Dietary phytogenics and galactomannan oligosaccharides in low fish meal and fish oil-based diets for European sea bass (Dicentrarchus labrax) juveniles: Effects on gut health and implications on in vivo gut bacterial translocation
Autoři:
Silvia Torrecillas aff001; Genciana Terova aff002; Alex Makol aff003; Antonio Serradell aff001; Victoria Valdenegro aff004; Elisabetha Gini aff002; Marisol Izquierdo aff001; Félix Acosta aff001; Daniel Montero aff001
Působiště autorů:
Grupo de Investigación en Acuicultura (GIA), IU-ECOAQUA, Universidad de Las Palmas de Gran Canaria, Crta. Taliarte s/n, Telde, Las Palmas, Canary Islands, Spain
aff001; Department of Biotechnology and Life Sciences, University of Insubria, Via J.H. Dunant, Varese, Italy
aff002; Delacon Biotechnik GmbH, Weissenwolffstrasse, Steyregg, Austria
aff003; Biomar A/S. BioMar AS, POB 1282 Sluppen, Trondheim, Norway
aff004
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0222063
Souhrn
European sea bass were fed four low FM/FO (10%/6%) diets containing galactomannan oligosaccharides (GMOS), a mixture of garlic oil and labiatae plants oils (PHYTO), or a combination of both functional products (GMOSPHYTO) for 63 days before exposing the fish to an intestinal Vibrio anguillarum infection combined with crowding stress. In order to evaluate functional diets efficacy in terms of gut health maintenance, structural, cellular, and immune intestinal status were evaluated by optical and electron microscopy and gene expression analyses. A semi-automated software was adapted to determine variations in goblet cell area and mucosal mucus coverage during the challenge test. Feeding with functional diets did not affect growth performance; however, PHYTO and GMOS dietary inclusion reduced European sea bass susceptibility to V. anguillarum after 7 days of challenge testing. Rectum (post-ileorectal valve) showed longer (p = 0.001) folds than posterior gut (pre-ileorectal valve), whereas posterior gut had thicker submucosa (p = 0.001) and higher mucus coverage as a result of an increased cell density than rectum. Functional diets did not affect mucosal fold length or the grade of granulocytes and lymphocytes infiltration in either intestinal segment. However, the posterior gut fold area covered by goblet cells was smaller in fish fed GMOS (F = 14.53; p = 0.001) and PHYTO (F = 5.52; p = 0.019) than for the other diets. PHYTO (F = 3.95; p = 0.049) reduced posterior gut goblet cell size and increased rodlet cell density (F = 3.604; p = 0.068). Dietary GMOS reduced submucosal thickness (F = 51.31; p = 0.001) and increased rodlet cell density (F = 3.604; p = 0.068) in rectum. Structural TEM analyses revealed a normal intestinal morphological pattern, but the use of GMOS increased rectum microvilli length, whereas the use of PHYTO increased (p≤0.10) Ocln, N-Cad and Cad-17 posterior gut gene expression. After bacterial intestinal inoculation, posterior gut of fish fed PHYTO responded in a more controlled and belated way in terms of goblet cell size and mucus coverage in comparison to other treatments. For rectum, the pattern of response was similar for all dietary treatments, however fish fed GMOS maintained goblet cell size along the challenge test.
Klíčová slova:
Biology and life sciences – Nutrition – Diet – Anatomy – Digestive system – Gastrointestinal tract – Rectum – Body fluids – Mucus – Bioengineering – Biotechnology – Genetic engineering – Genetically modified organisms – Physiology – Cell biology – Cellular types – Animal cells – Blood cells – White blood cells – Lymphocytes – Granulocytes – Immune cells – Medicine and health sciences – Immunology – Engineering and technology – People and places – Geographical locations – Europe
Zdroje
1. Ringø E, Løvmo L, Kristiansen M, Bakken Y, Salinas I, Myklebust R, et al. Lactic acid bacteria vs. pathogens in the gastrointestinal tract of fish: a review. Aquacult. Res. 2010; 41: 451–467. doi: 10.1111/j.1365-2109.2009.02339.x
2. Torrecillas S, Makol A, Betancor MB, Montero D, Caballero MJ, Sweetman J, et al. Enhanced intestinal epithelial barrier health estatus on European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides, Fish Shellfish Immunol. 2013; 34:1485–1495. doi: 10.1016/j.fsi.2013.03.351 23528875
3. Lazado CC, Caipang CMA. Mucosal immunity and probiotics in fish. Fish Shellfish Immunol 2014; 39:78–89. doi: 10.1016/j.fsi.2014.04.015 24795079
4. Barceló A, Claustre J, Moro F, Chayvialle JA, Cuber JC, Plaisancié P. Mucin secretion is modulated by luminal factors in the isolated vascularly perfused rat colon. Gut 2000; 46:218–224. doi: 10.1136/gut.46.2.218 10644316
5. Castro R, Tafalla C. Overview of fish immunity. In: Beck BH, Peatman E, editors. Mucosal Health in Aquaculture; 2015. pp.3–54. doi: 10.1016/B978-0-12-417186-2.00002–9
6. Ellis AE. Innate host defense mechanisms of fish against viruses and bacteria. Dev. Comp. Immunol. 2001; 25:827–839. 11602198
7. Van der Marel M, Schroers V, Neuhaus H, Steinhagen D. Chemotaxis towards, adhesion to, and growth in carp gut mucus of two Aeromonas hydrophila strains with different pathogenicity for common carp, Cyprinus carpio. L. J. Fish Dis. 2008; 31:321–330. doi: 10.1111/j.1365-2761.2008.00902.x 18355183
8. Torrecillas S, Makol A, Benítez-Santana T, Caballero MJ, Montero D, Sweetman J, et al. Reduced gut bacterial translocation in European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides (MOS). Fish Shellfish Immunol 2011; 30:674–681. doi: 10.1016/j.fsi.2010.12.020 21195771
9. Van Itallie CM, Anderson JM. Claudins and epithelial paracellular transport. Annu. Rev. Physiol. 2006; 68: 403–429. doi: 10.1146/annurev.physiol.68.040104.131404 16460278
10. Holthofer B, Windoffer R, Troyanovsky S, Leube RE. Structure and function of desmosomes. Int. Rev Cytol. 2007; 264; 65–163. doi: 10.1016/S0074-7696(07)64003-0 17964922
11. Sundh H, Kvamme BO, Fridell F, Olsen RE, Ellis T, Taranger GL, et al. Intestinal barrier function of Atlantic salmon (Salmo salar L.) post smolts is reduced by common sea cage environments and suggested as a possible physiological welfare indicator. BMC PhysioL. 2010; 10:22. doi: 10.1186/1472-6793-10-22 21062437
12. Gomez D, Sunyer JO, Salinas I. The mucosal immune system of fish: the evolution of tolerating commensals while fighting pathogens, Fish Shellfish Immunol. 2013; 35: 1729–1739. doi: 10.1016/j.fsi.2013.09.032 24099804
13. Rombout JHWM, Abelli L, Picchietti S, Scapigliati G, Kiron V. Teleost intestinal immunology. Fish Shellfish Immun. 2011; 31(5):616–26. doi: 10.1016/j.fsi.2010.09.001
14. Sundh H. Chronic stress and intestinal barrier function. Implications for infection and inflammation in intensive salmon aquaculture. PhD thesis University of Gothenburg. 2009; ISBN: 978-90-8585-512-5.
15. Urán PA, Gonçalves A, Taverne-Thiele JJ, Schrama JW, Verreth JAJ, Rombout JHWM. Soybean meal-induced enteritis in common carp (Cyprinus carpio L.) and the gene expression of inflammatory mediators in intestinal leukocytes. Fish Shellfish Immunol. 2008; 25:751–760. doi: 10.1016/j.fsi.2008.02.013 18954997
16. Urán PA, Schrama JW, Rombout JHWM, Taverne-Thiele JJ, Obach A, Koppe W, et al. Time-related changes of the intestinal morphology of Atlantic salmon (Salmo salar L.) at two different soy bean meal inclusion levels. J. Fish Dis. 2009; 32:733–744. doi: 10.1111/j.1365-2761.2009.01049.x 19515072
17. Benedito-Palos L, Navarro JC, Sitjà-Bobadilla A, Bell JG, Kaushik S, Pérez- Sánchez. High levels of vegetable oils in plant protein-rich diets fed to gilthead seabream (Sparus aurata L.): growth performance, muscle fatty acid profiles and histological alterations of target tissues. Br. J. Nutr. 2008; 100: 992–1003. doi: 10.1017/S0007114508966071 18377678
18. Øverland M, Sørensen M, Storebakken T, Penn M, Krogdahl Å, Skrede A. Pea protein concentrate substituting fish meal or soybean meal in diets for Atlantic salmon (Salmo salar)—effect on growth performance, nutrient digestibility, carcass composition, gut health, and physical feed quality, Aquaculture 2009; 288: 305–311. doi: 10.1016/j.aquaculture.2008.12.012
19. Krogdahl A, Penn M, Thorsen J, Refstie S, Bakke AM. Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids, Aquac. Res. 2010; 41: 333–344. doi: 10.1111/j.1365-2109.2009.02426.x
20. Torrecillas S, Montero D, Caballero MJ, Pittman KA, Custodio M, Campo A, et al. Dietary mannan oligosaccharides: counteracting the side effects of soybean meal oil inclusion on European sea bass (Dicentrarchus labrax) gut health and skin mucosa mucus production? Front. Immunol. 2015; 6:397. doi: 10.3389/fimmu.2015.00397 26300883
21. Montero D, Benitez-Dorta V, Caballero MJ, Ponce M, Torrecillas S, Izquierdo MS, et al. Dietary vegetable oils: effects on the expression of immune-related genes in Senegalese sole (Solea senegalensis) intestine, Fish. Shellfish Immunol. 2015; 44: 100–108. doi: 10.1016/j.fsi.2015.01.020 25655325
22. Calduch-Giner JA, Sitjà-Bobadilla A, Davey GC, Cairns MT, Kaushik S, Perez-Sanchez J. Dietary vegetable oils do not alter the intestine transcriotome of gilthead sea bream (Sparus aurata) but modulate the transcriptomic response to infection with Enteromyxum leei. BMC Genomics 2012 13: 470. doi: 10.1186/1471-2164-13-470 22967181
23. Torrecillas S, Mompel D, Caballero MJ, Montero D, Merrifield D, Rodiles A, et al. Effect of fish meal and fish oil replacement by vegetable meals and oils on gut health of European sea bass (Dicentrarchus labrax), Aquaculture 2017a; 468: 386–398. doi: 10.1016/j.aquaculture.2016.11.005
24. Torrecillas S, Rivero- Ramírez F, Izquierdo MS, Caballero MJ, Makol A, Suarez-Bregua P, 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. doi: 10.1016/j.fsi.2018.07.007 29981880
25. Silva PF, McHurk C, Thompson KD, Jayasuriya NS, Bron JE. Development of a quantitative semi-automated system for intestinal morphology assessment in Atlantic salmon, using image analysis. Aquaculture 2015; 442:100–111.
26. Zhou QC, Buentello JA, Gatlin III DM. The effects of dietary prebiotics on growth performance, immune response and intestinal morphology of red drum (Sciaenops ocellatus). Aquaculture 2010; 309: 253–257. doi: 10.1017/S0007114512001754
27. Abdelhamid AM, Soliman AAA. Possibility of using fenugreek seeds or cresson seeds in tilapia diets. J. Arab. Aquacult. Soc. 2012; 7: 75–90.
28. Zaki M, Labib E, Nour A, Tonsy H, Mahmoud S. Effect of some medicinal plant’s diets on mono sex Nile tilapia (Oreochromis niloticus), growth performance, feed utilization and physiological parameters. APCBEE Procedia. 2012; 4:220–7.
29. Yilmaz S, Ergün S, Celik ES. Effect of dietary herbal supplements on some physiological conditions of sea bass Dicentrarchus labrax. J. Aquat. Anim. Health 2013; 25: 98–103. 23914399
30. Reverter M, Bontemps N, Lecchini D, Banaigs B, Sasal P. Use of plant extracts in fish aquaculture as an alternative to chemotherapy: Current status and future perspectives. Aquaculture 2014; 433: 50–61. doi: 10.1016/j.aquaculture.2014.05.048
31. Awad E, Cerezuela R, Esteban MA. Effects of fenugreek (Trigonella foenum graecum) on gilthead seabream (Sparus aurata L.) Immune status and growth performance. Fish Shellfish Immunol. 2015; 45: 454–464. doi: 10.1016/j.fsi.2015.04.035 25956720
32. Cunha JA, Heizmann BM, Baldisserotto B. The effects of essential oils and their major compounds on fish bacterial pathogens–a review. J. Appl. Microbiol. 2018; 125: 328–344. doi: 10.1111/jam.13911 29742307
33. Torrecillas S, Makol A, Caballero MJ, Montero D, Robaina L, Real F, et al. Immune stimulation and improved infection resistance in European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides. Fish Shellfish Immunol. 2007; 23: 969–981. doi: 10.1016/j.fsi.2007.03.007 17766145
34. Ellis AE. General principles of fish vaccination. In: Ellis AE, editor. Fish Vaccination. Academic Press, London; 1988. pp. 1–19.
35. AOAC. Official methods of analysis. Association of Official Analytical Chemists, Washington, DC. 2000.
36. Folch J, Lees M, Sloane-Stanley GH. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 1957; 226: 497–509. 13428781
37. Christie WW. Lipid analysis. 2nd revised ed. Oxford: Pergamon Press; 1982.
38. Izquierdo MS, Arakawa T, Takeuchi T, Haroun R, Watanabe T. Effect of n-3 HUFA levels in Artemia on growth of larval Japanese flounder (Paralichthys olivaceus). Aquac. Nutr. 1992; 2:183–191. doi: 10.1016/0044-8486(92)90163-F
39. Martoja R, Martoja-Pierson M. Técnicas de Histología Animal. Barcelona: Toray- Masson S.A; 1970.
40. Hoffman EO, Flores TR, Coover J, Garret HB. Polychrome stains for high resolution light microscopy. Lab Med 1983; 14:779–781.
41. Terova G, Cattaneo AG, Preziosa E, Bernardini G, Saroglia M. Impact of acute stress on antimicrobial polypeptides mRNA copy number in several tissues of marine sea bass (Dicentrarchus labrax). BMC Immunol. 2011; 12:69. ISSN: 1471-2172. http://www.biomedcentral.com/1471-2172/12/69. doi: 10.1186/1471-2172-12-69 22204309
42. Torrecillas S, Robaina L, Caballero MJ, Montero D, Calandra G, Mompel D, et al. Combined replacement of fishmeal and fish oil in European sea bass (Dicentrarchus labrax): Production performance, tissue composition and liver morphology. Aquaculture 2017; 474: 101–112. doi: 10.1016/j.aquaculture.2017.03.031
43. Guerreiro A, Oliva-Teles P, Enes P. Prebiotics as functional ingredients: focus on Mediterranean fish aquaculture. Rev. Aquacult. 2017; 10: 800–832. doi: 10.1111/raq.12201
44. Sutili FJ, Gatlin DM, Rossi D, Heinzmann BM, Baldisserotto B. Plant essential oils as fish diet additives: benefits on fish health and stability in feed. Rev.Aquacult. 2017; 0:1–11. doi: 10.1111/raq.12197
45. Mudgil D. The Interaction Between Insoluble and Soluble Fiber. In: Samman RA, editor. Dietary fiber for the prevention of cardiovascular disease. Los Angeles: Elsevier, AP; 2017. pp.35–59. doi: 10.1016/B978-0-12-805130-6.00003–3
46. Raa J. The use of immune-stimulants in fish and shellfish feeds. In: Cruz -Suárez LE, Ricque-Marie D, Tapia-Salazar M, Olvera-Novoa MA, Civera-Cerecedo R, editors. Avances en Nutrición Acuícola V. V. Simposio Internacional de Nutrición Acuícola. 19–22 noviembre, 2000. Mérida, Yucatán, Mexico.47-49]47–49]
47. Bahi A, Guardiola F, Messina C, Mahdhi A, Cerezuela R, Santulli A, et al. Effects of dietary administration of fenugreek seeds, alone or in combination with probiotics, on growth performance parameters, humoral immune response and gene expression of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol. 2017; 60: 50–8. doi: 10.1016/j.fsi.2016.11.039 27856325
48. Guardiola FA, Bahi A, Bakhrouf A, Esteban MA. Effects of dietary supplementation with fenugreek seeds, alone or in combination with probiotics, on gilthead seabream (Sparus aurata L.) skin mucosal immunity, Fish Shellfish Immunol. 2017; 65: 169–178. doi: 10.1016/j.fsi.2017.04.014 28433714
49. Montero D, Serradell A, Kalinowski T, Makol A, Valdenegro V, Acosta F, et al. Dietary prebiotics and phytogenics in low fish meal and fish oil-based diets for European see bass (dicentrarchus labrax): Effects on stress resistance. 18th International Symposium in Fish Nutrition and Feeding. Las Palmas, June 3rd-7th June 2018. Session 6.1. 2018. Available from: http://www.isfnf2018.com/wp-content/uploads/2018/06/ORAL-6.1.pdf
50. Shalaby AM, Khattab YA, Abdel Rahman AM. Effects of garlic (Allium sativum) and chloramphenicol on growth performance, physiological parameters and survival of Nile tilapia (Oreochromis niloticus). J. Venom. Anim. Toxins 2006; 12: 172–201. doi: 10.1590/S1678-91992006000200003
51. Sahu BKD, Das BK, Mishra BK, Pradhan J, Sarangi N. Effect of Allium sativumn on the immunity and survival of Labeo rohita infected with Aeromonas hydrophila. J. Appl. Ichthyol. 2007; 23: 80–86. doi: 10.1111/j.1439-0426.2006.00785.x
52. Aly SM, Atti NMA, Mohamed MF. Effect of garlic on the survival, growth, resistance and quality of Oreochromis niloticus. 8th International Symposium on Tilapia in Aquaculture, 2008. pp. 277–296.
53. Nya EJ, Austin B. Use of garlic, Allium sativum, to control Aeromonas hydrophila infection in rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis. 2009; 32: 963–970. doi: 10.1111/j.1365-2761.2009.01100.x 19843196
54. Aly SM, Mohamed MF. Echinacea purpurea and Allium sativum as immunostimulants in fish culture using Nile tilapia (Oreochromis niloticus). J. Anim. Physiol. Anim. Nutr. 2010; 94; 31–39. doi: 10.1177/1329878X1013400105
55. Muzaffar F, Ansal MD, Dhawan A. Effect of garlic (Allium sativum L) supplemented on survival and growth of common carp (Cyprinus carpio L.) J. Anim. Nutr. 2017; 34:91–98.
56. Nya EJ, Dawood Z, Austin B. The garlic component, allicin, prevents disease caused by Aeromonas hydrophila in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis. 2010; 33: 293–300. doi: 10.1111/j.1365-2761.2009.01121.x 20082660
57. Thanikachalam K, Kasi M, Rathinam X. Effect of garlic peel on growth, hematological parameters and disease resistance against Aeromonas hydrophila in African catfish Clarias gariepinus (Bloch) fingerlings. Asian Pac. J. Trop. Med., 2010; 3: 614–618. doi: 10.1016/S1995-7645(10)60149-
58. Talpur AD, Ikhwanuddin M. Dietary effects of garlic (Allium sativum) on haemato-immunological parameters, survival, growth, and disease resistance against Vibrio harveyi [infection in Asian sea bass, Lates calcarifer (Bloch). Aquaculture 2012; 364: 6–12. doi: 10.1016/j.aquaculture.2012.07.035
59. Hoseinifar SH, Khalili M, Rufchaei R, Raeisi M, Attar M, Cordero H, 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. 2011; 47: 706–711. doi: 10.1016/j.fsi.2015.09.046
60. Metwally MAA. Effects of Garlic (Allium sativum) on Some Antioxidant Activities in Tilapia Nilotica (Oreochromis niloticus). World J. Fish Marine Sci. 2009; 1: 56–64.
61. Mohebbi A, Nematollahi A, Dorcheh EE, Asa FG. Influence of dietary garlic (Allium sativum) on the antioxidative status of rainbow trout (Oncorhynchus mykiss). Aquacult. Res. 2011; 1–10. doi: 10.1111/j.1365-2109.2011.02922.x
62. El-Barbary M. Detoxification and antioxidant effects of garlic and curcumin in Oreochromis niloticus injected with aflatoxin B1 with reference to gene expression of glutathione peroxidase (GPx) by RT-PCR. Fish physiol. Biochem. 2015; 42: 617–29. doi: 10.1007/s10695-015-0164-4 26590820
63. Abdel-Daim MM, Abdelkhalek NK, Hassan AM. Antagonistic activity of dietary allicin against deltamethrin-induced oxidative damage in freshwater Nile tilapia; Oreochromis niloticus. Ecotoxicol Environ Saf. 2015; 111:146–52. doi: 10.1016/j.ecoenv.2014.10.019 25450927
64. Büyükdeveci Effects of garlic-supplemented diet on growth performance and intestinal microbiota of rainbow trout (Oncorhynchus mykiss). Aquaculture 2018; 486: 170–174. doi: 10.1016/j.aquaculture.2017.12.022
65. Abutbul S, Golan A, Barazani O, Zilberg D. Use of Rosmarinus officinalis as a treatment against Streptococcus iniae in tilapia (Oreochromis sp.). Aquaculture 2004; 238:97–105. doi: 10.1016/j.aquaculture.2004.05.016
66. Amer SA, Metwally AE, Shimaa AAA.The influence of dietary supplementation of cinnamaldehyde and thymol on the growth performance, immunity and antioxidant status of monosex Nile tilapia fingerlings (Oreochromis niloticus). Egypt. J Aquat. Res. 2018; 44: 251–256. doi: 10.1016/j.ejar.2018.07.004
67. Zilberg D, Tal A, Froyman N, Abutbul S, Dudai N, Golan-Goldhirsh A. Dried leaves of Rosmarinus officinalis as a treatment for streptococcosis in tilapia. J Fish Dis. 2010; 33:361–369. doi: 10.1111/j.1365-2761.2009.01129.x 20158579
68. Yilmaz S, Ergün S, Çelik ES. Effects of herbal supplements on growth performance of sea bass (Dicentrarchus labrax): Change in body composition and some blood parameters. J. BioSci. Biotech. 2012; 1: 217–222.
69. Yilmaz S, Ergün S, Çelik ES. Effect of Dietary Spice Supplementations on Welfare Status of Sea Bass, Dicentrarchus labrax L. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 2014; 86: 229–237. doi: 10.1007/s40011-014-0444-2
70. Zheng ZlL Justin YWT, Liu HY Zhou XH, Xiang X Wang KY. Evaluation of oregano essential oil (Origanum heracleoticum L.) on growth, antioxidant effect and resistance against Aeromonas hydrophila in channel catfish (Ictalurus punctatus). Aquaculture 2009; 292:214–218. doi: 10.1016/j.aquaculture.2009.04.025
71. Nazzaro F, Fratianni F, de Martino L, Coppola R, Feo V. Effect of essential oils on pathogenic bacteria. Pharmaceuticals 2013; 6:1451–1474. doi: 10.3390/ph6121451 24287491
72. Bulfon C, Volpatti D, Galeotti M. Current research on the use of plant-derived products in farmed fish. Aquacult. Res. 2015; 46: 513–551. doi: 10.1111/are.12238
73. Bouyahya A, Bakri Y, Et-Touys A, Talbaoui A, Khouchlaa A, Charfi S, et al. Resistance aux antibiotiques et mecanismes d’action des huiles essentielles contre les bacteries. Phytotherapie 2017; 14: 1–11. doi: 10.1007/s10298-017-1118-z
74. Lillehoj H, Liu Y, Calsamiglia S, Fernández-Miyakawa ME, Chi F, Craven RL, et al. Phytochemicals as antibiotic alternatives to promote growth and enhance host health. Vet Res 2018; 49:76, doi: 10.1186/s13567-018-0562-6 30060764
75. Harder W. Anatomy of Fishes. Stuttgart: E. Schweizerbart’sche. 1975
76. Wilson JM, Castro LFC. Morphological diversity of the gastrointestinal tract in fishes. In: Grosell M, Farrell AP, Brauner CJ, editors. The Multifunctional Gut of Fish, Fish Physiology, vol. 30. Oxford: Elsevier Academic Press; 2011. pp. 1–55.
77. Baniak N, Luan X, Grunow A, Machen TE, Ianowski JP. The cytokines interleukin-1b and tumor necrosis factor-a stimulate CFTR-mediated fluid secretion by swine airway submucosal glands. Am. J. Physiol. Lung Cell Mol. Physiol. 2012; 303: L327–333. doi: 10.1152/ajplung.00058.2012 22683572
78. Kandori H, Hirayama K, Takeda M, Doi K. Histochemical, lectin-histochemical and morphometrical characteristics of intestinal goblet cells of germ-free and conventional mice. Exp. Animal 1996, 45: 155–160.
79. Miller HRP. Gastrointestinal mucus, a medium for survival and for elimination of parasitic nematodes and protozoa. Parasitology 1987; 94: S77–S100. doi: 10.1017/s0031182000085838 3295692
80. Janice JK, Waliul IK. Goblet Cells and Mucins: Role in Innate Defense in Enteric Infections. Pathogens 2013; 2:55–70. doi: 10.3390/pathogens2010055 25436881
81. Lilleeng E, Penn M, Haugland Ø, Xu C, Bakke AM, Krogdahl A, et al. Decreased expression of TGF-b, GILT and T-cell markers in the early stages of soybean enteropathy in Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 2009; 27, 65–72. doi: 10.1016/j.fsi.2009.04.007 19427383
82. Bakke-McKellep AM, Frøystad MK, Lilleeng E, Dapra F, Refstie S, Krogdahl A, et al. Response to soy: T-cell-like reactivity in the intestine of Atlantic salmon, Salmo salar L. J. Fish Dis. 2007; 30: 13–25. doi: 10.1111/j.1365-2761.2007.00769.x 17241401
83. Romarheim OH, Hetland DL, Skrede A, Øverland M, Mydland LV, Landsverk T. Prevention of soya-induced enteritis in Atlantic salmon (Salmo salar) by bacteria grown on natural gas is dose dependent and related to epithelial MHC II reactivity and CD8a1 intraepithelial lymphocytes. Br. J. Nutr. 2013; 109: 1062–1070. doi: 10.1017/S0007114512002899 22813713
84. Ishikawa N, Wakelin D, Mahida YR. Role of T helper 2 cells in intestinal goblet cell hyperplasia in mice infected with Trichinella spiralis. Gastroenterology 1997; 113: 542–549. doi: 10.1053/gast.1997.v113.pm9247474 9247474
85. Khan WI, Collins SM. Immune-mediated alteration in gut physiology and its role in host defence in nematode infection. Parasite Immunol. 2004; 26: 319–326. doi: 10.1111/j.0141-9838.2004.00715.x 15679628
86. Miller HR, Nawa Y. Nippostrongylus brasiliensis: intestinal goblet-cell response in adoptively immunized rats. Exp. Parasitol. 1979; 47: 81–90. doi: 10.1016/0014-4894(79)90010-9 421768
87. McDole JR, Wheeler LW, McDonald KG, Wang B, Konjufca V, Knoop KA, et al. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature 2012; 483: 345–349. doi: 10.1038/nature10863 22422267
88. Jaensson E, Uronen-Hansson H, Pabst O, Ekstenn B, Tina J, Coombes JL, et al. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 2008; 205:2139–2149. doi: 10.1084/jem.20080414 18710932
89. Pelaseyed T, Bergström JH, Gustafsson JK, Ermund A, Birchenough GM, Schütte A, et al. The mucus and mucins of the goblet cells and enterocytes. provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunol Rev. 2014; 260:8–20. doi: 10.1111/imr.12182 24942678
90. Torrecillas S, Montero D, Izquierdo, MS. Improved health and growth of fish fed mannan oligosaccharides: potential mode of action, Fish Shellfish Immunol. 2014; 36: 525–544. doi: 10.1016/j.fsi.2013.12.029 24412165
91. Dimitroglou A, Merrifield D, Carnevali O, Picchietti S, Avella M, Daniels C, et al. Microbial manipulations to improve fish health and production e a Mediterranean perspective. Fish Shellfish Immunol. 2011; 30:1–16. doi: 10.1016/j.fsi.2010.08.009 20801223
92. Johansson MEV, Sjövall H, Hansson GC. The gastrointestinal mucus system in health and disease. Nat. Rev. Gastroenterol. Hepatol. 2013; 10: 352–361. doi: 10.1038/nrgastro.2013.35 23478383
93. Amirkolaie AK, Verreth JAJ, Schrama JW. Effect of gelatinization degree and inclusion level of dietary starch on the characteristics of digesta and faeces in Nile tilapia (Oreochromis niloticus (L.)). Aquaculture 2006; 260: 194–205. doi: 10.1016/j.aquaculture.2013.02.009
94. Leenhouwers JI, ter Veld M, Verreth A.J, Schrama JW. Digesta characteristiscs and performance of African catfish (Clarias gariepinus) fed cereal grains that differ in viscosity. Aquaculture 2007; 264: 330–341. doi: 10.1016/j.aquaculture.2007.01.003
95. Desai MS, Seekatz AM, Koropatkin NM, Kamada N, Hickey CA, Wolter M, et al. A Dietary Fiber-Deprived Gut Microbiota Degrades the Colonic Mucus Barrier and Enhances Pathogen Susceptibility. Cell 2006; 17: 1339–1353. doi: 10.1016/j.cell.2016.10.043
96. Velin AK, Ericson AC, Braaf Y, Wallon C, Söderholm JD: Increased antigen and bacterial uptake in follicle associated epithelium induced by chronic psychological stress in rats. Gut 2004; 53:494–500. doi: 10.1136/gut.2003.028506 15016742
97. Olsen RE, Sundell K, Mayhew TM, Myklebust R, Ringø.: Acute stress alters intestinal function of rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture 2005; 250: 480–495. doi: 10.1016/j.aquaculture.2005.03.014
98. Montero D, Izquierdo MS. Welfare and health of fish fed vegetable oils as alternative lipid sources to fish oil, in: Turchini G, Ng W, Tocher D, editors. Fish Oil Replacement and Alternative Lipid Sources in Aquaculture Feeds, Cambridge: CRC Press, 2010; pp. 439–485.
99. Ray A, Ghosh K, Ringø E. Enzyme‐producing bacteria isolated from fish gut: a review. Aquacult. Nutr. 2012; 18: 465–492. doi: 10.1111/j.1365-2095.2012.00943.x
100. Ming WJ, Bersani L, Mantovani A. Tumor necrosis factor is chemotactic for monocytes and polymorphonuclear leukocytes, J. Immunol. 1987; 138: 1469–1474. 3805724
101. Young SH, Ye J, Frazer D, Shi X, Castranova V. Molecular mechanism of tumor necrosis factor-a production in 133-B-glucan (zymosan)-activated macrophages, J. Biol. Chem. 2001; 276: 20781–20787. doi: 10.1074/jbc.M101111200 11259437
102. Aubin J, Gatesoupe FJ, Labbe L, Lebrun L. Trial of probiotics to prevent the vertebral column compression syndrome in rainbow trout (Oncorhynchus mykiss Walbaum), Aquacult. Res. 2005; 36: 758–767. doi: 10.1111/j.1365-2109.2005.01280.x
103. Boonanuntanasarn S, Wongsasak U, Pitaksong T, Chaijamrus S. Effects of dietary supplementation with b-glucan and synbiotics on growth, haemolymph chemistry, and intestinal microbiota and morphology in the Pacific white shrimp, Aquacult. Nutr. 2016; 22: 837–845. doi: 10.1111/anu.12302
104. Guo JJ, Kuo CM, Chuang YC, Hong JW, Chou RL, Chen TI. The Effects of Garlic-Supplemented Diets on Antibacterial Activity against Streptococcusiniae and on Growth in Orange-Spotted Grouper, Epinepheluscoioides. Aquaculture 2012; 364–365: 33–38. doi: 10.1016/j.aquaculture.2012.07.023
105. Campbell TW. Clinical Chemistry of Fish and Amphibians. In: Thrall MA, Baker DC, Campbell TW, De Nicola D, Fettman MJ, Lassen ED, Rebar A, Weiser G, EDITORS., Veterinary Hematology and Clinical Chemistry: Text and Clinical Case Presentations, Philadelphia: Lippincott Williams and Wilkins, 2004. Pp. 499–517.
106. İrkin LC, Murat Y, Sevdan Y, Masashi M. Toxicological Evaluation of Dietary Garlic (Allium sativum) Powder in European Sea Bass Dicentrarchus labrax Juveniles. Food and Nutrition Sci. 2014; 5: 989–996. doi: 10.4236/fns.2014.511109
107. Vickers T. A study of the intestinal epithelium of the goldfish Carassius auratus: its normal structure, the dynamics of cell replacement, and the changes induced by salts of cobalt and manganese. Q J Microsc. Sci. 1962; 103:93–110.
108. Manera M, Simoni E, Dezfuli BS. The effect of dexamethasone on the occurrence and ultrastructure of rodlet cells in goldfish. J fish Biol. 2001; 59: 1239–1248. doi: 10.1111/j.1095-8649.2001.tb00188.x
109. Iger Y, Abraham M. Rodlet cells in the epidermis of fish exposed to stressors. Tissue Cell 1997; 29:431–438. doi: 10.1016/s0040-8166(97)80029-8 18627825
110. Reite OB, Evensen O. Inflammatory cells of teleostean fish: A review focusing on mast cells/eosinophilic granule cells and rodlet cells. Fish Shellfish Immunol. 2006; 20: 195–208. doi: 10.1016/j.fsi.2005.01.012
111. Sitjà-Bobadilla A, Estensoro I, Pérez-Sánchez J. Immunity to gastrointestinal microparasites of fish. Dev. Comp. Immunol. 2016; 64: 187–201. doi: 10.1016/j.dci.2016.01.014 26828391
112. Sfacteria A, Brines M, Blank U. The mast cell plays a central role in the immune system of teleost fish. Mol. Immunol. 2014: 63: 3–8. doi: 10.1016/j.molimm.2014.02.007
113. Bielek E. Membrane Transformations in Degenerating Rodlet Cells in Fishes of Two Teleostean Families (Salmonidae, Cyprinidae). Anat. Rec. 2008; 291:163–1706.
Článek vyšel v časopise
PLOS One
2019 Číslo 9
- Proč jsou nemocnice nepřítelem spánku? A jak to změnit?
- Dlouhodobá ketodieta může poškozovat naše orgány
- Není statin jako statin aneb praktický přehled rozdílů jednotlivých molekul
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Tisícileté topoly, mokří psi, stárnoucí kočky a ospalé octomilky – „jednohubky“ z výzkumu 2024/41