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ARGs in manure-treated soil decline swiftly after antibiotics phased out
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Data culled from one of the world’s oldest field experiments showed that phasing out antibiotics led to a swift decline in the incidence of accumulated antibiotic resistance genes, or ARGs, in soil treated with animal manure, according to a study published in Nature Scientific Reports.
The results may have implications in the global battle against antibiotic resistance (AR) in both medicine and agriculture. Although no direct link has been made, researchers said, “A strong bridge between clinical and agricultural AR is apparent and to reduce globally increasing AR, antibiotic use and stewardship must improve across all sectors. If this is not done, AR from imprudent sectors will cross-contaminate the whole system.”
Soils at Danish site archived since 1920s
David W. Graham, PhD, MASc, professor of environmental engineering at Newcastle University in the United Kingdom, and colleagues studied soils archived for nearly 100 years at the Askov Long-Term Experimental Station in Denmark. The Askov site has been in operation since 1894 when it was created to study the role of animal manure vs. inorganic fertilizers on soil fertility (fields at the site are each fertilized using only one of the two products).
Graham and colleagues consider Denmark to be “a benchmark for prudent antibiotic stewardship” because, although the country once widely used antibiotics in agriculture and animal production after a boom in the 1950s, it banned antibiotics for nontherapeutic use in the 1990s, and they gradually were phased out.
They harvested DNA from archived soils collected at the Askov site between 1923 and 2010 and contrasted relative abundances of four beta-lactam ARGs — blaTEM, blaSHV, blaOXA and blaCTX-M — and class 1 integron genes (int1) over time.
An increase in ARGs
Data showed no apparent major differences in relative abundance of the four ARGs in the soil treated by either manure or inorganic fertilizers before about 1960. However, Graham and colleagues noted subsequent changes, including:
- an increase in blaTEM, blaSHV and blaOXA levels in manure-treated soils in 1976 samples. The levels crested in the mid-1980s, then waned. Graham and colleagues observed no increase in ARG levels in soil treated by inorganic fertilizers.
- levels of blaCTX-M, which were steady over time in both types of soil before the 1980s, increased almost 15 times in soils treated with manure indicated by 1988 samples, before progressively declining until 2010.
“Clearly, manure additions resulted in higher soil ARG levels of all four genes, but increases differed over time among genes,” Graham and colleagues wrote. “Interestingly, temporal levels of int1 genes in the soils differed somewhat from beta-lactam ARGs, with a shallow increase occurring in parallel with increases in blaTEM, blaSHV, and blaOXA levels in the 1970 and 1980s, but then greatly increasing from the early 1990s through 2010.”
Discoveries with manure-treated soil
Graham and colleagues said they were able to answer key questions that arose from their data. Among their discoveries, they found that:
- ARG levels differed significantly between the two types of soil and were found to be “significantly” higher in soils treated with manure;
- Manure use for a century has increased the probability of broader ARG exposure in drainage water and fodder crops grown in the soils;
- Int1 levels increased by 10 times in manure-treated soils since the 1920s, implying that treating soil this way has “increased the intrinsic potential” of the soils for horizontal gene transfer. Graham and colleagues speculate that continued manure use may explain why int1 levels have increased since the mid-1990s despite Denmark’s ban on nontherapeutic antibiotic use in agriculture; and
- Patterns showed that the appearance of each beta-lactam ARG over time was consistent in soil samples and in a medical context, suggesting that agricultural and clinical antibiotic and resistance development are mutually influential.
‘Both optimistic and concerning results’
Graham and colleagues found what they called “both optimistic and concerning results” pertaining to AR. Although their data did not show whether environmental or clinical bla AR came first, cross-dissemination is “probable” based on the connectedness of environmental and human-associated AR. Such a debate is moot, however, because the genes are pervasive across nature, according to the researchers.
“Most importantly,” they wrote, “this connectivity suggests one cannot address broader problems of increasing AR by employing only medical, agricultural or environmental solutions because acquired AR (regardless of where it emerges) readily migrates across sectors. Therefore, having an antibiotic treatment fail in hospital may have nothing to do with the acquisition of AR in the hospital.”
The results also provide room for optimism by showing that bla genes declined to near baseline levels by 2010, indicating that reducing nontherapeutic use of antibiotics has an effect on AR, according to Graham and colleagues. However, they note that int1 genes increased during the same period.
“Optimistically,” they wrote, “we show if one reduces the apparent pressure of antibiotic use in the environment, AR can be reduced. A good starting point is the elimination of nontherapeutic antibiotic use in agriculture, which Denmark has done.
“However, recent increases in int1 and metal levels in the archived soils are concerning, and hint we may be solving one problem (reduced antibiotic use) by unintentionally creating another (increasing metals). Reducing nontherapeutic antibiotic use in agriculture is an important step, but one must consider the impact of alternate stewardship options within and across sectors or we will get nowhere relative to reducing AR in the future.” – by Gerard Gallagher
Disclosure: The researchers report no relevant financial disclosures.
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