Skip to main content

Advertisement

SpringerLink
Log in

Immunohematological status under acute ammonia stress of juvenile rainbow trout (Oncorhynchus mykiss Walbaum, 1792) fed garlic (Allium sativum) powder-supplemented meat and bone meal-based feeds

  • Original Article
  • Published:
Comparative Clinical Pathology Aims and scope Submit manuscript

Abstract

A feeding trial was conducted for 60 days to determine the effects of fish meal (FM) replacement with meat and bone meal (MBM) supplemented with garlic powder on the physiological and immunohematological status of juvenile rainbow trout (Oncorhynchus mykiss; 8.26 ± 1.10 g). Eight isonitrogenous (46% crude protein) and isoenergetic (22 mJ kg−1) diets were formulated containing increasing levels of MBM 0 (control), 25, 45, and 65% with or without garlic powder (3%). Our findings indicated that garlic supplementation increased red blood cell (RBC), hemoglobin (Hb), hematocrit (Ht), white blood cell (WBC), lysozyme, ACH50, and plasma protein, whereas decreased cholesterol, urea, glutamic oxaloacetic transaminase (GOT), glutamic pyruvic transaminase (GPT), and creatinine. The increase in dietary MBM without garlic supplementation resulted in elevated levels of urea, creatinine, GOT, and GPT, and reduced lysozyme, ACH50, Hb, and WBC. At the end of the feeding trial, 24-h exposure to un-ionized ammonia at 1 mg l−1 resulted in increase in cortisol and glucose, and decrease in Hb and Ht in treatments without supply of garlic. Fish fed feeds with garlic supplementation, regardless of inclusion levels of MBM, exhibited reduced plasma cortisol and glucose levels and increased survival rates under ammonia exposure conditions. In summary, dietary garlic supplementation positively influenced the immune status of rainbow trout, in particular under ammonia stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adamu KM, Kori-Siakpere O (2011) Effects of sublethal concentrations of tobacco (Nicotiana tobaccum) leaf dust on some biochemical parameters of Hybrid catfish (Clarias gariepinus and Heterobranchus bidorsalis). Braz Arch Biol Technol 54:183–196

    Article  Google Scholar 

  • Agrahari S, Pandey KC, Gopal K (2007) Biochemical alteration induced by monocrotophos in the blood plasma of fish, Channa punctatus (Bloch). Pestic Biochem Physiol 88:268–272

    Article  CAS  Google Scholar 

  • Ahmed R, Sharma S (1997) Biochemical studies on combined effects of garlic (Allium sativum Linn) and ginger (Zingiber officinale Rosc) in albino rats. Indian J Exp Biol 35:841–843

    CAS  PubMed  Google Scholar 

  • Aksnes A, Opstvedt J (1998) Content of digestible energy in fish feed ingredients determined by the ingredient-substitution method. Aquaculture 161:45–53

    Article  CAS  Google Scholar 

  • Anwar K (2003) Cypermethrin, a pyrethroid insecticide induces teratological and biochemical changes in young chick embryos. Pak J Biol Sci 6:1698–1705

    Article  Google Scholar 

  • Association of Official Analytical Chemists (AOAC) (1995) Official method of analysis, 16th edn. Association of Official Analytical Chemists, Arlington

    Google Scholar 

  • Banaee M, Sureda A, Mirvaghefi A, Ahmadi K (2011) Effects of diazinon on biochemical parameters of blood in rainbow trout (Oncorhynchus mykiss). Pestic Biochem Physiol 99:1–6

    Article  CAS  Google Scholar 

  • Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26

    Article  Google Scholar 

  • Barton BA, Morgan JD, Vijayan MM (2002) Physiological and condition-related indicators of environmental stress on fish. In: Adams SM (ed) Biological indicators of aquatic ecosystems stress. American Fisheries Society, Bethesda, pp 111–148

    Google Scholar 

  • Bernet D, Schmidt H, Wahli T, Burkhardt-Holm P (2001) Effluent from a sewage treatment works causes changes in serum chemistry of brown trout (Salmo trutta L.) Ecotoxicol Environ Saf 48:140–147

    Article  CAS  PubMed  Google Scholar 

  • Blaxhall PC (1972) The haematological assessment of the health of freshwater fish. J Fish Biol 4:593–604

    Article  CAS  Google Scholar 

  • Borek C (2001) Antioxidant health effects of aged garlic extract. J Nutr 131:1010S–1015S

    Article  CAS  PubMed  Google Scholar 

  • Bureau DP, Harris AM, Bevan DJ, Simmons LA, Azevedo PA, Cho CY (2000) Feather meals and meat and bone meals from different origins as protein sources in rainbow trout (Oncorhynchus mykiss) diets. Aquaculture 181(3–4):281–291

    Article  Google Scholar 

  • Burrells C, Williams P, Southgate P, Crampton V (1999) Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentrations of soybean proteins. Vet Immunol Immunop. 72:277–288

    Article  CAS  Google Scholar 

  • Chang MLW, Johnson MA (1980) Effect of garlic on carbohydrate metabolism and lipid synthesis in rats. J Nutr 110:931–936

    Article  CAS  PubMed  Google Scholar 

  • Cho SH, Lee SM (2012) Onion powder in the diet of the olive flounder, Paralichthys olivaceus: effects on the growth, body composition, and lysozyme activity. J World Aquacult Soc 43:30–38

    Article  Google Scholar 

  • Ciji A, Sahu N, Pal A, Dasgupta S, Akhtar M (2012) Alterations in serum electrolytes, antioxidative enzymes and haematological parameters of Labeo rohita on short-term exposure to sublethal dose of nitrite. Fish Physiol Biochem 38:1355–1365

    Article  CAS  PubMed  Google Scholar 

  • Cowey C (1992) Nutrition: estimating requirements of rainbow trout. Aquaculture 100:177–189

    Article  Google Scholar 

  • Das BK, Mukherjee SC (2003) Toxicity of cypermethrin in Labeo rohita fingerlings: biochemical, enzymatic and haematological consequences. Comp Biochem Physiol C 134:109–121

    Google Scholar 

  • Das P, Ayyappan S, Das B, Jena J (2004a) Nitrite toxicity in Indian major carps: sublethal effect on selected enzymes in fingerlings of Catla catla, Labeo rohita and Cirrhinus mrigala. Comp Biochem Physiol C 138:3–10

    CAS  Google Scholar 

  • Das PC, Ayyappan S, Jena J, Das B (2004b) Acute toxicity of ammonia and its sub-lethal effects on selected haematological and enzymatic parameters of mrigal, Cirrhinus mrigala (Hamilton). Aquac Res 35:134–143

    Article  CAS  Google Scholar 

  • Dederen L, Leuven R, Wendelaar S, Oyen F (1986) Biology of the acid-tolerant fish species Umbra pygmaea (De Kay, 1842). J Fish Biol 28:307–326

    Article  Google Scholar 

  • Dogan D, Can C (2011) Hematological, biochemical, and behavioral responses of Oncorhynchus mykiss to dimethoate. Fish Physiol Biochem 37:951–958

    Article  CAS  PubMed  Google Scholar 

  • Dorafshan S, Kalbassi MR, Pourkazemi M, Amiri BM, Karimi SS (2008) Effects of triploidy on the Caspian salmon Salmo trutta caspius haematology. Fish Physiol Biochem 34:195–200

    Article  CAS  PubMed  Google Scholar 

  • Efendy JL, Simmons DL, Campbell GR, Campbell JH (1997) The effect of the aged garlic extract, ‘Kyolic’, on the development of experimental atherosclerosis. Atherosclerosis 132:37–42

    Article  CAS  PubMed  Google Scholar 

  • Ellis A, Hastings T, Munro A (1981) The role of Aeromonas salmonicida extracellular products in the pathology of furunculosis. J Fish Dis 4:41–51

    Article  Google Scholar 

  • Esmaeili N, Abedian kenari A, Rombenso A (2017) Effects of fish meal replacement with meat and bone meal using garlic (Allium sativum) powder on growth, feeding, digestive enzymes and apparent digestibility of nutrients and fatty acids in rainbow trout (Oncorhynchus mykiss Walbaum, 1792). Aquac Nutr 2017(00):1–10

    Google Scholar 

  • Fabbri E, Capuzzo A, Moon TW (1998) The role of circulating catecholamines in the regulation of fish metabolism: an overview. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 120:177–192

    Article  CAS  PubMed  Google Scholar 

  • Farahi A, Kasiri M, Sudagar M, Iraei MS, Shahkolaei MD (2010) Effect of garlic (Allium sativum) on growth factors, some hematological parameters and body compositions in rainbow trout (Oncorhynchus mykiss). AACL Bioflux 3(4):317–323

    Google Scholar 

  • Fazllolahzadeh F, Keramati K, Nazifi S, Shirian S, Seifi S (2011) Effect of garlic (Allium sativum) on hematological parameters and plasma activities of ALT and AST of rainbow trout in temperature stress. Aust J Basic Appl Sci 5(9):84–90

    Google Scholar 

  • Friedrich M, Stepanowska K (2001) Effect of starvation on nutritive value of carp (Cyprinus carpio L.) and selected biochemical components of its blood. Acta Ichthyol Piscat 31:29–36

  • Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl Å, Nelson R (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38:551–579

    Article  CAS  Google Scholar 

  • Gilbert SC, Emmett M, Menter A, Silverman A, Klintmalm G (1989) Cyclosporine therapy for psoriasis: serum creatinine measurements are an unreliable predictor of decreased renal function. J Am Acad Dermatol 21:470–474

    Article  CAS  PubMed  Google Scholar 

  • Glässer G, Graefe E, Struck F, Veit M, Gebhardt R (2002) Comparison of antioxidative capacities and inhibitory effects on cholesterol biosynthesis of quercetin and potential metabolites. Phytomedicine 9:33–40

    Article  PubMed  Google Scholar 

  • Guo J, Kuo C, Chuang Y, Hong J, Chou R, Chen T (2012) The effects of garlic-supplemented diets on antibacterial activity against Streptococcus iniae and on growth in orange-spotted grouper, Epinephelus coioides. Aquaculture 364:33–38

    Article  Google Scholar 

  • Guo J, Kuo CM, Hong JW, Chou RL, Lee YH, Chen TI (2015) The effects of garlic-supplemented diets on antibacterial activities against Photobacterium damselae subsp. piscicida and Streptococcus iniae and on growth in Cobia, Rachycentron canadum. Aquaculture 435:111–115

    Article  CAS  Google Scholar 

  • Heming TA, Paleczny EJ (1987) Compositional changes in skin mucus and blood serum during starvation of trout. Aquaculture 66:265–273

    Article  CAS  Google Scholar 

  • Hemre GI, Sanden M, Bakke-Mckellep A, Sagstad A, Krogdahl Å (2005) Growth, feed utilization and health of Atlantic salmon Salmo salar L. fed genetically modified compared to non-modified commercial hybrid soybeans. Aquac Nutr 11:157–167

    Article  CAS  Google Scholar 

  • Hopkins TE, Cech JJ Jr (1992) Physiological effects of capturing striped bass in gill nets and fyke traps. T Am Fish Soc 121:819–822

    Article  Google Scholar 

  • Hrubec TC, Robertson JL, Smith SA, Tinker MK (1996) The effect of temperature and water quality on antibody response to Aeromonas salmonicida in sunshine bass (Morone chrysops × Morone saxatilis). Vet Immunol Immunopathol 50:157–166

    Article  CAS  PubMed  Google Scholar 

  • Israeli-Weinstein D, Kimmel E (1998) Behavioral response of carp (Cyprinus carpio) to ammonia stress. Aquaculture 165:81–93

    Article  CAS  Google Scholar 

  • Jee JH, Masroor F, Kang JC (2005) Responses of cypermethrin-induced stress in haematological parameters of Korean rockfish, Sebastes schlegeli. Aquac Res 36:898–905

    Article  Google Scholar 

  • Jeong HG, Lee YW (1998) Protective effects of diallyl sulfide on N-nitrosodimethylamine-induced immunosuppression in mice. Cancer Lett 134:73–79

    Article  CAS  PubMed  Google Scholar 

  • Jeyapriya S, Venkatesh P, Suresh N (2013) Acute and subchronic effect of monocrotophos on haematological indices in Catla catla (Hamilton). Int J Pure Appl Zool 1(3):235–240

    Google Scholar 

  • Jha AK, Pal A, Sahu N, Kumar S, Mukherjee S (2007) Haemato-immunological responses to dietary yeast RNA, ω-3 fatty acid and β-carotene in(Catla catla) juveniles. Fish Shellfish Immunol. 23:917–927

    Article  CAS  PubMed  Google Scholar 

  • Ji SC, Jeong GS, Im GS, Lee SW, Yoo JH, Takii K (2007) Dietary medicinal herbs improve growth performance, fatty acid utilization, and stress recovery of Japanese flounder. Fisheries Sci. 73:70–76

    Article  CAS  Google Scholar 

  • Kikuchi K (1999) Use of defatted soybean meal as a substitute for fish meal in diets of Japanese flounder (Paralichthys olivaceus). Aquaculture 179:3–11

    Article  Google Scholar 

  • Kim S-H, Kim J-H, Park M-A, Hwang SD, Kang J-C (2015) The toxic effects of ammonia exposure on antioxidant and immune responses in Rockfish, Sebastes schlegelii during thermal stress. Environ Toxicol Phar 40:954–959

    Article  CAS  Google Scholar 

  • Kiron V, Puangkaew J, Ishizaka K, Satoh S, Watanabe T (2004) Antioxidant status and nonspecific immune responses in rainbow trout (Oncorhynchus mykiss) fed two levels of vitamin E along with three lipid sources. Aquaculture 234:361–379

    Article  CAS  Google Scholar 

  • Köprücü SŞ, Köprücü K, Ural MŞ, İspir Ü, Pala M (2006) Acute toxicity of organophosphorous pesticide diazinon and its effects on behavior and some hematological parameters of fingerling European catfish (Silurus glanis L.) Pestic Biochem Physiol 86:99–105

    Article  Google Scholar 

  • Kris-Etherton PM, Harris WS, Appel LJ (2002) Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106:2747–2757

    Article  PubMed  Google Scholar 

  • Kumar V, Makkar HP, Amselgruber W, Becker K (2010) Physiological, haematological and histopathological responses in common carp (Cyprinus carpio L.) fingerlings fed with differently detoxified Jatropha curcas kernel meal. Food Chem Toxicology 48:2063–2072

    Article  CAS  Google Scholar 

  • Kumar V, Makkar H, Becker K (2011) Nutritional, physiological and haematological responses in rainbow trout (Oncorhynchus mykiss) juveniles fed detoxified Jatropha curcas kernel meal. Aquac Nutr 17:451–467

    Article  CAS  Google Scholar 

  • Lall S (2000) Nutrition and health of fish. In: Cruz-Suárez L, Ricque-Marie D, Tapia- Salazar M, Olvera-Novoa M, Civera-Cerecedo R (eds) Avances en Nutricio’n Acuı’cola V. Memorias del V Simposium Internacional de Nutricio’n Acuı’cola. Me´ rida, Yucata’n, Mexico, p 13–23. 19–22 November 2000

  • Larsson Å, Haux C, Sjöbeck M-L (1985) Fish physiology and metal pollution: results and experiences from laboratory and field studies. Ecotox Environ Saft 9:250–281

    Article  CAS  Google Scholar 

  • Li M, Yu N, Qin JG, Li E, Du Z, Chen L (2014) Effects of ammonia stress, dietary linseed oil and Edwardsiella ictaluri challenge on juvenile darkbarbel catfish Pelteobagrus vachelli. Fish shellfish immunol. 38:158–165

    Article  CAS  PubMed  Google Scholar 

  • Lin H, Chen X, Chen S, Zhuojia L, Huang Z, Niu J, Wu K, Lu X (2012) Replacement of fish meal with fermented soybean meal in practical diets for pompano (Trachinotus ovatus). Aquac Res 44:151–156

    Article  CAS  Google Scholar 

  • Liu L, Yeh Y-Y (2002) S-alk(en)yl cysteines of garlic inhibit cholesterol synthesis by deactivating HMG-CoA reductase in cultured rat hepatocytes. J Nutr 132:1129–1134

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Xie S, Zhu X, Lei W, Han D, Yang Y (2008) Effects of dietary ascorbic acid supplementation on the growth performance, immune and stress response in juvenile Leiocassis longirostris Günther exposed to ammonia. Aquac Res 39:1628–1638

    Google Scholar 

  • Lu F, Haga Y, Satoh S (2015) Effects of replacing fish meal with rendered animal protein and plant protein sources on growth response, biological indices, and amino acid availability for rainbow trout (Oncorhynchus mykiss). Fisheries Sci 81:95–105

    Article  CAS  Google Scholar 

  • Modesto KA, Martinez CB (2010) Effects of Roundup Transorb on fish: hematology, antioxidant defenses and acetylcholinesterase activity. Chemosphere 81:781–787

    Article  CAS  PubMed  Google Scholar 

  • Mohebbi A, Nematollahi A, Dorcheh EE, Asad FG (2012) Influence of dietary garlic (Allium sativum) on the antioxidative status of rainbow trout (Oncorhynchus mykiss). Aquac Res 43:1184–1193

    Article  CAS  Google Scholar 

  • Montero D, Mathlouthi F, Tort L, Afonso J, Torrecillas S, Fernandez-Vaquero A, Negrin D, Izquierdo M (2010) Replacement of dietary fish oil by vegetable oils affects humoral immunity and expression of pro-inflammatory cytokines genes in gilthead sea bream Sparus aurata. Fish Shellfish Immunol 29:1073–1081

    Article  CAS  PubMed  Google Scholar 

  • Nobahar Z, Gholipour-Kanani H, Kakoolaki S, Jafaryan H (2014) Effect of garlic (Allium sativum) and nettle (Urtica dioica) on growth performance and hematological parameters of beluga (Huso huso). Iran J Aquat Anim Health 1(1):63–69

    Google Scholar 

  • NRC (National Research Council) (1993) Nutrient requirements of warmwater fishes and shellfishes, revised edn. National Academy Press, Washington, p 225

    Google Scholar 

  • Nya EJ, Dawood Z, Austin B (2010) The garlic component, allicin, prevents disease caused by Aeromonas hydrophila in rainbow trout, Oncorhynchus mykiss. J Fish Dis 33:293–300

    Article  CAS  PubMed  Google Scholar 

  • Olsen RE, Hansen A-C, Rosenlund G, Hemre G-I, Mayhew TM, Knudsen DL, Eroldoğan OT, Myklebust R, Karlsen Ø (2007) Total replacement of fish meal with plant proteins in diets for Atlantic cod (Gadus morhua L.) II—health aspects. Aquaculture 272:612–624

    Article  CAS  Google Scholar 

  • Ortuno J, Esteban M, Meseguer J (2000) High dietary intake of α-tocopherol acetate enhances the non-specific immune response of gilthead seabream (Sparus aurata L.) Fish Shellfish Immunol. 10:293–307

    Article  CAS  PubMed  Google Scholar 

  • Pan C, Chien Y, Wang Y (2011) Antioxidant defence to ammonia stress of characins (Hyphessobrycon eques Steindachner) fed diets supplemented with carotenoids. Aquac Nutr 17:258–266

    Article  CAS  Google Scholar 

  • Perrier H, Perrier C, Gudefin Y, Gras J (1972) Adrenaline-induced hypercholesterolemia in the rainbow trout (Salmo gairdnerii Richardson): a separate study in male and female trout and the effect of adrenergic blocking agents. Comp Biochem Physiol A 43:341–347

  • Rao YV, Das B, Jyotyrmayee P, Chakrabarti R (2006) Effect of Achyranthes aspera on the immunity and survival of Labeo rohita infected with Aeromonas hydrophila. Fish Shellfish Immunol 20:263–273

    Article  Google Scholar 

  • Rawles S, Thompson K, Brady Y, Metts L, Aksoy M, Gannam A, Twibell R, Ostrand S, Webster C (2011) Effects of replacing fish meal with poultry by-product meal and soybean meal and reduced protein level on the performance and immune status of pond-grown sunshine bass (Morone chrysops× M. saxatilis). Aquac Nutr 17:708–721

    Article  Google Scholar 

  • Reddy A, Ayyanna K, Yellamma K (1991) Cypermethrin induced modulations in lipid metabolism of freshwater teleost, Tilapia mossambica. Biochem Int 23:963–967

    CAS  PubMed  Google Scholar 

  • Řehulka J (2000) Influence of astaxanthin on growth rate, condition, and some blood indices of rainbow trout, Oncorhynchus mykiss. Aquaculture 190:27–47

    Article  Google Scholar 

  • Sahu S, Das B, Mishra B, Pradhan J, Sarangi N (2007) Effect of Allium sativum on the immunity and survival of Labeo rohita infected with Aeromonas hydrophila. J Appl Ichthyol 23:80–86

    Article  CAS  Google Scholar 

  • Saurabh S, Sahoo P (2008) Lysozyme: an important defence molecule of fish innate immune system. Aquac Res 39:223–239

    Article  CAS  Google Scholar 

  • Selye H (1950) Stress and the general adaptation syndrome. Brit Med J 1:1383–1392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shalaby A, Khattab Y, Abdel Rahman A (2006) Effects of garlic (Allium sativum) and chloramphenicol on growth performance, physiological parameters and survival of Nile tilapia (Oreochromis niloticus). J Venom Anim Toxins 12:172–201

    Google Scholar 

  • Sheela C, Augusti K (1992) Antidiabetic effects of S-allyl cysteine sulphoxide isolated from garlic (Allium sativum). Indian J Exp Biol 30:523–526

    CAS  PubMed  Google Scholar 

  • Shimeno S, Takeda M, Takayama S, Fukui A, Sasaki H, Kajiyama H (1981) Adaptation of hepatopancreatic enzymes to dietary carbohydrate in carp. Bull Jpn Soc Sci Fish 47:71–77

    Article  CAS  Google Scholar 

  • Small BC (2004) Effect of isoeugenol sedation on plasma cortisol, glucose, and lactate dynamics in channel catfish Ictalurus punctatus exposed to three stressors. Aquaculture 238:469–481

    Article  CAS  Google Scholar 

  • Subhadra B, Lochmann R, Rawles S, Chen R (2006) Effect of fish-meal replacement with poultry by-product meal on the growth, tissue composition and hematological parameters of largemouth bass (Micropterus salmoides) fed diets containing different lipids. Aquaculture 260:221–231

    Article  CAS  Google Scholar 

  • Sunyer JO, Tort L (1995) Natural hemolytic and bactericidal activities of sea bream (Sparus aurata) serum are effected by the alternative complement pathway. Vet Immunol Immunop 45:333–345

    Article  CAS  Google Scholar 

  • Svobodova Z, Luskova V, Drastichova J, Svoboda M, Žlábek V (2003) Effect of deltamethrin on haematological indices of common carp (Cyprinus carpio L.) Acta Vet Brno 72:79–85

    Article  CAS  Google Scholar 

  • Talpur AD, Ikhwanuddin M (2012) 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 364:6–12

    Article  Google Scholar 

  • Thurston RV, Russo RC (1983) Acute toxicity of ammonia to rainbow trout. T AM FISH SOC 112:696–704

    Article  CAS  Google Scholar 

  • Tietz NW, Andresen BD (1986) Textbook of clinical chemistry. Saunders, Philadelphia

    Google Scholar 

  • Timmons MB, Ebeling JM (2010) Recirculating Aquaculture, 2nd edn. Northeastern Regional Aquaculture Center, Ithaca 948 pp

    Google Scholar 

  • Tiwari S, Singh A (2003) Metabolic changes in the snake head fish (Channa punctatus) due to latices of Euphorbia royleana. Asian Fish Sci 16:147–156

    Google Scholar 

  • Toffaletti JG, McDonnell EH (2008) Variation of serum creatinine, cystatin C, and creatinine clearance tests in persons with normal renal function. Clin Chim Acta 395:115–119

    Article  CAS  PubMed  Google Scholar 

  • Tukmechi A, Andani HRR, Manaffar R, Sheikhzadeh N (2011) Dietary administration of beta-mercapto-ethanol treated Saccharomyces cerevisiae enhanced the growth, innate immune response and disease resistance of the rainbow trout, Oncorhynchus mykiss. Fish shellfish immunol. 30:923–928

    Article  CAS  PubMed  Google Scholar 

  • Watanabe T, Verakunpiriya V, Watanabe K, KIRON V, SATOH S (1997) Feeding of rainbow trout with non-fish meal diets. Fisheries sci 63:258–266

    Article  CAS  Google Scholar 

  • Wepener V, Van Vuren J, Du Preez H (1992) The effect of hexavalent chromium at different pH values on the haematology of Tilapia sparrmanii (Cichlidae). Comp Biochem Physiol C 101:375–381

    Article  CAS  PubMed  Google Scholar 

  • Williams KC, Barlow CG, Rodgers LJ, Ruscoe I (2003) Potential of meat meal to replace fish meal in extruded dry diets for barramundi, Lates calcarifer (Bloch). I. Growth performance. Aquac Res 34:23–32

    Article  CAS  Google Scholar 

  • Yang J-L, Chen H-C (2003) Effects of gallium on common carp (Cyprinus carpio): acute test, serum biochemistry, and erythrocyte morphology. Chemosphere 53:877–882

    Article  CAS  PubMed  Google Scholar 

  • Yeh S-P, Chang C-A, Chang C-Y, Liu C-H, Cheng W (2008) Dietary sodium alginate administration affects fingerling growth and resistance to Streptococcus sp. and iridovirus, and juvenile non-specific immune responses of the orange-spotted grouper, Epinephelus coioides. Fish shellfish immunol 25:19–27

    Article  CAS  PubMed  Google Scholar 

  • Yeong KJ, Jin CY (1996) Effects of ammonia concentration on histological and physiological status in black seabream (Acanthopagrus schlegeli). Korean J Fish Aquat Sci 29:828–836

    Google Scholar 

  • Yılmaz S, Ergün S, Çelik EŞ (2014) Effect of dietary spice supplementations on welfare status of sea bass, Dicentrarchus labrax L.. Proc Natl Acad Sci, India Sect B 1–9

  • Yu M-C, Li Z-J, Lin H-Z, Wen G-L, Ma S (2008) Effects of dietary Bacillus and medicinal herbs on the growth, digestive enzyme activity, and serum biochemical parameters of the shrimp Litopenaeus vannamei. Aquacult Int 16:471–480

    Article  Google Scholar 

  • Zelisko PM, Brook MA (2002) Stabilization of α-chymotrypsin and lysozyme entrapped in water-in-silicone oil emulsions. Langmuir 18:8982–8987

    Article  CAS  Google Scholar 

  • Zhang X, Xie P, Li D, Shi Z (2007) Hematological and plasma biochemical responses of crucian carp (Carassius auratus) to intraperitoneal injection of extracted microcystins with the possible mechanisms of anemia. Toxicon 49:1150–1157

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Aquaculture, Faculty of Natural Resources and Marine Sciences, Tarbiat Modares University, PO Box 64414-356, Noor, Mazandaran, Iran

    Noah Esmaeili & Abdolmohamad Abedian Kenari

  2. Nutrition Laboratory, Institute of Oceanography, Autonomous University of Baja California, CP. 22860, Ensenada, Mexico

    Artur Rombenso

Authors
  1. Noah Esmaeili
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abdolmohamad Abedian Kenari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Artur Rombenso
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdolmohamad Abedian Kenari.

Ethics declarations

This study was founded by the Tarbiat Modares University (Noor, Iran).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable national and institutional guidelines for the care and use of rainbow trout were according to the Iran Veterinary Organization and also Tarbiat Modares University (The guidelines (adopted from the Declaration of Helsinki (1975) and The Society for Neuroscience Animal Care and Use guidelines (1998)) were approved for implementation by the Medical Ethics Committee, School of Medical Sciences of the Tarbiat Modares University on 28th Farvardin, 1385/17th April, 2006).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Esmaeili, N., Kenari, A.A. & Rombenso, A. Immunohematological status under acute ammonia stress of juvenile rainbow trout (Oncorhynchus mykiss Walbaum, 1792) fed garlic (Allium sativum) powder-supplemented meat and bone meal-based feeds. Comp Clin Pathol 26, 853–866 (2017). https://doi.org/10.1007/s00580-017-2457-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00580-017-2457-8

Keywords

Search

Navigation