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

Joanna Ciol Harrison; Grace V Morgan; Aditya Kuppravalli; Nicole Novak; Michael Farrell; Sienna Bircher; Emily Garner; Nicholas J Ashbolt; Amy Pruden; Rebecca L Muenich; Treavor H Boyer; Clinton Williams; Warish Ahmed; Rasha Maal-Bared; Kerry A Hamilton

doi:10.1016/j.scitotenv.2024.177455

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

Sci Total Environ. 2024 Nov 20:177455. doi: 10.1016/j.scitotenv.2024.177455. Online ahead of print.

Authors

Affiliations

¹ The Biodesign Institute Center for Environmental Health Engineering, Arizona State University, 1001 S. McAllister Ave, Tempe, AZ 85281, USA; School of Sustainable Engineering and the Built Environment, Arizona State University, Tempe, AZ 85281, USA.
² The Biodesign Institute Center for Environmental Health Engineering, Arizona State University, 1001 S. McAllister Ave, Tempe, AZ 85281, USA.
³ Wilson Engineers, Tempe, AZ 85282, USA.
⁴ Wadsworth Department of Civil and Environmental Engineering, West Virginia University, Morgantown, WV 26505, USA.
⁵ Cooperative Research Centre for Solving Antimicrobial Resistance in Agribusiness, Food and Environments (CRC SAAFE), Mawson Lakes, SA 5095, Australia.
⁶ Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, VA 24061, USA.
⁷ Biological and Agricultural Engineering, University of Arkansas, 4183 Bell Engineering Center, Fayetteville, AR 72701, USA.
⁸ School of Sustainable Engineering and the Built Environment, Arizona State University, Tempe, AZ 85281, USA.
⁹ US Department of Agriculture Arid Land Agricultural Research Center, Maricopa, AZ, USA.
¹⁰ CSIRO Environment, Ecosciences Precinct, 41 Boggo Road, Dutton Park, QLD 4102, Australia.
¹¹ Bellevue Research and Testing Laboratory, CDM Smith, 14432 SE Eastgate Way Suite 100, Bellevue, WA 98007, USA.
¹² The Biodesign Institute Center for Environmental Health Engineering, Arizona State University, 1001 S. McAllister Ave, Tempe, AZ 85281, USA; School of Sustainable Engineering and the Built Environment, Arizona State University, Tempe, AZ 85281, USA. Electronic address: kerry.hamilton@asu.edu.

PMID: 39577596
DOI: 10.1016/j.scitotenv.2024.177455

Abstract

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 log₁₀(gene copies [gc]/g) to 12.92 log₁₀(gc/g) (with these range values reported per dry weight), and aqueous concentrations ranged from 0.9 log₁₀(gc/L) to 14.6 log₁₀(gc/L). Mean ARB concentrations per gram of biosolids ranged from 2.02 log₁₀ (colony forming units [CFU]/g) to 9.00 log₁₀ (CFU/g) (dry weight), and aqueous concentrations ranged from 3.23 log₁₀ (CFU/L) to 12.0 log₁₀ (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.

Keywords: Antibiotic resistance genes (ARGs); Antimicrobial resistance (AMR); Biosolids; One health; Quantitative microbial risk assessment (QMRA); Sewage sludge.

Publication types

Review