Determinants of antimicrobial resistance in biosolids: A systematic review, database, and meta-analysis.

Biosolids can provide a nutrient rich soil amendment, particularly for poor soils and semi-arid or drought-prone areas. However, there are concerns that sludge and biosolids could be a source of propagation and exposure to AMR determinants such as antibiotic resistant bacteria (ARB), and antibiotic resistance genes (ARGs). To inform risk assessment efforts, a systematic literature review was performed to build a comprehensive spreadsheet database of ARB and ARG concentrations in biosolids (and some sludges specified as intended for land application), along with 69 other quantitative and qualitative meta-data fields from 68 published studies describing sampling information and processing methods that can be used for modeling purposes. Mean ARG concentrations per gram in positive samples of biosolids ranged from -5.7 log ₁₀ (gene copies [gc]/g) to 12.92 log ₁₀ (gc/g) (with these range values reported per dry weight), and aqueous concentrations ranged from 0.9 log ₁₀ (gc/L) to 14.6 log ₁₀ (gc/L). Mean ARB concentrations per gram of biosolids ranged from 2.02 log ₁₀ (colony forming units [CFU]/g) to 9.00 log ₁₀ (CFU/g) (dry weight), and aqueous concentrations ranged from 3.23 log ₁₀ (CFU/L) to 12.0 log ₁₀ (CFU/L). ARG log removal values (LRVs) during sewage sludge stabilization were calculated from a meta-analysis of mean concentrations before and after stabilization from 31 studies, ranging from -2.05 to 5.52 logs. The classes of resistance most relevant for a risk assessment corresponded to sulfonamide (sul1 and sul2), tetracycline (tetZ, tetX, tetA and tetG), beta-lactam (bla _TEM ), macrolide (ermB and ermF), aminoglycoside (strA and aac(6')-Ib-cr), and integron-associated (intI1). The resistance classes most relevant for ARB risk assessment included sulfonamides (sulfamethoxazole and sulfamethazine), cephalosporin (cephalothin and cefoxitin), penicillin (ampicillin), and ciprofloxin (ciprofloxacin). Considerations for exposure assessment are discussed to highlight risk assessment needs relating to antimicrobial resistance (AMR) associated with biosolids application. This study aids in prioritization of resources for reducing the spread of AMR within a One Health framework.
Competing Interests: Declaration of competing interest The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Kerry Hamilton reports financial support was provided by Water Research Foundation. Kerry Hamilton reports financial support was provided by U.S. Department of Agriculture. Nicholas Ashbolt reports administrative support was provided by The Cooperative Research Centre for Solving Antimicrobial Resistance in Agribusiness, Food and Environments (CRC SAAFE). If there are other authors, they declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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