifar E, Falahatkar B, Akrami R: Effects of dietary thymol-carvacrol on growth performance, hematological parameters and tissue composition of juvenile rainbow trout, Oncorhynchus mykiss. J Appl Ichthyol. 2011; 27(4): 1057–1060. Publisher Full Text
  • 30.  Hardi EH, et al.: Antibacterial activities of some Borneo plant extracts against pathogenic bacteria of Aeromonas hydrophila and Pseudomonas sp. AACL Bioflux. 2016; 9(3): 638–646.
  • 31.  Hoseinifar SH, Zoheiri F, Lazado CC: Dietary phytoimmunostimulant Persian hogweed (Heracleum persicum) has more remarkable impacts on skin mucus than on serum in common carp (Cyprinus carpio). Fish Shellfish Immunol. 2016; 59: 77–82. PubMed Abstract | Publisher Full Text
  • 32.  Parry RM Jr, Chandan RC, Shahani KM: A rapid and sensitive assay of muramidase. Proc Soc Exp Biol Med. 1965; 119(2): 384–386. PubMed Abstract | Publisher Full Text
  • 33.  Van Doan H, et al.: Effects of Cordyceps militaris spent mushroom substrate and Lactobacillus plantarum on mucosal, serum immunology and growth performance of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 2017; 70: 87–94. Publisher Full Text
  • 34.  Hoseinifar SH, et al.: Enrichment of common carp (Cyprinus carpio) diet with medlar (Mespilus germanica) leaf extract: Effects on skin mucosal immunity and growth performance. Fish Shellfish Immunol. 2017; 67: 346–352. PubMed Abstract | Publisher Full Text
  • 35.  Hardi EH, et al.: Antibacterial activity of Boesenbergia pandurata, Zingiber zerumbet and Solanum ferox extracts against Aeromonas hydrophila and Pseudomonas sp. Nusantara Biosci. 2016; 8(1): 18–21. Publisher Full Text
  • 36.  Kathia CM, et al.: Probiotics used in Biofloc system for fish and crustacean culture: A review. Int J Fisheries Aquatic Studies. 2017; 5(5): 120–125.
  • 37.  Rodrigues MS, et al.: Mannoprotein dietary supplementation for Pacific white shrimp raised in biofloc systems. Aquaculture. 2018; 488: 90–95. Publisher Full Text
  • 38.  Lara-Flores M, et al.: Use of the bacteria Streptococcus faecium and Lactobacillus acidophilus, and the yeast Saccharomyces cerevisiae as growth promoters in Nile tilapia (Oreochromis niloticus). Aquaculture. 2003; 216(1-4): 193–201. Publisher Full Text
  • 39.  Gatesoupe FJ: The effect of three strains of lactic bacteria on the production rate of rotifers, Brachionus plicatilis, and their dietary value for larval turbot, Scophthalmus maximus. Aquaculture. 1991; 96(3-4): 335–342. Publisher Full Text
  • 40.  Gildberg A, Mikkelsen H: Effects of supplementing the feed to Atlantic cod (Gadus morhua) fry with lactic acid bacteria and immuno-stimulating peptides during a challenge trial with Vibrio anguillarum. Aquaculture. 1998; 167(1-2): 103–113. Publisher Full Text
  • 41.  Hoseinifar SH, et al.: Effects of date palm fruit extracts on skin mucosal immunity, immune related genes expression and growth performance of common carp (Cyprinus carpio) fry. Fish Shellfish Immunol. 2015; 47(2): 706–711. PubMed Abstract | Publisher Full Text
  • 42.  Li P, Gatlin D: Evaluation of the prebiotic GroBiotic®-A and brewers yeast as dietary supplements for sub-adult hybrid striped bass (Morone chrysops×M. saxatilis) challenged in situ with Mycobacterium marinum. Aquaculture. 2005; 248: 197–205. Publisher Full Text
  • 43.  Mohamed K, Fattah BA, Eid A: Evaluation of using some feed additives on growth performance and feed utilization of monosex Nile tilapia (Oreochromis niloticus) fingerlings. Agricultural Res J, Suez Canal University. 2007; 7(3): 49–54.
  • 44.  Carbone D, Faggio C: Importance of prebiotics in aquaculture as immunostimulants. Effects on immune system of Sparus aurata and Dicentrarchus labrax. Fish Shellfish Immunol. 2016; 54: 172–178. Publisher Full Text
  • 45.  Abd Elmonem A, Shalaby S, El-Dakar A: Response of red tilapia to different levels of some medicinal plants by-products black seed and roquette seed meals. Proc First Conf Egyptian Aquacultural Society. 2002. Publisher Full Text
  • 46.  Dawood MA, Koshio S: Recent advances in the role of probiotics and prebiotics in carp aquaculture: a review. Aquaculture. 2016; 454: 243–251. Publisher Full Text
  • 47.  Zou HK, et al.: Agaricus bisporus powder improved cutaneous mucosal and serum immune parameters and up-regulated intestinal cytokines gene expression in common carp (Cyprinus carpio) fingerlings. Fish Shellfish Immunol. 2016; 58: 380–386. PubMed Abstract | Publisher Full Text
  • 48.  Hardi EH, et al.: Immunomodulatory and antibacterial effects of Boesenbergia pandurata, Solanum ferox, and Zingiber zerumbet on tilapia, Oreochromis niloticus. AACL Bioflux. 2017; 10(2): 182–190.
  • 49.  Faggio C, et al.: Cytotoxicity, haemolymphatic parameters, and oxidative stress following exposure to sub-lethal concentrations of quaternium-15 in Mytilus galloprovincialis. Aquatic Toxicol. 2016; 180: 258–265. PubMed Abstract | Publisher Full Text
  • 50.  Miandare HK, et al.: The effects of galactooligosaccharide on systemic and mucosal immune response, growth performance and appetite related gene transcript in goldfish (Carassius auratus gibelio). Fish Shellfish Immunol. 2016; 55: 479–483. Publisher Full Text
  • 51.  Safari R, et al.: The effects of dietary Myrtle (Myrtus communis) on skin mucus immune parameters and mRNA levels of growth, antioxidant and immune related genes in zebrafish (Danio rerio). Fish Shellfish Immunol. 2017; 66: 264–269. Publisher Full Text
  • 52.  Grundy MM, et al.: Re-evaluation of the mechanisms of dietary fibre and implications for macronutrient bioaccessibility, digestion and postprandial metabolism. Br J Nutr. 2016; 116(5): 816–833. PubMed Abstract | Publisher Full Text | Free Full Text
  • 53.  Schwartz SE, et al.: Sustained pectin ingestion delays gastric emptying. Gastroenterology. 1982; 83(4): 812–817. PubMed Abstract
  • 54.  Ho YY, Lin CM, Wu MC: Evaluation of the prebiotic effects of citrus pectin hydrolysate. J Food Drug Anal. 2017; 25(3): 550–558. PubMed Abstract | Publisher Full Text
  • 55.  Naqash F, et al.: Emerging concepts in the nutraceutical and functional properties of pectin—A Review. Carbohydr Polym. 2017; 168: 227–239. PubMed Abstract | Publisher Full Text
  • 56.  Hardi EH, et al.: Boesenbergia pandurata application in goldfish (Cyprinus carpio) feed to enhance fish growth, immunity, and resistance to bacterial infection. OSF. 2021. Publisher Full Text
  • 57.  Amend DF: Potency testing of fish vaccines. Fish Biologics: Serodiagnostics and Vaccines. 1981; 49: 447–454.

Comments on this article Comments (0)

Version 2
VERSION 2 PUBLISHED 06 Aug 2021
Comment
Author details Author details
Competing interests
Grant information
Article Versions (2)
Copyright
Download
 
Export To
metrics
Views Downloads
F1000Research - -
PubMed Central
Data from PMC are received and updated monthly.
 - -
Citations
SEE MORE DETAILS
CITE
how to cite this article
Hardi EH, Saptiani G, Nugroho RA et al. Boesenbergia pandurata application in Goldfish (Cyprinus carpio) Feed to Enhancing Fish Growth, Immunity System, and Resistance to Bacterial Infection [version 2; peer review: 2 approved]. F1000Research 2021, 10:766 (https://doi.org/10.12688/f1000research.52889.2)
NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article.
track
receive updates on this article
Track an article to receive email alerts on any updates to this article.

Open Peer Review

Current Reviewer Status: ?
Key to Reviewer Statuses VIEW
ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions
Version 2
VERSION 2
PUBLISHED 26 Nov 2021
Revised
Views
3
Cite
Reviewer Report 07 Dec 2021
Angela Mariana Lusiastuti, Research Institute for Freshwater Aquaculture and Fisheries Extension (RIFAFE), Bogor, Indonesia 
Approved
VIEWS 3
https://doi.org/10.5256/f1000research.79656.r101240
The revisions are ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Lusiastuti AM. Reviewer Report For: Boesenbergia pandurata application in Goldfish (Cyprinus carpio) Feed to Enhancing Fish Growth, Immunity System, and Resistance to Bacterial Infection [version 2; peer review: 2 approved]. F1000Research 2021, 10:766 (https://doi.org/10.5256/f1000research.79656.r101240)
The direct URL for this report is:
https://f1000research.com/articles/10-766/v2#referee-response-101240
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
Report a concern
Views
3
Cite
Reviewer Report 07 Dec 2021
A. Abinawanto, Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia, Depok, Indonesia 
Approved
VIEWS 3
https://doi.org/10.5256/f1000research.79656.r101239
This research article provides the information (data) comprehensively. The study was designed appropriately and the method was explained in detail. This research article was also supported by statistical analysis. The conclusion was drawn adequately. The current literature was cited in ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Abinawanto A. Reviewer Report For: Boesenbergia pandurata application in Goldfish (Cyprinus carpio) Feed to Enhancing Fish Growth, Immunity System, and Resistance to Bacterial Infection [version 2; peer review: 2 approved]. F1000Research 2021, 10:766 (https://doi.org/10.5256/f1000research.79656.r101239)
The direct URL for this report is:
https://f1000research.com/articles/10-766/v2#referee-response-101239
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
Report a concern
Version 1
VERSION 1
PUBLISHED 06 Aug 2021
Views
15
Cite
Reviewer Report 18 Nov 2021
A. Abinawanto, Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia, Depok, Indonesia 
Approved with Reservations
VIEWS 15
https://doi.org/10.5256/f1000research.56217.r100290
The manuscript is quite good, generally. I made some corrections to the manuscript. These include species names being written in italic. In some tables should also add a “plus-minus mark” (±) following the average. In the Abstract, it should be ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Abinawanto A. Reviewer Report For: Boesenbergia pandurata application in Goldfish (Cyprinus carpio) Feed to Enhancing Fish Growth, Immunity System, and Resistance to Bacterial Infection [version 2; peer review: 2 approved]. F1000Research 2021, 10:766 (https://doi.org/10.5256/f1000research.56217.r100290)
The direct URL for this report is:
https://f1000research.com/articles/10-766/v1#referee-response-100290
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
Report a concern
  • Author Response 26 Nov 2021
    Esti Handayani Hardi, Microbiology environmental Laboratory, Faculty of Fisheries and Marine Science, Mulawarman University, Samarinda/East Kalimantan, 75123, Indonesia
    26 Nov 2021
    Author Response
    Thank you for the review of my article, I made some revisions
    :
    1. Checking again the italics 
       
    2.  We have added more information and literature to
    ... Continue reading
    Report a concern
  • Respond or Comment
COMMENTS ON THIS REPORT
  • Author Response 26 Nov 2021
    Esti Handayani Hardi, Microbiology environmental Laboratory, Faculty of Fisheries and Marine Science, Mulawarman University, Samarinda/East Kalimantan, 75123, Indonesia
    26 Nov 2021
    Author Response
    Thank you for the review of my article, I made some revisions
    :
    1. Checking again the italics 
       
    2.  We have added more information and literature to
    ... Continue reading
    Report a concern
Views
12
Cite
Reviewer Report 22 Oct 2021
Angela Mariana Lusiastuti, Research Institute for Freshwater Aquaculture and Fisheries Extension (RIFAFE), Bogor, Indonesia 
Approved with Reservations
VIEWS 12
https://doi.org/10.5256/f1000research.56217.r95791
I think this script is good, using herbs as an alternative to chemical drugs. Abstract, Introduction, Methods, and Results are good. The focus of the Discussion should be on BPE as an immunostimulant, not as a prebiotic. If you want ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Lusiastuti AM. Reviewer Report For: Boesenbergia pandurata application in Goldfish (Cyprinus carpio) Feed to Enhancing Fish Growth, Immunity System, and Resistance to Bacterial Infection [version 2; peer review: 2 approved]. F1000Research 2021, 10:766 (https://doi.org/10.5256/f1000research.56217.r95791)
The direct URL for this report is:
https://f1000research.com/articles/10-766/v1#referee-response-95791
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
Report a concern
  • Author Response 15 Nov 2021
    Esti Handayani Hardi, Microbiology environmental Laboratory, Faculty of Fisheries and Marine Science, Mulawarman University, Samarinda/East Kalimantan, 75123, Indonesia
    15 Nov 2021
    Author Response
    Thank you very much for the revision and response.

    In this research, I want to evaluate the effect of Boesenbergia pandurata Application in Goldfish (Cyprinus carpio) specifically on growth, ... Continue reading
    Report a concern
  • Respond or Comment
COMMENTS ON THIS REPORT
  • Author Response 15 Nov 2021
    Esti Handayani Hardi, Microbiology environmental Laboratory, Faculty of Fisheries and Marine Science, Mulawarman University, Samarinda/East Kalimantan, 75123, Indonesia
    15 Nov 2021
    Author Response
    Thank you very much for the revision and response.

    In this research, I want to evaluate the effect of Boesenbergia pandurata Application in Goldfish (Cyprinus carpio) specifically on growth, ... Continue reading
    Report a concern

Comments on this article Comments (0)

Version 2
VERSION 2 PUBLISHED 06 Aug 2021
Comment

Open Peer Review

Reviewer Status

Alongside their report, reviewers assign a status to the article:

Approved
The paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations
A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved
Fundamental flaws in the paper seriously undermine the findings and conclusions

Reviewer Reports

Invited Reviewers
1 2
Version 2
(revision)
 26 Nov 21 		read read
Version 1
06 Aug 21 		read read
  1. Angela Mariana Lusiastuti, Research Institute for Freshwater Aquaculture and Fisheries Extension (RIFAFE), Bogor, Indonesia
  2. A. Abinawanto, Universitas Indonesia, Depok, Indonesia

Comments on this article

All Comments(0)

Add a comment
Sign up for content alerts

Browse by related subjects

    keyboard_arrow_left Back to all reports
    keyboard_arrow_left Back to all reports
    keyboard_arrow_left Back to all reports
    keyboard_arrow_left Back to all reports
    Alongside their report, reviewers assign a status to the article:
    Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
    Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
    Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
    Sign In
    If you've forgotten your password, please enter your email address below and we'll send you instructions on how to reset your password.

    The email address should be the one you originally registered with F1000.
    Email address not valid, please try again

    You registered with F1000 via Google, so we cannot reset your password.

    To sign in, please click here.

    If you still need help with your Google account password, please click here.

    You registered with F1000 via Facebook, so we cannot reset your password.

    To sign in, please click here.

    If you still need help with your Facebook account password, please click here.

    Code not correct, please try again
    Email us for further assistance.
    Server error, please try again.