• Irene Ortega Blázquez
  • Maria José Grande Burgos
  • Pilar Martínez Viedma
  • Julia Toledo del Árbol
  • Mari Carmen López Aguayo
  • Rubén Pérez Pulido
  • Rosario Lucas
  • Antonio Galvez University of Jaen, Department of Health Sciences
Keywords: antimicrobial resistance; seafood; high hydrostatic pressure; biopreservation


Seafoods may carry strains of bacterial pathogens resistant to clinically-used antibiotics. This review summarizes recent work on antimicrobial resistance from seafoods. Since ready-to-eat seafoods may also be at risk of transmitting antimicrobial resistance through the food chain, it is important to analyse how food processing methods may affect the bacterial populations in foods. Recent studies based on high-hydrostatic pressure applied on seafoods in combination with natural antimicrobials (bacteriocins and essential oils) indicate that the combined treatments achieve a greatest reduction of bacterial loads in the food. Nevertheless, application of high-throughput sequencing technology to study the dynamics of bacterial population surviving treatments reveals complex changes in bacterial populations during food storage. This makes necessary to further study the antimicrobial resistance in those strains surviving treatments and which may be consumed along with the processed food.


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Abriouel, H., Lucas, R., Omar, N. B., Valdivia, E., & Gálvez, A. Potential Applications of the Cyclic Peptide Enterocin AS-48 in the Preservation of Vegetable Foods and Beverages. Probiotics Antimicrob. Prot., 2, 2010, 77–89.
Ahmed, A. M., Maruyama, A., Khalifa, H. O., Shimamoto, T., & Tadashi, T. Seafood as a Reservoir of Gram-negative Bacteria Carrying Integrons and Antimicrobial Resistance Genes in Japan. Biomed. Environ. Sci., 28(12), 2015, 924-927.
Ananou, S., Zentar, H., Martínez-Bueno, M., Gálvez, A., Maqueda, M., & Valdivia, E. (2014). The impact of enterocin AS-48 on the shelf-life and safety of sardines (Sardina pilchardus) under different storage conditions. Food Microbiol., 44, 2014, 185–195.
Balasubramaniam, V. M., Martínez-Monteagudo, S. I., & Gupta, R. Principles and Application of High Pressure–Based Technologies in the Food Industry. Annu. Rev. Food Sci. T., 6, 2015, 435-462.
Baños, A., García-López, J. D., Núñez, C., Martínez-Bueno, M., Maqueda, M., & Valdivia, E. (2016). Biocontrol of Listeria monocytogenes in fish by enterocin AS-48 and Listeria lytic bacteriophage P100. LWT - Food Sci. Technol. 66, 2016, 672–677.
Boss, R., Overesch, G., & Baumgartner, A. Antimicrobial Resistance of Escherichia coli, Enterococci, Pseudomonas aeruginosa, and Staphylococcus aureus from Raw Fish and Seafood Imported into Switzerland. J. Food Prot., 79(7), 2016, 1240-1246.
Brillhart, C. D., & Joens, L. A. Prevalence and characterization of Salmonella serovars isolated from oysters served raw in restaurants. J. Food Prot., 74(6), 2011, 1025-1029.
Cabello, F. C., Godfrey, H. P., Buschmann, A. H., & Dölz, H. J. Aquaculture as yet another environmental gateway to the development and globalisation of antimicrobial resistance. Lancet Infect. Dis., 16, 2016, e127–e133.
Cebrián, R., Baños, A., Valdivia, E., Pérez-Pulido, R., Martínez-Bueno, M., & Maqueda, M. Characterization of functional, safety, and probiotic properties of Enterococcus faecalis UGRA10, a new AS-48-producer strain. Food Microbiol. 30, 2012, 59–67.
Changkaew, K., Utrarachkij, F., Siripanichgon, K., Nakajima, C., Suthienkul, O., & Suzuki, Y. Characterization of antibiotic resistance in Escherichia coli isolated from shrimps and their environment. J. Food Prot., 77(8), 2014, 1394-1401.
Çoban, Ö. E., Patir, B., & Yilmaz, O. Protective effect of essential oils on the shelf life of smoked and vacuum packed rainbow trout (Oncorhynchus mykiss W.1792) fillets. J. Food Sci. Technol., 51, 2014, 2741–2747.
Dong, X., Wang, X., Chen, X., Yan, Z., Cheng, J., Gao, L., Liu, Y., & Li, J. Genetic Diversity and Virulence Potential of Staphylococcus aureus Isolated from Crayfish (Procambarus clarkii). Curr. Microbiol., 74(1), 2017, 28-33.
Dubert, J., Osorio, C. R., Prado, S., & Barja, J. L. Persistence of Antibiotic Resistant Vibrio spp. in Shellfish Hatchery Environment. Microb. Ecol., 72(4), 2016, 851-860.
Elmahdi, S., DaSilva, L. V., & Parveen, S. Antibiotic resistance of Vibrio parahaemolyticus and Vibrio vulnificus in various countries: A review. Food Microbiol., 57, 2016, 128-134.
Erkan, N. The effect of thyme and garlic oil on the preservation of vacuum-packaged hot Smoked rainbow trout (Oncorhynchus mykiss). Food Bioprocess Technol., 5, 2012, 1246–1254.
Erkan, N., Tosun, S. Y., Ulusoy, S., & Üretener, G. The use of thyme and laurel essential oil treatments to extend the shelf life of bluefish (Pomatomus saltatrix) during storage in ice. J. Consum. Protec. Food Saf., 6, 2011, 39–48.
European Commission. (2017). Communication from the Commission to the Council and the European Parliament a European One Health Action Plan against Antimicrobial Resistance (AMR).
European Food Safety Authority (EFSA) and European Centre for Disease Prevention and Control (ECDC). The European Union Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2016. EFSA Journal, 16(2), 2018, 5182.
Elbashir, S., Parveen, S., Schwarz, J., Rippen, T., Jahncke, M., & DePaola, A. Seafood pathogens and information on antimicrobial resistance: A review. Food Microbiol., 70, 2018, 85-93.
Food and Agriculture Organization (FAO). (2016). GLOBEFISH Highlights-Issue 3/2016. FAO, Rome.
Food and Agriculture Organization (FAO). (2017). Antimicrobial resistance (AMR) in aquaculture. COFI:AQ/IX/2017/SBD.11. FAO, Rome
Galvez, A., Lucas, R., Pérez-Pulido, R., & Grande-Burgos, M. J. (2014). Food Biopreservation. New York: Springer.
Giatrakou, V., Kykkidou, S., Papavergou, A., Kontominas, M. G., & Savvaidis, I. N. Potential of oregano essential oil and MAP to extend the shelf life of fresh swordfish: a comparative study with ice storage. J. Food Sci., 73, 2008, 167–173.
Grande-Burgos, M. J., Pérez-Pulido, R., López-Aguayo, M. C., Gálvez, A., & Lucas, R. The cyclic antibacterial peptide enterocin AS-48: isolation, mode of action, and possible food applications. Int. J. Mol. Sci., 15, 2014, 22706–22727.
Grevskott, D. H., Svanevik, C. S., Sunde, M., Wester, A. L., & Lunestad, B. T. Marine Bivalve Mollusks As Possible Indicators of Multidrug-Resistant Escherichia coli and Other Species of the Enterobacteriaceae Family. Front Microbiol., 18, 2017, 8:24.
Gupta, S., Rajauria, G., & Abu-Ghannam, N. Study of the microbial diversity and antimicrobial properties of Irish edible brown seaweeds. Int. J. Food Sci. Technol., 45 2010, 482-489.
Hammad, A. M., Shimamoto, T., & Shimamoto, T. Genetic characterization of antibiotic resistance and virulence factors in Enterococcus spp. from Japanese retail ready-to-eat raw fish. Food Microbiol., 38, 2014, 62-66.
Han, Y., Wang, J., Zhao, Z., Chen, J., Lu, H., & Liu, G. Fishmeal Application Induces Antibiotic Resistance Gene Propagation in Mariculture Sediment. Environ. Sci. Technol., 51(18), 2017, 10850–10860.
Harpaz, S., Glatman, L., Drabkin, V., & Gelman, A. Effects of herbal essential oils used to extend the shelf-life of freshwater reared Asian sea bass fish (Lates calcarifer). J. Food Protect., 66, 2003, 410–417.
Jack, R. W., Tagg, J. R., & Ray, B. Bacteriocins of Gram-positive bacteria. Microbiol. Mol. Biol. Rev., 59, 1995, 171–200.
Johnson, E. M., Jung, D. Y., Jin, D. Y., Jayabalan, D. R., Yang, D. S. H., & Suh, J. W. Bacteriocins as food preservatives: Challenges and emerging horizons. Crit. Rev. Food Sci. Nutr., 7, 2017, 1–25.
Kang, C. H., & So, J. S. Antibiotic and heavy metal resistance in Shewanella putrefaciens strains isolated from shellfishes collected from West Sea, Korea. Mar Pollut Bull., 112(1-2), 2016, 111-116.
Kang, C. H., Shin, Y., Jang, S., Jung, Y., & So, J. S. Antimicrobial susceptibility of Vibrio alginolyticus isolated from oyster in Korea. Environ Sci Pollut Res Int., 23(20), 2016, 21106-21112.
Kostaki, M., Giatrakou, V., Savvaidis, I. N., & Kontominas, M. G. Combined effect of MAP and thyme essential oil on the microbiological, chemical and sensory attributes of organically aquacultured sea bass (Dicentrarchus labrax) fillets. Food Microbiol., 26, 2009, 475–482.
Kykkidou, S., Giatrakou, V., Papavergou, A., Kontominas, M. G., Savvaidis, & I. N. Effect of thyme essential oil and packaging treatments on fresh Mediterranean swordfish fillets during storage at 4°C. Food Chem., 115, 2009, 169-175.
Li, L., Ye, L., Kromann, S., & Meng, H. Occurrence of Extended-Spectrum β-Lactamases, Plasmid-Mediated Quinolone Resistance, and Disinfectant Resistance Genes in Escherichia coli Isolated from Ready-To-Eat Meat Products. Foodborne Pathog Dis., 14(2), 2017, 109-115
Li, C., Gölz, G., Alter, T., Barac, A., Hertwig, S., & Riedel, C. Prevalence and Antimicrobial Resistance of Yersinia enterocolitica in Retail Seafood. J Food Prot., 23, 2018, 497-501.
Lopatek, M., Wieczorek, K., & Osek, J. Prevalence and Antimicrobial Resistance of Vibrio parahaemolyticus Isolated from Raw Shellfish in Poland. J. Food Prot., 78(5), 2015, 1029-33.
Maravić, A., Šamanić, I., Šprung, M., Fredotović, Ž., Ilić, N., Dragičević, J., & Puizina, J. Broad-spectrum resistance of Pseudomonas aeruginosa from shellfish: infrequent acquisition of novel resistance mechanisms. Environ. Monit. Assess., 190(2), 2018, 81.
Martin, M., Barbeyron, T., Martin, R., Portetelle, D., Michel, G., & Vandenbol. M. The cultivable surface microbiota of the brown alga Ascophyllum nodosum is enriched in macroalgal-polysaccharide-degrading bacteria. Front. Microbiol., 6, 2015, 1487.
Mastromatteo, M., Danza, A., Conte, A., Muratore, G., & DelNobile, M. A. Shelf life of ready to use peeled shrimps as affected by thymol essential oil and modified atmosphere packaging. Int. J. Food Microbiol., 144, 2010, 250–256.
Morejón, I. F., González, A., & Ferrús, M. A. Detection, Identification, and Antimicrobial Susceptibility of Arcobacter spp. Isolated from Shellfish in Spain. Foodborne Pathog. Dis., 14(4), 2017, 238-243.
Nawaz, M., Khan, S. A., Tran, Q., Sung, K., Khan, A. A., Adamu, I, Steele, R. S. Isolation and characterization of multidrug-resistant klebsiella spp. Isolated from shrimp imported from Thailand. Int. J. Food Microbiol., 155, 2012, 179–184.
Noor Uddin, G. M., Larsen, M. H., Gaurdabassi, L. & Dalsgaard, A. Bacterial flora and antimicrobial resistance in raw frozen cultured seafood imported into Denmark. J. Food Protect., 76, 2016, 490-496.
Obaidat, M. M, & Bani Salman, A. E. Antimicrobial Resistance Percentages of Salmonella and Shigella in Seafood Imported to Jordan: Higher Percentages and More Diverse Profiles in Shigella. J. Food Prot., 80(3), 2017, 414-419.
Ortega Blázquez, I., Grande Burgos, M. J., Pérez-Pulido, R., Gálvez, A., & Lucas, R. Treatment With High-Hydrostatic Pressure, Activated Film Packaging With Thymol Plus Enterocin AS-48, and Its Combination Modify the Bacterial Communities of Refrigerated Sea Bream (Sparus aurata) Fillets. Front. Microbiol., 9, 2018, 314.
Ortega-Morente, E., Fernández-Fuentes, M. A., Grande-Burgos, M. J., Abriouel, H., Pérez-Pulido, R., & Gálvez, A. Biocide tolerance in bacteria. Int. J. Food Microbiol., 162, 2013, 13–25.
Pal, C., Bengtsson-Palme, J., Kristiansson, E., & Larsson, D. G. Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics., 16, 2015, 964.
Pitrowska, M. & Popowska, M. Insight into the mobilome of Aeromonas strains. Front. Microbiol., 6, 2015, 494.
Queenan, K., Häsler, B., & Rushton, J. A One Health approach to antimicrobial resistance surveillance: is there a business case for it? Int. J. Antimicrob. Agents., 48, 2016, 422–427.
Quitral, V., Donoso, M. L., Ortiz, J., Herrera, M. V., Araya, H., & Aubourg, S. P. Chemical changes during the chilled storage of Chilean jack mackerel (Trachurus murphyi): effect of a plant-extract icing system. LWT Food Sci. Tech., 42, 2009, 1450–1454.
Rees, E. E., Davidson, J., Fairbrother, J. M., St Hilaire, S., Saab, M., & McClure, J. T. Occurrence and antimicrobial resistance of Escherichia coli in oysters and mussels from Atlantic Canada. Foodborne Pathog. Dis., 12(2), 2015, 164-169.
Romero, J. L., Grande Burgos, M. J., Pérez-Pulido, R., Gálvez, A., & Lucas, R. Resistance to Antibiotics, Biocides, Preservatives and Metals in Bacteria Isolated from Seafoods: Co-Selection of Strains Resistant or Tolerant to Different Classes of Compounds. Front. Microbiol., 8, 2017, 1650.
Roschanski, N., Guenther, S., Vu, T. T. T., Fischer, J., Semmler, T., Huehn, S., Alter, T., & Roesler, U. VIM-1 carbapenemase-producing Escherichia coli isolated from retail seafood, Germany 2016. Euro Surveill., 22(43), 2017.
Ryu, S. H., Park, S. G., Choi, S. M., Hwang, Y. O., Ham, H. J., Kim, S. U., Lee, Y. K., Kim, M. S., Park, G. Y., Kim, K. S., & Chae, Y. Z. Antimicrobial resistance and resistance genes in Escherichia coli strains isolated from commercial fish and seafood. Int. J. Food Microbiol., 152(1-2), 2012, 14-18.
Said, L. B., Hamdaoui, M., Jouini, A., Boudabous, A., Slama, K. B., Torres, C., & Klibi, N. First Detection of CTX-M-1 in Extended-Spectrum β-Lactamase-Producing Escherichia coli in Seafood from Tunisia. J. Food Prot., 17, 2017, 1877-1881.
Sergelidis, D., Abrahim, A., Papadopoulos, T., Soultos, N., Martziou, E., Koulourida, V., Govaris, A., Pexara, A., Zdragas, A., & Papa, A. Isolation of methicillin-resistant Staphylococcus spp. from ready-to-eat fish products. Lett. Appl. Microbiol., 59(5), 2014, 500-506.
Singh, R. P., Baghel, R. S., Reddy, C. R., & Jha, B. Effect of quorum sensing signals produced by seaweed-associated bacteria on carpospores liberation from Gracilaria dura. Front. Plant Sci., 6, 2015, 117.
Sanjit Singh, A., Lekshmi, M., Prakasan, S., Nayak, B. B., & Kumar, S. Multiple Antibiotic-Resistant, Extended Spectrum-β-Lactamase (ESBL)-Producing Enterobacteria in Fresh Seafood. Microorganisms., 5(3), 2017, pii: E53.
Tran, Q. T., Nawaz, M. S., Deck, J., Nguyen, K. T., & Cerniglia, C. E. Plasmid-mediated quinolone resistance in pseudomonas putida isolates from imported shrimp. Appl. Environ. Microbiol., 77(5), 2011, 1885-1887.
Valenzuela, A. S., Benomar, N., Abriouel, H., Cañamero, M. M., & Gálvez, A. Isolation and identification of Enterococcus faecium from seafoods: antimicrobial resistance and production of bacteriocin-like substances. Food Microbiol., 27(7), 2010, 955-961.
Vignaroli, C., Di Sante, L., Leoni, F., Chierichetti, S., Ottaviani, D., Citterio, B., & Biavasco, F. Multidrug-resistant and epidemic clones of Escherichia coli from natural beds of Venus clam. Food Microbiol., 59, 2016, 1-6.
Wang, F., Jiang, L., Yang, Q., Han, F., Chen, S., Pu, S., Vance, A., & Ge, B. Prevalence and antimicrobial susceptibility of major foodborne pathogens in imported seafood. J. Food Prot., 74(9), 2011, 1451-1461.
Wang, C. Y., Huang, H. W., Hsu, C. P., & Yang, B. B. Recent advances in food processing using high hydrostatic pressure technology. Crit. Rev. Food Sci. Nutr., 56, 2016, 527–540.
Watts, J. E. M., Schreier, H. J., Lanska, L., & Hale, M. S. The rising tide of antimicrobial resistance in aquaculture: Sources, sinks and solutions. Mar. Drugs., 15(6), 2017, pii: E158.
Wieczorek, K., & Osek, J. Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from fresh and smoked fish in Poland. Food Microbiol., 64, 2017, 164-171.
Yano, Y., Hamano, K., Tsutsui, I., Aue-Umneoy, D., Ban, M., & Satomi, M. Occurrence, molecular characterization, and antimicrobial susceptibility of Aeromonas spp. in marine species of shrimps cultured at inland low salinity ponds. Food Microbiol., 47, 2015, 21-27.