Friday, 24 October 2014

Antibiotic resistance; not simply a terrestrial problem

Aquaculture is an emerging industry with the potential to provide humans with a high quality protein source whilst reducing pressure on capture fisheries. Aquaculture currently provides 50% of seafood for human consumption but if global seafood consumption rates are to be sustained production will need to reach 80 million tons by 2050 (Bostock et al., 2010; FAO, 2006). Transmission of antibiotic resistant pathogenic bacteria via the medium of seawater is a potential threat to the aquaculture industry as well as wild fisheries, and higher trophic levels in the marine food web, including us!

Methodology; This study by Scarano et al. (2014) was a multisite survey on the antibiotic resistance of Vibrio spp. isolated from gilthead sea bream (Sparus aurata) reared in Italian mariculture systems. Healthy adult Sparus aurata were selected from mariculture farms in three Italian regions and samples from the skin, gills, muscles, and intestinal content were taken for microbial analysis. Samples were inoculated onto agar and Vibrio spp. colonies identified for genetic analysis. Antibiotic resistance was determined by exposing Vibrio spp. to 15 of the most commonly used antibiotics in aquaculture and human medicine.

Findings; 17 Vibrio species were identified in the tissue samples and the two most abundant species were Vibrio harveyi and Vibrio alginolyticus with 55 and 50 strains respectively. V. harveyi is a significant Sparus aurata pathogen in the Mediterranean as is V.alginolyticus which can also cause wound infections in humans and has been shown to produce tetradotoxin in pufferfish. There was a significant difference in Vibrio spp. recovery between the three locations, indicating spatial scale is an important factor in the distribution of Vibrio spp. I was disappointed that no samples were taken of the ambient seawater to see if environmental Vibrio spp. abundance correlated with the fish tissue samples.

Multiple antibiotic resistance was observed in 96% of Vibrio spp. strains whilst V. harveyi was resistant to 9 microbial agents. Of the top four antibiotics that Vibrio spp. were found to be resistant to, two of these (amoxicillin and sulfadiazine) are licensed antibiotics for aquaculture use. The commonly shared resistance to these antimicrobials raises the question as to their overuse in aquaculture and to the presumption that other potentially pathogenic bacteria genera are also resistant.

Erythromycin (a commonly used antibiotic in aquaculture and human medicine) was found to be of low efficacy in inhibiting Vibrio spp. growth. An interesting explanation for this is for the intrinsic resistance of gram negative bacteria to macrolide antibiotics and not necessarily acquisition of resistance genes (Leclerq & Courvalin, 1991).

One of the main limitations of the study was the need for Vibrio spp. to be culturable for the identification of species and antibiotic resistance. However, many marine bacteria are not culturable. Perhaps the development of metagenomic analyses of antibiotic resistance genes would be a useful avenue to pursue in the future.

Wider significance; This paper is a valuable contribution to the poorly understood area of antibiotic resistance in marine bacteria. The responsible use of antibiotcs is vital to maintain their effectiveness in the future. Low-risk alternatives that promote health in aquaculture systems such as dietary immunostimulants and probiotic supplementation should be employed in preference to antibiotics.

Main reference:
Scarano, C., Spanu, C., Ziino, G., Pedonese, F., Dalmasso, A., Spanu, V., Virdis, S., and De Santis, E. (2014). Antibiotic resistance of Vibrio species isolated from Sparus aurata reared in Italian mariculture. New Microbiologica. 37, 329-337.
Additional references:
Bostock, J., McAndrew, B., Richard, R., Jauncey, K., Telfer, T., Lorenzen, K., Little, D., Ross, L., Handisyde, L., Gatwad, I., and Corner, R. (2010). Aquaculture: Global Status and Trends. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences, 365, pp. 2897-912.
FAO, 2006. State of World Aquaculture [online]. [Accessed 19th October 2014] Available at: http://www.fao.org/fishery/topic/13540/en
Leclerq, R. and Courvalin, P. (1991). Intrinsic and unusual resistance to macrolide, lincosamide, and streptogramin antibiotics in bacteria. Antimicrobial Agents and Chemotherapy. 37(7), 1273-1276.

4 comments:

  1. I would like to pose a question. What is the likelihood of the flux of antibiotic resistance genes between the marine environment and terrestrial/freshwater systems? Could freshwater aquaculture or the practice of dumping raw sewage into water systems promote the spread of antibiotic resistance to the marine environment?

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  2. Hi Matthew,
    Thank you for your post. I think using antibiotics in aquacultures for human food sources or even in meat production (Cows/Pigs etc.) is always a difficult one. It not only would affect the animals itself, but as far as I know it also is a high risk for human health. I am afraid I can`t answer your question, but could you maybe explain the mechanism of antibiotic resistance spreading?
    My friend who was doing is Masters in USA last year told me about a really interesting project he was working on. Water used in freshwater aquaculture was connected through a pipe system to agricultural fields and used to water the plants. Excess water was then transported back to the aquaculture. This seems like a very natural filtering system, I am not sure though if this could stop spreading antibiotic resistance?

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  3. Hi Matt,

    Interesting article, I was wondering what the impact of antibiotic use would be on fish health? Although anti-biotics increase short-term growth presumably they reduce the diversity of their gut microflora opening them up to infections by resistant organisms, like Clostridium difficile infections in humans. Do you know of any work on this subject?

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  4. Hi Tabea, sorry for the tardy reply. The spread of antibiotic resistance must be a function of the input mechanism, namely the amount of antibiotics used, which may increase as aquaculture production intensifies. Generally antibiotic licensing for aquaculture is tightly regulated in the EU, however this is not the case for many other developing countries where legislation is lacking. For example antibiotics intended for humans and/or veterinary purposes are routinely used in aquaculture.

    Antibiotics intended for fish are often incorporated into the feed which poses a potential mechanism for transfer to humans at the mixing phase. Antibiotics reaching the fish gut may affect non-target species selecting for antibiotic resistance in pathogenic bacterial species, especially if an insufficient course of antibiotics is administered, and how can you be sure that every fish is receiving the correct dose? Horizontal gene transfer in the biodiverse gut may facilitate spread of antibiotic resistance genes, which may be able to enter the marine environment through faecal matter. The spread of antibiotic resistant pathogenic bacteria from aquaculture species to wild populations could exacerbate the flux of antibiotic resistance genes through migratory patterns.

    There is also the obvious flux of antibiotic resistant bacteria up the food chain including to humans via consumption of seafood that has been improperly cooked e.g. sushi.

    I hope this is of some use. It is interesting to hear of water from aquaculture being used for agriculture. I suppose aquatic bacteria are less likely to survive in terrestrial environments so the spread of antibiotic resistance would be reduced. However if there was a heavy rain event there would likely be run-off into natural water courses and this may facilitate the spread of antibiotic resistant bacteria.

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