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Official Journal of the Australasian College for Infection Prevention and Control
RESEARCH ARTICLE

Superbugs: the ever growing threat in our food supply

Peter Collignon
+ Author Affiliations
- Author Affiliations

A Infectious Diseases Unit and Microbiology Department, The Canberra Hospital, PO Box 11, Woden, ACT 2606, Australia.

B Canberra Clinical School, Australian National University, Canberra, ACT 0200, Australia. Email: peter.collignon@act.gov.au

Healthcare Infection 17(4) 145-147 https://doi.org/10.1071/HI12051
Submitted: 2 November 2012  Accepted: 2 November 2012   Published: 27 November 2012

Dear Editor,

Antibiotic resistance is rapidly rising. Many bacterial infections are now very difficult, and sometimes impossible, to treat. Gram negative bacteria are the pointy end of this growing problem, including very common bacteria such as E. coli. 1 , 2

Antibiotic resistance is proportional to use. The more antibiotics used, the more resistance develops and spreads. This is both in individuals (e.g. with pneumococcus) and for populations in different countries. 3 5

With many common bacteria, transmission is almost entirely human-to-human (e.g. pneumococcus, gonococcus, meningococcus). Thus, any antibiotic resistance seen in these bacteria will be almost entirely due to antibiotics used in the human sector. However with some other bacteria, the resistance seen is almost entirely due to what has occurred in the agriculture sector. Examples are non-typhoid salmonella and campylobacter. In developed countries these bacteria are almost entirely acquired from food animals (via foods). These are zoonoses, and thus almost all the antibiotic resistance is a result of what happens with antibiotic use in food animals. Vegetarians are also at risk because water, food crops and fields (via manure) can be contaminated with resistant bacteria. There is also the additional chance of cross contamination of non-meat products from meats along the food chain. 6

There are other bacteria where the risk of acquisition from animal sources is more difficult to precisely define, but appears to be quite important. Examples are E. coli and Enterococcus. 6 12 We also sometimes get surprises. Until recently Staphylococcus aureus and MRSA were thought to be almost fairly exclusive human pathogens. However, in many countries (e.g. The Netherlands and Denmark), MRSA is now found frequently in pigs and these strains infect people. 13 Clostridium difficile is now clearly associated with food animals and people are infected with strains found in these animals. There are increasing numbers of people with community onset C. difficile infections. Foods are a likely way these bacterial strains were acquired. 14 16

Resistant E. coli are a major concern because E. coli is the most common bacterial pathogen causing serious infections in people. Bloodstream infection rates vary from 25–60 per 100 000 people per year. 17 This is just the tip of the iceberg, for every such serious and life threatening bloodstream infection, there are likely to be about a hundred other infections (e.g. urinary tract infections). What is now very disconcerting is the increasing multi-resistance resistance worldwide in E. coli. 1 , 7 , 11 , 12

Much of this resistance in E. coli (especially to third generation cephalosporins and fluoroquinolones) is related to resistance that develops in bacteria carried by food animals – especially poultry. 1 , 3 , 6 , 7 , 9 , 11 , 12 This resistance results from the misuse of antibiotics in these animals. Worldwide each year, billions of chicken are injected with third generation cephalosporins just before or after hatching (with ceftiofur) and/or fed fluoroquinolones in their drinking water (e.g. enrofloxacin) for nearly all their lives.

Antibiotics have been used for over 60 years as growth promoters. They are also used for prophylaxis (called ‘metaphylaxis’ when large numbers of animals or entire herds are treated at the same time). 18 This is in stark contrast to what happens in human medicine, where individual patient use is the norm. It effectively means that huge numbers of animals are treated continuously for most of their life with either in-feed or in-water antibiotics. It explains why over 70% of all antibiotics used in most countries are used in food animals. Some of these prophylactic antibiotics are last-line or ‘critically important’ classes of antibiotics for humans, such as the fluoroquinolones and third and fourth generation cephalosporins. 8

While there is ongoing debate on what proportion of antibiotic resistant bacteria infecting people come from food animals, it appears to be substantial. An example of where good practice can help people with serious infections is Australia. It is the only country that has banned the use of fluoroquinolones in food animals. It is not coincidental that Australia has also one of the lowest resistance rates in campylobacter, salmonella and E. coli to fluoroquinolones in the world. 19

In Europe and elsewhere there is abundant evidence that the routine use of third and fourth generation cephalosporins in food animals has contributed to the epidemic of ESBL and other resistant E. coli occurring in community onset infections. 1 , 3 , 6 , 7 , 9 , 11 , 12 In Holland between 20–50% of all bloodstream infections caused by ESBL E. coli are the same strains as found in poultry. 12 Around the world, hundreds of millions of chickens, if not billions, are injected with antibiotics such as aminoglycosides and third generation cephalosporins each year. In addition, most chickens receive fluoroquinolones for most of their relatively short life (~35 days). Thus it is not surprising that we are seeing astronomically high levels of antibiotic resistant E. coli in poultry in countries such as China 21 and even in many areas of Europe. 1 , 6 , 7 In Europe, the resistance patterns of E. coli in blood cultures from humans correlates better with what is seen in poultry than it does with human antimicrobial consumption. 3

There is overwhelming evidence around the world that using antibiotics in food animals, causes resistant bacteria to develop in large numbers and that these bacteria are transmitted to people via the food and water. There is also ample evidence that resistant bacteria, such as ESBL E. coli, cause substantially increased mortality and morbidity in humans. 20

We need more vigorous action to stop the use of third generation cephalosporins in food animals in Australia, so that we don’t get the same problem that is occurring elsewhere. We need to be vigilant to ensure that foods imported into this country are not tainted with superbugs such as ESBL E. coli. We urgently need action to stop the use worldwide of critically important antibiotics such as fluoroquinolones and third generation cephalosporins in food animals and the overall ongoing excessive use and abuse of large volumes of antibiotics in food animals.


Conflict of interest

The author has no conflicts to declare.


Funding

The author received no funding in relation to this letter.



References

[1]  Carlet J, Collignon P, Goldmann D, Goossens H, Gyssens IC, Harbarth S, et al Society’s failure to protect a precious resource: antibiotics. Lancet 2011; 378 369–71.
Society’s failure to protect a precious resource: antibiotics.Crossref | GoogleScholarGoogle Scholar |

[2]  Hughes JM. Preserving the lifesaving power of antimicrobial agents. JAMA 2011; 305 1027–8.
Preserving the lifesaving power of antimicrobial agents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtFWlu7o%3D&md5=6c342e6b2752976713895211e16a453bCAS |

[3]  Vieira AR, Collignon P, Aarestrup FM, McEwen SA, Hendriksen RS, Hald T, et al Association between antimicrobial resistance in Escherichia coli isolates from food animals and blood stream isolates from humans in Europe: an ecological study. Foodborne Pathog Dis 2011; 8 1295–301.
Association between antimicrobial resistance in Escherichia coli isolates from food animals and blood stream isolates from humans in Europe: an ecological study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKmurvE&md5=2fb2625a4eb6294dab09ae1e16cc4746CAS |

[4]  Goossens H, Ferech M, Vander Stichele R, Elseviers M, ESAC Project Group Outpatient antibiotic use in Europe and association with resistance: a cross-national database study. Lancet 2005; 365 579–87.

[5]  Nasrin D, Collignon PJ, Roberts L, Wilson EJ, Pilotto LS, Douglas RM. Effect of beta lactam antibiotic use in children on pneumococcal resistance to penicillin: prospective cohort study. BMJ 2002; 324 28–30.
Effect of beta lactam antibiotic use in children on pneumococcal resistance to penicillin: prospective cohort study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVSntg%3D%3D&md5=910c5c8d24ddb07dafb60c5128970fe5CAS |

[6]  Collignon P, Powers JH, Chiller TM, Aidara-Kane A, Aarestrup FM. World Health Organization ranking of antimicrobials according to their importance in human medicine: A critical step for developing risk management strategies for the use of antimicrobials in food production animals. Clin Infect Dis 2009; 49 132–41.
World Health Organization ranking of antimicrobials according to their importance in human medicine: A critical step for developing risk management strategies for the use of antimicrobials in food production animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVCns78%3D&md5=508a04b365987586eb6b81c495dcb9e8CAS |

[7]  Collignon P. Resistant Escherichia coli–we are what we eat. Clin Infect Dis 2009; 49 202–4.
Resistant Escherichia coli–we are what we eat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpt12qsL0%3D&md5=5c12375311ee7e469d089d9587c28f4dCAS |

[8]  Collignon P. The Importance of a One Health Approach to Preventing the Development and Spread of Antibiotic Resistance. Curr Top Microbiol Immunol 2012; Jun 13. [Epub ahead of print]. 10.1007/82_2012_224

[9]  Johnson JR, Sannes MR, Croy C, Johnston B, Clabots C, Kuskowski MA, et al Antimicrobial drug–resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002–2004. Emerg Infect Dis 2007; 13 838–46.
Antimicrobial drug–resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002–2004.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnt1Sks7w%3D&md5=3d55992e2fe82a35ae3bf5addd22d057CAS |

[10]  Heuer OE, Hammerum AM, Collignon P, Wegener HC. Human health hazard from antimicrobial-resistant enterococci in animals and food. Clin Infect Dis 2006; 43 911–6.
Human health hazard from antimicrobial-resistant enterococci in animals and food.Crossref | GoogleScholarGoogle Scholar |

[11]  Jakobsen L, Spangholm DJ, Pedersen K, Jensen LB, Emborg HD, Agersø Y, et al Broiler chickens, broiler chicken meat, pigs and pork as sources of ExPEC related virulence genes and resistance in Escherichia coli isolates from community-dwelling humans and UTI patients. Int J Food Microbiol 2010; 142 264–72.
Broiler chickens, broiler chicken meat, pigs and pork as sources of ExPEC related virulence genes and resistance in Escherichia coli isolates from community-dwelling humans and UTI patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFKktbo%3D&md5=2cc29e53474bbb82d3a02a3622dcc65eCAS |

[12]  Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, et al Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerg Infect Dis 2011; 17 1216–22.
Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands.Crossref | GoogleScholarGoogle Scholar |

[13]  Verkade E, Bergmans AM, Budding AE, van Belkum A, Savelkoul P, Buiting AG, et al Recent Emergence of Staphylococcus aureus Clonal Complex 398 in Human Blood Cultures. PLoS ONE 2012; 7 e41855
Recent Emergence of Staphylococcus aureus Clonal Complex 398 in Human Blood Cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1ant7vF&md5=1a63f9c8d2ade554a2312328932cbc1aCAS |

[14]  Pappas G. You can teach old pathogens new tricks: the zoonotic potential of Escherichia coli, Clostridium difficile, Staphylococcus aureus, and enterococci, or from Noah’s Ark to Pandora’s Box. Clin Microbiol Infect 2012; 18 617–8.
You can teach old pathogens new tricks: the zoonotic potential of Escherichia coli, Clostridium difficile, Staphylococcus aureus, and enterococci, or from Noah’s Ark to Pandora’s Box.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38jitF2mtA%3D%3D&md5=881a59eaebb69679de98b516d921f21dCAS |

[15]  Squire MM, Riley TV. Clostridium difficile Infection in Humans and Piglets: A ‘One Health’ Opportunity. Curr Top Microbiol Immunol 2012; Jun 14. [Epub ahead of print] 10.1007/82_2012_237

[16]  Hensgens MP, Keessen EC, Squire MM, Riley TV, Koene MG, de Boer E, et al European Society of Clinical Microbiology and Infectious Diseases Study Group for Clostridium difficile (ESGCD). Clostridium difficile infection in the community: a zoonotic disease? Clin Microbiol Infect 2012; 18 635–45.
European Society of Clinical Microbiology and Infectious Diseases Study Group for Clostridium difficile (ESGCD). Clostridium difficile infection in the community: a zoonotic disease?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFOhtrzL&md5=f515a4bee93830e90ee9aab3b6b0f405CAS |

[17]  Kennedy KJ, Roberts JL, Collignon PJ. Escherichia coli bacteraemia in Canberra: incidence and clinical features. Med J Aust 2008; 188 209–13.

[18]  Step DL, Engelken T, Romano C, Holland B, Krehbiel C, Johnson JC, et al Evaluation of three antimicrobial regimens used as metaphylaxis in stocker calves at high risk of developing bovine respiratory disease. Vet Ther 2007; 8 136–47.
| 1:STN:280:DC%2BD2szpvFyltQ%3D%3D&md5=ae4857a7b60d5c29d915b649a799025aCAS |

[19]  Cheng AC, Turnidge J, Collignon P, Looke D, Barton M, Gottlieb T. Control of fluoroquinolone resistance through successful regulation, Australia. Emerg Infect Dis 2012; 18 1453–60.
Control of fluoroquinolone resistance through successful regulation, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVCjsLjK&md5=89128132d7dc319a9899bfcb679e05b5CAS |

[20]  de Kraker ME, Davey PG, Grundmann H, BURDEN study group Mortality and hospital stay associated with resistant Staphylococcus aureus and Escherichia coli bacteremia: estimating the burden of antibiotic resistance in Europe. PLoS Med 2011; 8 e1001104
Mortality and hospital stay associated with resistant Staphylococcus aureus and Escherichia coli bacteremia: estimating the burden of antibiotic resistance in Europe.Crossref | GoogleScholarGoogle Scholar |

[21]  Ho PL, Chow KH, Lai EL, Lo WU, Yeung MK, Chan J, et al Extensive dissemination of CTX-M-producing Escherichia coli with multidrug resistance to ‘critically important’ antibiotics among food animals in Hong Kong, 2008–10. J Antimicrob Chemother 2011; 66 765–8.
Extensive dissemination of CTX-M-producing Escherichia coli with multidrug resistance to ‘critically important’ antibiotics among food animals in Hong Kong, 2008–10.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsFKltrc%3D&md5=feff9367b1032d744db9416d1c3fc291CAS |