A Surveillance Study of Culturable and Antimicrobial-Resistant Bacteria in Two Urban WWTPs in Northern Spain

  1. Pino-Hurtado, Mario Sergio 1
  2. Fernández-Fernández, Rosa 1
  3. Campaña-Burguet, Allelen 1
  4. González-Azcona, Carmen 1
  5. Lozano, Carmen 1
  6. Zarazaga, Myriam 1
  7. Torres, Carmen 1
  1. 1 Universidad de La Rioja
    info

    Universidad de La Rioja

    Logroño, España

    ROR https://ror.org/0553yr311

Revista:
Antibiotics

ISSN: 2079-6382

Año de publicación: 2024

Volumen: 13

Número: 10

Páginas: 955

Tipo: Artículo

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DOI: 10.3390/ANTIBIOTICS13100955 GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Antibiotics

Repositorio institucional: lock_openAcceso abierto Editor

Resumen

Background/Objectives: Wastewater treatment plants (WWTPs) are hotspots for the spread of antimicrobial resistance into the environment. This study aimed to estimate the proportion of clinically relevant antimicrobial-resistant bacteria in two Spanish urban WWTPs, located in the region of La Rioja (Spain); Methods: Ninety-four samples (48 water/46 sludge) were collected and streaked on ten different selective media, in order to recover the culturable bacterial diversity with relevant resistance phenotypes: Extended-Spectrum β-Lactamase-producing Escherichia coli/Klebsiella pneumoniae (ESBL-Ec/Kp), Carbapenem-resistant Enterobacteriaceae (CR-E), Methicillin-resistant Staphylococcus aureus (MRSA), and Vancomycin-resistant Enterococcus faecium/faecalis (VR-E. faecium/faecalis). Isolates were identified by MALDI-TOF and were tested for antimicrobial susceptibility using the disk diffusion method. The confirmation of ESBL production was performed by the double-disk test; Results: A total of 914 isolates were recovered (31 genera and 90 species). Isolates with clinically relevant resistance phenotypes such as ESBL-Ec/Kp and CR-E were recovered in the effluent (0.4 × 100–4.8 × 101 CFU/mL) and organic amendment samples (1.0–101–6.0 × 102 CFU/mL), which are discharged to surface waters/agricultural fields. We reported the presence of VR-E. faecium in non-treated sludge and in the digested sludge samples (1.3 × 101–1 × 103 CFU/mL). MRSA was also recovered, but only in low abundance in the effluent (0.2 × 101 CFU/mL); Conclusions: This study highlights the need for improved wastewater technologies and stricter regulations on the use of amendment sludge in agriculture. In addition, regular monitoring and surveillance of WWTPs are critical for early detection and the mitigation of risks associated with the spread of antimicrobial resistance.

Referencias bibliográficas

  • Forde, (2020), Clin. Microb. Rev., 33, pp. 10
  • Inoue, (2019), Glob. Health Med., 1, pp. 61, 10.35772/ghm.2019.01026
  • Walsh, T.R., Gales, A.C., Laxminarayan, R., and Dodd, P.C. (2023). Antimicrobial Resistance: Addressing a Global Threat to Humanity. PLoS Medic., 20.
  • Lozano, (2016), Environ. Pollut., 212, pp. 71, 10.1016/j.envpol.2016.01.038
  • Manaia, (2018), Environ. Internat., 115, pp. 312, 10.1016/j.envint.2018.03.044
  • Harnisz, (2020), Sci. Total Environ., 741, pp. 140466, 10.1016/j.scitotenv.2020.140466
  • Manaia, (2023), Crit. Rev. Environ. Sci. Tech., 53, pp. 754, 10.1080/10643389.2022.2085956
  • Wang, (2023), Sci. Total Environ., 877, pp. 162772, 10.1016/j.scitotenv.2023.162772
  • Rorat, A., Courtois, P., Vandenbulcke, F., and Lemiere, S. (2019). Sanitary and environmental aspects of sewage sludge management. Industrial and Municipal Sludge, Butterworth-Heinemann.
  • Styszko, (2022), Scient. Rep., 12, pp. 12227, 10.1038/s41598-022-16354-5
  • Matussek, (2010), J. Appl. Microbiol., 108, pp. 1244, 10.1111/j.1365-2672.2009.04515.x
  • Biavasco, (2007), Appl. Environ. Microbiol., 73, pp. 3307, 10.1128/AEM.02239-06
  • Devane, (2020), Water Res., 185, pp. 116204, 10.1016/j.watres.2020.116204
  • Makowska, (2021), Sci. Total Environ., 765, pp. 144176, 10.1016/j.scitotenv.2020.144176
  • Karimi, F., Samarghandi, M.R., Shokoohi, R., Godini, K., and Arabestani, M.R. (2016). Prevalence and Removal Efficiency of Enterococcal Species and Vancomycin-resistant Enterococci of a Hospital Wastewater Treatment Plant. Avic. J. Environ. Health Eng., 3.
  • Silva, V., Ribeiro, J., Rocha, J., Manaia, C.M., Silva, A., Pereira, J.E., Maltez, L., Capelo, J.L., Igrejas, G., and Poeta, P. (2022). High Frequency of the EMRSA-15 Clone (ST22-MRSA-IV) in Hospital Wastewater. Microorganisms, 10.
  • Abbassi, (2017), J. Water Health., 15, pp. 638, 10.2166/wh.2017.258
  • Schmiege, (2021), Sci. Total Environ., 785, pp. 147269, 10.1016/j.scitotenv.2021.147269
  • Savin, (2022), Sci. Total Environ., 804, pp. 150000, 10.1016/j.scitotenv.2021.150000
  • Hassen, (2021), FEMS Microb. Ecol., 97, pp. fiaa231, 10.1093/femsec/fiaa231
  • Alouache, (2014), Microb. Drug Resist., 20, pp. 30, 10.1089/mdr.2012.0264
  • Rocha, J., Ferreira, C., Mil-Homens, D., Busquets, A., Fialho, A.M., Henriques, I., Gomila, M., and Manaia, C.M. (2022). Third generation cephalosporin-resistant Klebsiella pneumoniae thriving in patients and in wastewater: What do they have in common?. BMC Genom., 23.
  • Galler, (2014), Clinic. Microb. Infect., 20, pp. O132, 10.1111/1469-0691.12336
  • Hoelle, (2019), J. Water Health, 17, pp. 219, 10.2166/wh.2019.165
  • Wang, (2018), Sci. Total Environ., 621, pp. 990, 10.1016/j.scitotenv.2017.10.128
  • Cardoso, (2013), Diagn. Microb. Infect. Dis., 76, pp. 80, 10.1016/j.diagmicrobio.2013.02.001
  • Bondarczuk, (2019), Sci. Total Environ., 650, pp. 2951, 10.1016/j.scitotenv.2018.10.050
  • Cahill, (2019), Sci. Total Environ., 672, pp. 618, 10.1016/j.scitotenv.2019.03.428
  • Onalenna, (2022), Heliyon, 8, pp. e09089, 10.1016/j.heliyon.2022.e09089
  • Azuma, (2022), Sci. Total Environ., 839, pp. 156232, 10.1016/j.scitotenv.2022.156232
  • Chen, (2024), J. Environ. Sci., 138, pp. 227, 10.1016/j.jes.2023.04.012
  • Sousa, (2021), Sci. Total Environ., 782, pp. 146892, 10.1016/j.scitotenv.2021.146892
  • Korzeniewska, (2012), Water Air Soil Pollut., 223, pp. 4039, 10.1007/s11270-012-1171-z
  • Caltagirone, M., Nucleo, E., Spalla, M., Zara, F., Novazzi, F., Marchetti, V.M., Piazza, A., Bitar, I., De Cicco, M., and Paolucci, S. (2017). Occurrence of Extended Spectrum β-Lactamases, KPC-Type, and MCR-1.2-Producing Enterobacteriaceae from Wells, River Water, and Wastewater Treatment Plants in Oltrepò Pavese Area, Northern Italy. Front. Microb., 8.
  • Hocquet, (2016), J. Hosp. Infect., 93, pp. 395, 10.1016/j.jhin.2016.01.010
  • Marutescu, G., Popa, M., Gheorghe-Barbu, I., Barbu, I.C., Rodríguez-Molina, D., Berglund, F., Blaak, H., Flach, C.-F., Kemper, A., and Spießberger, B. (2023). Wastewater treatment plants, an “escape gate” for ESCAPE pathogens. Front. Microb., 14.
  • Schwaiger, (2010), Environ. Res., 110, pp. 318, 10.1016/j.envres.2010.02.009
  • Zurfluh, (2017), Int. J. Antimicrob. Agent., 50, pp. 436, 10.1016/j.ijantimicag.2017.04.017
  • Rolbiecki, (2021), Intern. J. Hyg. Environ. Health., 237, pp. 113831, 10.1016/j.ijheh.2021.113831
  • Hrenovic, (2017), Water Res., 126, pp. 232, 10.1016/j.watres.2017.09.007
  • Blaak, (2021), Sci. Total Environ., 776, pp. 145925, 10.1016/j.scitotenv.2021.145925
  • Yao, (2017), Front Microb., 8, pp. 1143, 10.3389/fmicb.2017.01143
  • Liu, M., Zheng, L., Zhu, L., Lu, G., Guo, H., Guan, J., Jing, J., Sun, S., Wang, Y., and Wang, Z. (2023). Characteristics of Carbapenem-resistant Klebsiella pneumoniae in sewage from a tertiary hospital in Jilin Province, China. PLoS ONE, 18.
  • Ekwanzala, (2020), J. Glob. Antim. Resist., 20, pp. 94, 10.1016/j.jgar.2019.07.011
  • (2021), Int. J. One Health, 7, pp. 1, 10.14202/IJOH.2021.1-5
  • Wang, S., Xu, L., Chi, X., Li, Y., Kou, Z., Hou, P., Xie, H., Bi, Z., and Zheng, B. (2019). Emergence of NDM-1- and CTX-M-3-Producing Raoultella ornithinolytica in Human Gut Microbiota. Front. Microb., 10.
  • Iovleva, (2019), Antim. Agents Chemother., 64, pp. 10
  • Chi, (2020), Antimicrob. Agents Chemother., 64, pp. 10, 10.1128/AAC.01983-19
  • Castanheira, (2009), J. Clin. Microb., 47, pp. 4129, 10.1128/JCM.01502-09
  • Zheng, (2015), Antim. Agents Chemother., 59, pp. 7086, 10.1128/AAC.01363-15
  • Zou, (2022), Environ. Pollut., 306, pp. 119437, 10.1016/j.envpol.2022.119437
  • Boopathy, (2017), Bioresource Tech., 240, pp. 144, 10.1016/j.biortech.2017.02.093
  • Thompson, (2013), J. Appl. Microb., 114, pp. 44, 10.1111/jam.12037
  • Wan, (2014), Water Res., 64, pp. 288, 10.1016/j.watres.2014.07.014
  • Melin, (2009), Water Res., 43, pp. 925, 10.1016/j.watres.2008.11.036
  • Goldstein, (2012), Environ. Health Perspect., 120, pp. 1551, 10.1289/ehp.1205436
  • Tiago, (2006), FEMS Microb. Ecol., 55, pp. 322, 10.1111/j.1574-6941.2005.00032.x
  • Torres, (1994), J. Antim. Chemoth., 33, pp. 553, 10.1093/jac/33.3.553
  • Rehbinder, (2009), Acta Vet Scand., 51, pp. 24, 10.1186/1751-0147-51-24
  • Varela, (2013), Scienc Total Environ., 450–451, pp. 155, 10.1016/j.scitotenv.2013.02.015
  • Pérez-Etayo, L., González, D., Leiva, J., and Vitas, A.I. (2020). Multidrug-Resistant Bacteria Isolated from Different Aquatic Environments in the North of Spain and South of France. Microorganisms, 8.
  • Sib, (2020), Sci. Total Environ., 746, pp. 140894, 10.1016/j.scitotenv.2020.140894
  • Savin, (2020), Appl. Environ. Microb., 86, pp. e02748-19, 10.1128/AEM.02748-19
  • Ferreira, (2023), FEMS Microbes, 4, pp. xtad008, 10.1093/femsmc/xtad008