In the midst of the giant Salmonella Heidelberg outbreak last week — now up to 107 cases in 31 states, and triggering a recall of 36 million pounds of ground turkey — it was easy to miss that a second and even more troubling strain of resistant Salmonella is on the move. As I wrote last week, that strain is called Salmonella Kentucky ST198, it is much more drug-resistant than the U.S. Heidelberg outbreak, and it has been spreading since 2002 from Egypt and north Africa through Europe, and has now been identified in the United States. Its primary vector appears to be chicken meat.
There is an interesting and troubling aspect to the spreading Kentucky strain that there wasn’t time to talk about last week, in the midst of the Heidelberg news. It’s this: The authors suspect that this enhanced resistance — to Cipro, and thus the class called fluoroquinolones that are very important in treating Salmonella — may have come into African chickens via drug use in aquaculture.
The authors are especially concerned about farms that practice what’s called “integrated aquaculture,” in which chicken litter and manure are used to fertilize ponds in which fish are grown, and waste from the ponds is harvested and used as poultry feed.
They write in the Journal of Infectious Diseases:
How the ST198-X1 CIPR Kentucky clone entered in the poultry sector in various parts of Africa remains to be determined. This clone was found in at least 2 species of poultry (chicken and turkey). Furthermore, a preliminary investigation revealed that poultry industries of Nigeria, Morocco, and Ethiopia used indigenous domestic fowl, arguing against the dissemination of a common contaminated poultry lineage throughout Africa…
Intensive aquaculture reliant on large amounts of antimicrobial agents may have played an initial role through the acquisition of the genomic island SGI1-K. Intensive pond aquaculture was introduced in Egypt in the mid-1990s, and today, Egypt is responsible for 80% of the farmed fish production on the African continent. The presence of an ISVch4 element from the aquatic environmental bacteria Vibrio cholerae in all the SGI1-Ks, -Ps, and -Qs variants harbored by the ST198-X1 CIPR clone points to the role of the aquatic ecosystem in the acquisition of the SGI1. Furthermore, SGI1 variants were reported for at least 2 other serotypes of Salmonella… The independent acquisition of SGI1 by these 3 distinct serotypes suggests that its transfer occurred repeatedly in a single geographic area.
Translating and expanding: The spread of this new resistance factor cannot have been because one vertical commercial breed of chicken was purchased by the widely separated farmers in Ethiopia, Nigeria and Morocco in whose chickens this resistance factor was found; they were all using local breeds. It is possible the resistance could have developed through the use of chicken feed laced with fluoroquinolones, which is sold in Africa. But the association between the resistance DNA and the waterborne bacterium V. cholerae suggests that fish farming played a role too, either through medicated fish feed, or because the cycling of chicken byproducts into the ponds and fish and then out again as aquaculture waste may have spread that DNA much more broadly.
This is speculative, but it is also dismaying, because integrated aquaculture is both very common — I’ve casually observed it, not really looking for it, in several countries in Southeast Asia — and also frequently recommended by food agencies as a way to produce a lot of protein in a sustainable manner with minimal drain on local ecologies. (Here’s just a few of the many manuals on it, stashed in the document repository of the UN’s Food and Agriculture Organization.)
I can’t see any suggestion in those accumulated manuals that inserting antibiotics into the integrated cycle of fish and chicken farming could have unpredictable effects. But it happens that another set of authors have had the same idea, and have just published a warning in Applied and Environmental Microbiology regarding the use of antibiotic-laced feed in integrated pig and fish farms in Vietnam.
They used a small experimental farm near Hanoi built on the traditional model, called VAC for vuon, ao, chuong — garden, pond, pigpen — in which the pigsty is built on the dike-bank of the pond so that wastes drain directly into it. (Parenthetical: I once asked a farmer in central Vietnam how his ponds got so perfectly round. He said, with much more courtesy than I deserved, that it was because they were bomb craters, from what is called in Vietnamese “the American war.”)
Over a four-month period, the researchers fed the pigs first drug-free feed, then antibiotic-laced feed, then repeated the cycle. During each month, they checked the pigs’ manure and the pond’s sediment for the presence of resistance factors in E. coli and other gut bacteria. In the months when the pigs were receiving the antibiotic-laden feed, the researchers found significantly higher amounts of antimicrobial resistance in the manure and the pond. To confirm that the drug resistance was not coming from an outside source — runoff fro other farms, wildlife, birds — they typed the bacteria from the manure and the sediment, and found they matched.
And it turns out that this was not the first time a warning bell has been rung about about the use of antibiotics in integrated animal/fish farms. The lead author in the current paper recorded the same effect in chicken/fish farms in Thailand as far back as 2003. (That was an observation, however — which led them to set up the controlled experiment in the newly published one.)
I extract several lessons from these findings, all of them depressing.
The first is the revelation, new to me at least, that antibiotic overuse is not solely a problem in industrialized-world agriculture, but has spread into small-scale developing-world farming as well. (For many posts on why agricultural antibiotics are a problem, look here and here.) The second is the uncomfortable realization that even small-scale aquaculture can be as environmentally problematic as the giant open-water farms that Barry Estabrook has called “feedlots of the sea.”
And finally there is yet another reinforcement of something that regrettably has been proven repeatedly, dating back to Stuart Levy’s seminal paper in 1976. Once the resistance factors created by agricultural antibiotics get going, there is no way to predict where or how far they will spread — and that the only way to slow their dissemination, and the human health effects that result, is to control the drugs’ overuse to start.
- Le Hello, S et al. International Spread of an Epidemic Population of Salmonella enterica Serotype Kentucky ST198 Resistant to Ciprofloxacin. Journal of Infectious Diseases, ahead of print. DOI: 10.1093/infdis/jir409
- Dang, ST et al. Impact of medicated feed on the development of antimicrobial resistant bacteria in integrated pig-fish farms in Vietnam. Applied and Environmental Microbiology, ahead of print. doi:10.1128/AEM.02975-10
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