Environmental Science and Pollution Research

, Volume 25, Issue 34, pp 34200–34211 | Cite as

Dietary propionic acid enhances antibacterial and immunomodulatory effects of oxytetracycline on Nile tilapia, Oreochromis niloticus

  • Mohammed El-AdawyEmail author
  • Magdy Abd El-Aziz
  • Kamal El-Shazly
  • Nadia G. Ali
  • Mohammed Abu El-MagdEmail author
Research Article


This study was carried out to evaluate the potential antibacterial and immunomodulatory effects of the dietary acidifier propionic acid (PA) when given alone or in combination with oxytetracycline (OTC) on Nile tilapia (Oreochromis niloticus). Apparently healthy O. niloticus (n = 240; 52 ± 3.75 g) were randomly allocated into four equal groups (n = 60/group): control group fed a basal diet alone and the other three groups fed basal diets supplemented with either PA (200 mg /kg of diet, PA group) or OTC (500 mg/kg of diet, OTC group) alone or in combination (PA + OTC group). Each group was subdivided into two subgroups (n = 30/subgroup, each subgroup had triplicate of 10 fish); subgroup (A) was used to evaluate the antibacterial effects with the aforementioned 2 weeks feeding regime, and subgroup (B) was used to evaluate the immunomodulatory effects against Aeromonas hydrophila infection with similar 2 weeks feeding regime. Among the four groups, PA + OTC group showed the highest significant (p < 0.0001) antibacterial activity as indicated by widest inhibition zones against A. hydrophila and lowest total gastrointestinal bacterial counts. Additionally, this group had the best immunomodulatory effect as noticed by a significant (p < 0.05) increase in total serum protein, globulin, IgM, phagocytic activity and index, lysosome activity, and significant (p < 0.05) upregulation in the expression levels of immunity-related genes (MHC I, MHC IIA, MHC IIB, Tlr7, IgM heavy chain, TNFα, and IL1β) in head-kidney. Notably, the combined dietary PA and OTC improved the hematological parameters and reduced the oxidative damage of hepatopancreas and head-kidney induced by OTC. This data suggests dietary PA as potential adjuvant to OTC in O. niloticus diets to get maximal antibacterial and immunomodulatory effects.


Oreochromis niloticus Propionic acid Oxytetracycline Immunity 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abdelhadya DH, El-Magd MA, Elbialy ZI, Saleh AA 2017 Bromuconazole-induced hepatotoxicity is accompanied by upregulation of PXR/CYP3A1 and downregulation of CAR/CYP2B1 gene expression. Toxicol Mech Methods, 1-7Google Scholar
  2. Abo-Al-Ela HG, El-Nahas AF, Mahmoud S, Ibrahim EM (2017) Vitamin C modulates the Immunotoxic effect of 17alpha-Methyltestosterone in Nile Tilapia. Biochemistry 56:2042–2050CrossRefGoogle Scholar
  3. Al-Harbi AH, Naim Uddin M (2004) Seasonal variation in the intestinal bacterial flora of hybrid tilapia (Oreochromis niloticus×Oreochromis aureus) cultured in earthen ponds in Saudi Arabia. Aquaculture 229:37–44CrossRefGoogle Scholar
  4. Alday-Sanz V, Corsin F, Irde E, Bondad-Renantaso MG 2012 Survey of the use of veterinary medicines in aquaculture. In: Improving biosecurity through prudent and responsible use of veterinary medicine in aquatic food production (ed. by M.G. Bondad-Renantaso, J.R. Arthurs & R.P. Subasinghe), pp. 29–45. FAO fisheries and aquaculture technical paper 547, FAO, Rome, ItalyGoogle Scholar
  5. Anuta JD, Buentello A, Patnaik S, Lawrence AL, Mustafa A, Hume ME, Gatlin DM, Kemp MC (2011) Effect of dietary supplementation of acidic calcium sulfate (Vitoxal) on growth, survival, immune response and gut microbiota of the Pacific white shrimp, Litopenaeus vannamei. J World Aquacult Soc 42:834–844CrossRefGoogle Scholar
  6. Baruah K, Sahu NP, Pal AK, Jain KK, Debnath D, Mukherjee SC (2007) Dietary microbial phytase and citric acid synergistically enhances nutrient digestibility and growth performance of Labeo rohita (Hamilton) juveniles at sub-optimal protein level. Aquac Res 38:109–120Google Scholar
  7. Croisetiere S, Tarte PD, Bernatchez L, Belhumeur P (2008) Identification of MHC class IIbeta resistance/susceptibility alleles to Aeromonas salmonicida in brook charr (Salvelinus fontinalis). Mol Immunol 45:3107–3116CrossRefGoogle Scholar
  8. da Silva BC, Vieira FdN, Mouriño JLP, Ferreira GS, Seiffert WQ (2013) Salts of organic acids selection by multiple characteristics for marine shrimp nutrition. Aquaculture 384-387:104–110CrossRefGoogle Scholar
  9. Defoirdt T, Boon N, Sorgeloos P, Verstraete W, Bossier P (2009) Short-chain fatty acids and poly-β-hydroxyalkanoates: (new) biocontrol agents for a sustainable animal production. Biotechnol Adv 27:680–685CrossRefGoogle Scholar
  10. Defoirdt T, Halet D, Sorgeloos P, Bossier P, Verstraete W (2006) Short-chain fatty acids protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii. Aquaculture 261:804–808CrossRefGoogle Scholar
  11. El-Hady MA, Ahmed HA (2014) Multiplex PCR for rapid detection of infectious bacterial fish diseases with special reference to Aeromonas hydrophila and Yersinia ruckeri in Egypt. Anim Health Res J 2:284–290Google Scholar
  12. El-Magd MA, Kahilo KA, Nasr NE, Kamal T, Shukry M, Saleh AA 2016a A potential mechanism associated with lead-induced testicular toxicity in rats. Andrologia 49 CrossRefGoogle Scholar
  13. El-Magd MA, Saleh AA, Abdel-Hamid TM, Saleh RM, Afifi MA (2016b) Is really endogenous ghrelin a hunger signal in chickens?: association of GHSR SNPs with increase appetite, growth traits, expression and serum level of GHRL, and GH. Gen Comp Endocrinol 237:131–139CrossRefGoogle Scholar
  14. Fujiki K, Matsuyama H, Yano T (1994) Protective effect of sodium alginates against bacterial infection in common carp, Cyprinus carpio L. J Fish Dis 17:349–355CrossRefGoogle Scholar
  15. Gupta MV, Acosta BO (2004) A review of global tilapia farming practices. Aquaculture Asia Magazine 10:7–12Google Scholar
  16. Haque M, Chowdhury R, Islam K, Akbar M (2012) Propionic acid is an alternative to antibiotics in poultry diet. Bangladesh J Anim Sci 38:8CrossRefGoogle Scholar
  17. Hofmann MJ, Bracamonte SE, Eizaguirre C, Barluenga M (2017) Molecular characterization of MHC class IIB genes of sympatric Neotropical cichlids. BMC Genet 18:15CrossRefGoogle Scholar
  18. Kesarcodi-Watson A, Kaspar H, Lategan MJ, Gibson L (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274:1–14CrossRefGoogle Scholar
  19. Khajepour F, Hosseini SA (2012) Citric acid improves growth performance and phosphorus digestibility in Beluga (Huso huso) fed diets where soybean meal partly replaced fish meal. Anim Feed Sci Technol 171:68–73CrossRefGoogle Scholar
  20. Kumar H, Kawai T, Akira S (2011) Pathogen recognition by the innate immune system. Int Rev Immunol 30:16–34CrossRefGoogle Scholar
  21. Kwon YM, Ricke SC (1998) Induction of acid resistance of Salmonella typhimurium by exposure to short-chain fatty acids. Appl Environ Microbiol 64:3458–3463Google Scholar
  22. Lim C, Klesius PH, Lückstädt C (2010) Effects of dietary levels of potassium diformate on growth, feed utilization and resistance to Streptococcus iniae of Nile tilapia, Oreochromis niloticus. In: Abstract in proceedings of the 14th international symposium on fish nutrition and feeding. Qingdao, ChinaGoogle Scholar
  23. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408CrossRefGoogle Scholar
  24. Luthman J, Jacobsson SO (1985) The effect of citric acid on the availability of tetracyclines in calves. Nordisk Veterinaermedicin 37:22–26Google Scholar
  25. Ng W-K, Koh C-B (2017) The utilization and mode of action of organic acids in the feeds of cultured aquatic animals. Rev Aquac 9:342–368CrossRefGoogle Scholar
  26. Ng W-K, Koh C-B, Sudesh K, Siti-Zahrah A (2009) Effects of dietary organic acids on growth, nutrient digestibility and gut microflora of red hybrid tilapia, Oreochromis sp., and subsequent survival during a challenge test with Streptococcus agalactiae. Aquac Res 40:1490–1500CrossRefGoogle Scholar
  27. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity (Edinb) 96:7–21CrossRefGoogle Scholar
  28. Reda RM, Ibrahim RE, Ahmed E-NG, El-Bouhy ZM (2013) Effect of oxytetracycline and florfenicol as growth promoters on the health status of cultured Oreochromis niloticus. Egypt J Aqua Res 39:241–248CrossRefGoogle Scholar
  29. Reda RM, Mahmoud R, Selim KM, El-Araby IE (2016) Effects of dietary acidifiers on growth, hematology, immune response and disease resistance of Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol 50:255–262CrossRefGoogle Scholar
  30. Saleh AA, El-Magd MA (2018) Beneficial effects of dietary silver nanoparticles and silver nitrate on broiler nutrition. Environ Sci Pollut Res 25:27031–27038. CrossRefGoogle Scholar
  31. Sharawy ZZ, Thiele R, Abbas EM, El-Magd MA, Hassaan MS, Peter C, Schmidt J, Saborowski R, Goda AMA-S, Slater MJ (2017) Antioxidant response, body composition of whiteleg shrimp Litopenaeus vannamei co-cultured with Nile tilapia Oreochromis niloticus in recirculating aquaculture. Aquacult Environ Interactions 9:257–268CrossRefGoogle Scholar
  32. Surya KS, Basanta KD, Bibhuti BP (2014) Isolation, biochemical characterization, antibiotic susceptibility study of Aeromonas hydrophila isolated from freshwater fish. Int J Curr Microbiol App Sci 3:259–267Google Scholar
  33. Tafalla C, Novoa B, Alvarez JM, Figueras A (1999) In vivo and in vitro effect of oxytetracycline treatment on the immune response of turbot, Scophthalmus maximus (L.). J Fish Dis 22:271–276CrossRefGoogle Scholar
  34. Tanekhy M, Khalil R, Hofi H, Hashish E (2016) The biochemical, pathological and immunological effectiveness of commercial probiotics in Nile tilapia Oreochromis niloticus. Pakistan J Zool 48:1269–1282Google Scholar
  35. Trushenski JT, Aardsma MP, Barry KJ, Bowker JD, Jackson CJ, Jakaitis M, McClure RL, Rombenso AN (2018) Oxytetracycline does not cause growth promotion in finfish. J Anim Sci 96:1667–1677CrossRefGoogle Scholar
  36. Wang JP, Lee JH, Yoo JS, Cho JH, Kim HJ, Kim IH (2010) Effects of phenyllactic acid on growth performance, intestinal microbiota, relative organ weight, blood characteristics, and meat quality of broiler chicks. Poult Sci 89:1549–1555CrossRefGoogle Scholar
  37. Wanner M, Walker W, Sutter HM, Riond JL, Broz J (1991) Influence of dietary citric acid and calcium on the bioavailability of orally administered chlortetracycline in piglets. J Veterinary Med Ser A 38:755–762CrossRefGoogle Scholar
  38. Wyatt RD, Miller BL (1985) Effect of mixed organic acid administration on blood levels of chlortetracycline in broiler chicks. Poult Sci 64:59–64CrossRefGoogle Scholar
  39. Yin Z, Lam TJ, Sin YM (1997) Cytokine-mediated antimicrobial immune response of catfish,Clarias gariepinus, as a defence against Aeromonas hydrophila. Fish & Shellfish Immunol 7:93–104CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Pharmacology, Faculty of Veterinary MedicineKafrelsheikh UniversityKafr ElsheikhEgypt
  2. 2.Fish Disease LabNational Institute of Oceanography and Fishery (NIOF)CairoEgypt
  3. 3.Department of Anatomy, Faculty of Veterinary MedicineKafrelsheikh UniversityKafr ElsheikhEgypt

Personalised recommendations