Co-occurrence of antibiotic and metal resistance in long-term sewage sludge-amended soils: influence of application rates and pedo-climatic conditions

Abstract

Urban sewage sludge (USS) is increasingly being used as an alternative organic amendment in agriculture. Because USS originates mostly from human excreta, partially metabolized pharmaceuticals have also been considered in risk assessment studies after reuse. In this regard, we investigated the cumulative effect of five annual USS applications on the spread of antibiotic-resistant bacteria (ARB) and their subsequent resistance to toxic metals in two unvegetated soils. Eventually, USS contained bacterial strains resistant to all addressed antibiotics with indices of resistance varying between 0.25 for gentamicin to 38% for ampicillin and azithromycin. Sludge-amended soils showed also the emergence of resistome for all tested antibiotics compared to non-treated controls. In this regard, the increase of sludge dose generally correlated with ARB counts, while soil texture had no influence. On the other hand, the multi-antibiotic resistance (MAR) of 52 isolates selected from USS and different soil treatments was investigated for 10 most prescribed antibiotics. Nine isolates showed significant MAR index (≥ 0.3) and co-resistance to Cd, As and Be as well. However, events including an extreme flash flood and the termination of USS applications significantly disrupted ARB communities in all soil treatments. In any case, this study highlighted the risks of ARB spread in sludge-amended soils and a greater concern with the recent exacerbation of antibiotic overuse following COVID-19 outbreak.

Reuse of Sludge as Organic Soil Amendment: Insights into the Current Situation and Potential Challenges

“…Industrial sludge is the by-product of wastewater treatment that does not have domestic/urban origins. More precisely, it originates from wastewater that does not contain any human excreta [51]. Major industrial activities that generate wastewater and sludge include food processing, PPMs, tanning, and the textile industries, as well as GTL processes [18,20,52].…”

“…The final sun-dried GTL sludge is dark brown to black in color and has an earthy smell and a friable consistency. As an industrial sludge, the major difference from sewage sludge is the absence of human gastrointestinal pathogens and corresponding drug-resistant genes [51,55].…”

“…In this regard, Khadhar et al [131] found total concentrations of 16 EPA-priority polycyclic aromatic hydrocarbons (PAHs) varying from 96 to the highest level of 7718 mg kg −1 in mixed urban and industrial Tunisian sludges. Many emerging pollutants are released continuously into the environment, even in very low amounts, and some may cause chronic toxicity, endocrine disruption in humans and aquatic wildlife, and the development of pathogenic bacteria resistance [51]. In this regard, the COVID-19 outbreak has induced an overconsumption of personal care products and partially metabolized antibiotics that resist wastewater treatment processes and end up adsorbed onto the sludge fraction in significant amounts as compared to normal conditions [132].…”

“…One of the most recent concerns about biological contamination in soils after sewage sludge application is the proliferation of antibiotic-resistant bacteria (ARB) or genes (ARGs) [51]. Accordingly, Zhang et al [135] found that the application of sewage sludge compost led to ARB enrichment with a special resistance to cefotaxime (β-lactam antibiotic) in soil.…”

“…They also observed the influence of soil types on ARB dynamics after amendments. In another study, ARB were detected in long-term sewage sludge-amended semi-arid soils, with co-resistance of some strains such as Chryseobacterium indoltheticum (ATCC 27950) to the toxic metals Cd, As, and Be [51]. In general, the human health risks associated with different drug-resistant pathogens present in urban effluents are of particular concern, especially after the advent of the COVID-19 pandemic [51,136].…”