Travel the world – can antibiotic resistant bacteria hitchhike with migratory birds?

By Jonas Waldenström

800px-Seasons1.svgThe beauty of a planet rotating around a slightly tilted axis (23.5 % to the orbital plane, to be exact) is the variation this brings to the intensity of the sunlight that hits the ground. It gives rise to predictable seasonal changes, at our high latitudes equal to a blooming spring, a warm summer, a foggy and mild autumn, and a frosty winter. The tilted axis also means that when it is dark and cold Sweden, it is sunny and lovely on the other side of the globe. Or in other words: when my kids make snow angels in the yard, the penguins rear their chicks under the austral sun.

A large number of animals, in particular birds, but also bats, antelopes, and even insects, utilize the shifts in climate and migrate to make most of the boom of ephemeral resources made available during the warmer seasons. Go to the food, reproduce, raise the offspring, and then pull back to chill-out at lower latitudes during the non-breeding season. A related phenomenon has evolved in some human populations – it is now common that British, German and Swedish people undertake annual migratory movements to Spain. Unlike the other animals mention above, the human movements mainly involve the post-reproductive life-stages. Hordes of well-off elderly now bask in the sun and marinate their livers in cheap red wine. Senescence in the sun.

Basking in the sun

Basking in the sun

A reason why our elderly go to Spain, and not onwards to Morocco, or east to Turkey is the apparent similarities to home. It is different in Spain, yes, but still rather similar to Bavaria, Sussex or Jönköping – just warmer and more vibrant. But not too dangerous, or too vibrant. You can trust the water to be (moderately) clean, and you can eat the food without worrying too much about infections. A prophylactic intake of wine and a diet consisting of 50% canned foodstuffs from home and you are unlikely to succumb to nasty disease.

In epidemiology, we know for certain that travel brings you in contact with disease-causing organisms. When we travel we expose ourselves to pathogens to which our immune systems lack experience, and therefore fail to take swift actions. This is nothing new – this was the fait of the native Indians in South America facing the import of pathogens such as smallpox and whooping cough from invading conquistadores. And in tropical Africa, the Yellow Fever took a large toll of the missionaries sent to christen the heathens; and those fortunate to survive had to endure repeated spells of malaria fevers, and gastrointestinal unpleasantness. Today, prophylaxis and vaccines make us more prepared, but disease risks are a constant worry for the traveller even in our time. And when we get back from our travels we may carry bugs with us and cause secondary cases back at home. In the last weeks we have seen cases of MERS coronavirus associated with haji in Mecca in Arabic countries and Europe. In many gastrointestinal bacterial infections we see a higher degree of antibiotic resistance in travel-associated cases than in domestic cases. Simply, what goes around comes around – and travelling stirs the pot to a boil.

Furthermore, what we put in the pot – the meat and the apples – is highly important. Very little on your dinner plate was grown in your backyard, in fact the ingredients that make up the dish may have travelled half around the globe before being eaten by you. Our food animals are amplifying hosts for many pathogens that cause human infections. The shear numbers of animal involved, the transportation of animals and products, and the frequent use of antibiotics in the food production industry make an additional potent driving force for antibiotic resistance evolution.

On top of this, in the last decade a question whether wild birds can act as flying intercontinental carriers of resistant bacteria has emerged, again and again. The idea can be summarized as follows: If a bird picks up a resistant bug during the non-breeding period, and that bacterium becomes established in the gut, there is a chance that the bacterium could be disseminated along the migratory route all the way to the breeding grounds. Given the state of the world, where for instance there is a marked south-to-north gradient in bacterial resistance problems in Europe, and likewise between South and North America, bird migration can be associated with words like ‘risk’ and ‘threats’. Birds as flying missiles, or pathogen arks.

Did the pathogens fit on the Ark?

Did the pathogens fit on the Ark?

Seemingly elegant, this hypothesis suffers from a number of limitations. First, birds need to be colonized by the nasty bacteria in the first place. Then the bacteria need to be maintained in the gut of the bird for a considerable time, allowing the bird and the bug to move during migration. Once migrated, the bacteria need to be shed in such a manner that they find their way to humans, or more likely our domestic food animals, and then end up on our plate. A long way to go for a microorganism.

Our research group is addressing such questions. The first step is to thoroughly survey the occurrence of antibiotic resistant bacteria in wild birds. This process has going on for a few years, and although there is room for many, many more studies we do know something by now. First, antibiotic resistant bacteria are everywhere, literally everywhere – from the Arctic tundra to the vicinity of the Antarctic research bases. Wildlife is exposed to resistant bacteria and some birds, such as gulls and crows, tend to often carry resistant bugs. Second, we know from genotyping studies that the same types of resistance markers occur in bacteria both from human/food animals and in wild birds. Thus, there is an exchange between sources, likely heavily tilted towards a dissemination from anthropogenic sources to wildlife (rather than the opposite) and it seems most strongly occurring in specific bird species that are in close proximity to humans and food animals.

The most recent study from our group on this subject was published a few weeks ago. The study focused on a bird species that qualify for all of the check points that make a species a possible resistance disseminator culprit: the Franklin’s gull Leucophaeus pipixan. This species breeds in North America, in shallow lakes on the prairies between USA and Canada, but spend the non-breeding season all the way down in southern South America. In Peru and Chile it is common to see thousands of Franklin’s gulls at river mouths on the Pacific coast. And in these rivers the collected wastewater from millions of people are discharged. Thus the gulls find themselves in a habitat that potentially is full of unwanted antibiotic resistant microbes.

Gaviotas de Franclin at Con-con. Photo Jonas Bonnedahl

Gaviotas de Franclin at Con-con. Photo Jonas Bonnedahl

The team visited the Aconcagua and the Bio-Bio rivers in central Chile, where the water met the sea at Concón and Talcahuano, respectively. At these gorgeous sand beaches they sampled Franklin’s gulls. Samples were also collected from 49 healthy human volunteers from the city of San Antonio. Back in Sweden, the samples were cultivated for the presence of Escherichia coli, the most commonly used indicator bacterium in antibiotic research. Randomly collected isolates were then tested against a panel of 10 different antibiotics to measure the degree of acquired resistance. The original samples were also screened for a specific class of resistance mechanisms called extended spectrum beta-lactamases. Bacteria that produce these ESBL enzymes are resistant to a range of lactam antibiotics. ESBL resistance is an emerging problem all over the world, causing suffering and premature deaths.

The resistance profiles from the 267 avian E. coli were similar to that of human samples, with moderate resistance to ampicillin (10.1 %), tetracycline (8.2 %), and streptomycin (6.0 %). Only nitrofurantoin displayed full susceptibility in all samples; all others were in the range of 0.5 – 5 %. However, looking at ESBL in the samples, the gull sample had a prevalence of 30 %, compared to 12 % in the human sample. Not only were there loads of ESBL-positive birds, the ESBL variants were dominated by blaCTX-M-1 and blaCTX-M -15 genotypes that has been extensively described in E. coli causing human infections. Also a multilocus sequence typing of the bacteria showed connections to bacterial genotypes common in infections.

Thus, on the warm sands of Chile sits Franklin’s gulls and enjoy the austral summer. In their intestines they carry resistant bugs with the same genotypes that can cause  infections in humans. Remains to show if the birds can carry these bacteria to the US, or whether carriage is short-lived and more a product of the local environment.

Link to the article here:

Hernandez J, Johansson A, Stedt J, Bengtsson S, Porczak A, et al. (2013) Characterization and Comparison of Extended-Spectrum β-Lactamase (ESBL) Resistance Genotypes and Population Structure of Escherichia coli Isolated from Franklin’s Gulls (Leucophaeus pipixcan) and Humans in Chile. PLoS ONE 8(9): e76150. doi:10.1371/journal.pone.0076150

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Antarctica on the horizon

By Jonas Waldenström

We had some great news last week! Our application to the Chilean research council was funded and our project Campylobacter in Antarctica can be launched in 2014! And what a launch it is: three years with fieldwork on the Antarctic Peninsula! Among penguins and skuas, whales and icebergs, seals and snow! Stuff for legends – Shackleton land, the last frontier – home of the brave!

The last frontier

The last frontier

The project is headed by Dr Daniel Gonzalez-Acuna from the University of Concepción in Chile – one of the best parasitologists in South America and a fantastic, enthusiastic guy! We have collaborated intensely for a number of years already, and last year was the closure of the first Antarctic program. That project aimed at understanding the life cycle of the seabird tick Ixodes uriae and its capacity of transmitting different diseases such as Borrelia, ornithosis, and others. Remember: this is a barren, dry and extremely cold environment, and it is incredible to think that this is also the preferred habitat for a parasitic arthropod. The penguin chicks – the provider of blood meals – are only available during the short Austral summer, and a life cycle can take many years to complete.

Dr Daniel Gonzalez-Acuna and an eight legged fellow

Dr Daniel Gonzalez-Acuna and an eight legged fellow

Most of the results of the previous expeditions are still in the lab, or are being analyzed in the computer. But some stuff is already out. During one of the expeditions a number of samples were collected from the sea just outside the scientific bases at different intervals from the bases’ sewage outlets. The water was filtrated and the filters cultivated for the presence of fecal coliform bacteria. In cases where bacterial growth was present, we went on and identified the bacteria and tested their susceptibility to different antibiotics. Much to our surprise we found real nasty bugs in the samples – ESBL-producing E. coli. The same type of bugs that can cause hospital-acquired infections in many parts of the world. Definitely not bugs to be leaked out into the Antarctic. This article, published in 2012 in AEM, was picked up by the press and spread around widely!

This time we will look at Campylobacter, especially Campylobacter jejuni, but also Campylobacter coli and Campylobacter lari. C. jejuni is a leading cause of bacterial gastroenteritis in humans. However, humans are only accidental hosts for this zoonotic pathogen. It has been detected from a wide range of animal species, primarily birds – and very frequently in poultry. This is likely where you, dear reader, may have made its acquaintance. Although the number of asymptomatic infections probably is high – some say very high – if you get bad, it is real bad. Stomach pains, vomiting and profuse diarrhea! All nasty, real nasty.

An army of locals on the march (photo by Jonas Bonnedahl)

An army of locals on the march (photo by Jonas Bonnedahl)

Why penguins? First, it is interesting to make a thorough inventory of what is in Antarctic wildlife. Are the campylobacters found in Antarctica similar to those in other areas of the world, and to disease-causing strains? However, equally interesting are the population genetic structure of campylobacters, and the frequent horizontal transmission of genes within and even between species. Like a jigsaw puzzle, where genome parts are exchanged and rearranged in new constellations. And now when all tools are available: which genes are found in strains adapted to live in cold environments? What do they do, and how do they work?

Many questions, and many good reasons to go to Antarctica. Time to pack my Shackleton outfit!

Proper researchers in field fittings

Proper researchers in field fittings

Hernández, J., Stedt, J., Bonnedahl, J., Molin, Y., Drobni, M., Calisto-Ulloa, N., Gomez-Fuentes, C., Soledad Astorga-España, M., González-Acuña, D., Waldenström, J., Blomqvist, M. & Olsen, B. 2012. Extended Spectrum β-Lactamase (ESBL), Antarctica. Applied and Environmental Microbiology 78: 2056-2058. [doi: 10.1128/AEM.07320-11]