Removal of bacterial contaminants and antibiotic resistance genes by conventional wastewater treatment processes in Saudi Arabia: Is the treated wastewater safe to reuse for agricultural irrigation?

Water Research

Volumn 73, Issue , 2015, Pages 277-290

  Al Jassim, Nada ^a   Ansari, Mohd Ikram ^a   Harb, Moustapha ^a   Hong, Pei Ying ^a  

^a KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

Antibiotic resistance; Conventional activated sludge processes; Microbial contaminants; Microbial risk; Water reuse

Indexed keywords

ACTIVATED SLUDGE PROCESS; ANTIBIOTICS; BACTERIA; GENES; IRRIGATION; RISK ASSESSMENT; RNA; WASTEWATER RECLAMATION; WASTEWATER TREATMENT; WATER CONSERVATION;

ACTIVATED-SLUDGE PROCESS; AGRICULTURAL IRRIGATION; ANTIBIOTICS RESISTANCE; CONVENTIONAL ACTIVATED SLUDGE PROCESS; CONVENTIONAL ACTIVATED SLUDGES; MICROBIAL CONTAMINANT; MICROBIAL RISK; REUSE; TREATED WASTEWATER; WATER REUSE;

EFFLUENTS;

ANTIINFECTIVE AGENT; BACTERIAL RNA; PHARMACOLOGY; RNA 16S; WASTE WATER;

FECES; GENE EXPRESSION; IRRIGATION; MICROBIAL COMMUNITY; PATHOGEN; RNA; WASTEWATER; WATER QUALITY; WATER TREATMENT;

ACINETOBACTER; AEROMONAS HYDROPHILA; ANTIBIOTIC RESISTANCE; ARCOBACTER; ARTICLE; BACTERIAL COUNT; BACTERIAL GENE; BACTERIUM; BACTERIUM ISOLATE; CONTROLLED STUDY; DNA SEQUENCE; DRUG EFFECTS; EFFLUENT; ENTEROBACTER; FECAL COLIFORM; GENETICS; HIGH THROUGHPUT SEQUENCING; IRRIGATION (AGRICULTURE); ISOLATION AND PURIFICATION; LEGIONELLA; MICROBIAL COMMUNITY; MICROBIOLOGY; MOLECULAR GENETICS; MYCOBACTERIUM; NEISSERIA; NONHUMAN; PRIORITY JOURNAL; PROCEDURES; PSEUDOMONAS AERUGINOSA; RECYCLING; RISK ASSESSMENT; SAUDI ARABIA; SEWAGE; STANDARDS; STREPTOCOCCUS; TETH GENE; TETO GENE; TETQ GENE; TETW GENE; TETZ GENE; WASTE COMPONENT REMOVAL; WASTE WATER; WASTE WATER MANAGEMENT; WATER MANAGEMENT;

AGRICULTURAL IRRIGATION; ANTI-BACTERIAL AGENTS; BACTERIA; DRUG EFFECTS; DRUG RESISTANCE, MICROBIAL; GENETICS; ISOLATION AND PURIFICATION; METHODS; MICROBIOLOGY; MOLECULAR SEQUENCE DATA; PHARMACOLOGY; RECYCLING; RISK ASSESSMENT; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SAUDI ARABIA; SEQUENCE ANALYSIS, DNA; STANDARDS; WASTE DISPOSAL, FLUID; WASTE WATER; WATER PURIFICATION;

SAUDI ARABIA;

ACINETOBACTER; AEROMONAS; AEROMONAS HYDROPHILA; ARCOBACTER; BACTERIA (MICROORGANISMS); ENTEROBACTER; ENTEROCOCCUS; LEGIONELLA; MYCOBACTERIUM; NEISSERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; STREPTOCOCCUS;

EID: 84922759067     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2015.01.036     Document Type: Article

References (64)

1. Abu-Rizaiza O.S. Modification of the standards of wastewater reuse in Saudi Arabia. Water Res. 1999, 33(11):2601-2608.
2. Al-Jassem D. Treated Sewage Effluent Initiative Aims to Ease Water Shortages 2012, Jeddah.
3. Al-Jasser A.O. Saudi wastewater reuse standards for agricultural irrigation: Riyadh treatment plants effluent compliance. J. King Saudi Univ. - Eng. Sci. 2011, 23:1-8.
4. Al-Tawfiq J.A. Father-to-infant transmission of community-acquired methicillin-resistant Staphylococcus aureus in a neonatal intensive care unit. Infect. Control Hosp. Epidemiol. 2006, 27(6):636-637.
5. Al-Tawfiq J.A. Increasing antibiotic resistance among isolates of Escherichia coli recovered from inpatients and outpatients in a Saudi Arabian hospital. Infect. Control Hosp. Epidemiol. 2006, 27(7):748-753.
6. Al-Tawfiq J.A., Stephens G., Memish Z.A. Inappropriate antimicrobial use and potential solutions: a Middle Eastern perspective. Expert Rev. Anti Infect. Ther. 2010, 8(7):765-774.
7. Aly M., Balkhy H.H. The prevalence of antimicrobial resistance in clinical isolates from Gulf Corporation Council countries. Antimicrob. Resist. Infect. Control 2012, 1(1):26.
8. Amann R.I., Binder B.J., Olson R.J., Chisholm S.W., Devereux R., Stahl D.A. Combination of 16s ribosomal-RNA-targeted oligonucleotide probes with flow-cytometry for analyzing mixed microbial-populations. Appl. Environ. Microbiol. 1990, 56(6):1919-1925.
9. Aminov R.I., Chee-Sanford J.C., Garrigues N., Teferedegne B., Krapac I.J., White B.A., Mackie R.I. Development, validation, and application of PCR primers for detection of tetracycline efflux genes of gram-negative bacteria. Appl. Environ. Microbiol. 2002, 68(4):1786-1793.
10. Aminov R.I., Garrigues-Jeanjean N., Mackie R.I. Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl. Environ. Microbiol. 2001, 67(1):22-32.
11. APHA, AWWA, WEF Standard Method for the Examination of Water and Wastewater 2012, 4-69. American Water Works Association.
12. APHA, AWWA, WEF Standard Method for the Examination of Water and Wastewater 2012, 2-66. American Water Works Association.
13. APHA, AWWA, WEF Standard Method for the Examination of Water and Wastewater 2012, 9-69. American Water Works Association.
14. APHA, AWWA, WEF Standard Method for the Examination of Water and Wastewater 2012, 2-13. American Water Works Association.
15. Ashbolt N.J., Amezquita A., Backhaus T., Borriello P., Brandt K.K., Collignon P., Coors A., Finley R., Gaze W.H., Heberer T., Lawrence J.R., Larsson D.G.J., McEwen S.A., Ryan J.J., Schonfeld J., Silley P., Snape J.R., Van den Eede C., Topp E. Human Health Risk Assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ. Health Perspect. 2013, 121(9):993-1001.
16. Balkhy H.H., Cunningham G., Chew F.K., Francis C., Nakhli D.J.A., Almuneef M.A., Memish Z.A. Hospital- and community-acquired infections: a point prevalence and risk factors survey in a tertiary care center in Saudi Arabia. Int. J. Infect. Dis. 2006, 10(4):326-333.
17. Bodey G.P., Bolivar R., Fainstein V., Jadeja L. Infections caused by Pseudomonas aeruginosa. Rev. Infect. Dis. 1983, 5(2):279-313.
18. Breazeal M.V., Novak J.T., Vikesland P.J., Pruden A. Effect of wastewater colloids on membrane removal of antibiotic resistance genes. Water Res. 2013, 47(1):130-140.
19. Bukhari E.E., Al-Otaibi F.E. Severe community-acquired infection caused by methicillin-resistant Staphylococcus aureus in Saudi Arabian children. Saudi Med. J. 2009, 30(12):1595-1600.
20. Chakraborty T., Huhle B., Hof H., Bergbauer H., Goebel W. Marker exchange mutagenesis of the aerolysin determinant in Aeromonas-hydrophila demonstrates the role of aerolysin in A-hydrophila-associated systemic infections. Infect. Immun. 1987, 55(9):2274-2280.
21. Cole J.R., Wang Q., Cardenas E., Fish J., Chai B., Farris R.J., Kulam-Syed-Mohideen A.S., McGarrell D.M., Marsh T., Garrity G.M., Tiedje J.M. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009, 37(Database issue):D141-D145.
22. da Silva M.F., Vaz-Moreira I., Gonzalez-Pajuelo M., Nunes O.C., Manaia C.M. Antimicrobial resistance patterns in Enterobacteriaceae isolated from an urban wastewater treatment plant. FEMS Microbiol. Ecol. 2007, 60(1):166-176.
23. Davies J.C. Pseudomonas aeruginosa in cystic fibrosis: pathogenesis and persistence. Paediatr. Respir. Rev. 2002, 3(2):128-134.
24. Dwidjosiswojo Z., Richard J., Moritz M.M., Dopp E., Flemming H.C., Wingender J. Influence of copper ions on the viability and cytotoxicity of Pseudomonas aeruginosa under conditions relevant to drinking water environments. Int. J. Hyg. Environ. Health 2011, 214(6):485-492.
25. Edgar R.C., Haas B.J., Clemente J.C., Quince C., Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011, 27(16):2194-2200.
26. Fahrenfeld N., Ma Y., O'Brien M., Pruden A. Reclaimed water as a reservoir of antibiotic resistance genes: distribution system and irrigation implications. Front. Microbiol. 2013, 4:130.
27. FAO Water Use in Agriculture 2005, Food and Agriculture Organization of the United Nations, Rome.
28. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N., Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(34):13780-13785.
29. Galvin S., Boyle F., Hickey P., Vellinga A., Morris D., Cormican M. Enumeration and characterization of antimicrobial-resistant Escherichia coli bacteria in effluent from municipal, hospital, and secondary treatment facility sources. Appl. Environ. Microbiol. 2010, 76(14):4772-4779.
30. George I., Crop P., Servais P. Fecal coliform removal in wastewater treatment plants studied by plate counts and enzymatic methods. Water Res. 2002, 36(10):2607-2617.
31. Gerba C.P., Choi C.Y. Viruses in Foods 2006, 345. Springer. S.M. Goyal (Ed.).
32. Harwood V.J., Levine A.D., Scott T.M., Chivukula V., Lukasik J., Farrah S.R., Rose J.B. Validity of the indicator organism paradigm for pathogen reduction in reclaimed water and public health protection. Appl. Environ. Microbiol. 2005, 71(6):3163-3170.
33. Hazlett L.D., Rosen D.D., Berk R.S. Age-related susceptibility to Pseudomonas-aeruginosa ocular infections in mice. Infect. Immun. 1978, 20(1):25-29.
34. Hong P.Y., Al-Jassim N., Ansari M.I., Mackie R.I. Environmental and public health implications of water reuse: antibiotics, antibiotic resistant bacteria, and antibiotic resistance genes. Antibiotics 2013, 2(3):367-399.
35. KICP The KAUST Industry Collaboration Program (KICP) Annual Strategic Study - Promoting Wastewater Reclamation and Reuse in the Kingdom of Saudi Arabia: Technology Trends, Innovation Needs, and Business Opportunities 2010, KAUST.
36. Li W.Z., Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22(13):1658-1659.
37. McDonnell G., Russell A.D. Antiseptics and disinfectants: activity, action, and resistance. Clin. Microbiol. Rev. 1999, 12(1):147-179.
38. McKinney C.W., Pruden A. Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environ. Sci. Technol. 2012, 46(24):13393-13400.
39. Memish Z.A., Shibl A.M., Kambal A.M., Ohaly Y.A., Ishaq A., Livermore D.M. Antimicrobial resistance among non-fermenting Gram-negative bacteria in Saudi Arabia. J. Antimicrob. Chemother. 2012, 67(7):1701-1705.
40. Michael I., Rizzo L., McArdell C.S., Manaia C.M., Merlin C., Schwartz T., Dagot C., Fatta-Kassinos D. Urban wastewater treatment plants as hotspots for the release of antibiotics in the environment: a review. Water Res. 2013, 47(3):957-995.
41. Mitch W.A., Sedlak D.L. Formation of N-nitrosodimethylamine (NDMA) from dimethylamine during chlorination. Environ. Sci. Technol. 2002, 36(4):588-595.
42. Mitch W.A., Sedlak D.L. Characterization and fate of N-nitrosodimethylamine precursors in municipal wastewater treatment plants. Environ. Sci. Technol. 2004, 38(5):1445-1454.
43. Mokracka J., Koczura R., Kaznowski A. Multiresistant Enterobacteriaceae with class 1 and class 2 integrons in a municipal wastewater treatment plant. Water Res. 2012, 46(10):3353-3363.
44. Muscarella L.F. Contribution of tap water and environmental surfaces to nosocomial transmission of antibiotic-resistant Pseudomonas aeruginosa. Infect. Control Hosp. Epidemiol. 2004, 25(4):342-345.
45. Navarro E., Segura J.C., Castano M.J., Solera J. Use of real-time quantitative polymerase chain reaction to monitor the evolution of Brucella melitensis DNA load during therapy and post-therapy follow-up in patients with brucellosis. Clin. Infect. Dis. 2006, 42(9):1266-1273.
46. Pruden A. Balancing water sustainability and public health goals in the face of growing concerns about antibiotic resistance. Environ. Sci. Technol. 2014, 48(1):5-14.
47. Rizzo L., Manaia C., Merlin C., Schwartz T., Dagot C., Ploy M.C., Michael I., Fatta-Kassinos D. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci. Total Environ. 2013, 447:345-360.
48. Rose J.B., Farrah S.R., Harwood V.J., Levine A.D., Lukasik J., Menendez P., Scott T.M. Reduction of Pathogens, Indicator Bacteria, and Alternative Indicators by Wastewater Treatment and Reclamation Processes 2004, IWA, London, UK.
49. Rudnick J.R., Beck-Sague C.M., Anderson R.L., Schable B., Miller J.M., Jarvis W.R. Gram-negative bacteremia in open-heart-surgery patients traced to probable tap-water contamination of pressure-monitoring equipment. Infect. Control Hosp. Epidemiol. 1996, 17(5):281-285.
50. Saleem M., Bukhari A.A., Al-Malack M.H. Removal efficiencies of indicator micro-organisms in the Al-Khobar wastewater treatment plant. Environ. Eng. Sci. 2000, 17(4):227-232.
51. Saleem M., Bukhari A.A., Al-Malack M.H. Seasonal variations in the bacterial population in an activated sludge system. J. Environ. Eng. Sci. 2003, 2(2):155-162.
52. Shi P., Jia S., Zhang X.X., Zhang T., Cheng S., Li A. Metagenomic insights into chlorination effects on microbial antibiotic resistance in drinking water. Water Res. 2013, 47(1):111-120.
53. Shibl A., Memish Z., Pelton S. Epidemiology of invasive pneumococcal disease in the Arabian Peninsula and Egypt. Int. J. Antimicrob. Agents 2009, 33(5):e411-419. 410.
54. Smeets P.W.M.H.,Medema G.J.,v.D.J.C. The Dutch secret: how to provide safe drinking water without chlorine in the Netherlands. Drink. Water Eng. Sci. 2009, 2:1-14.
55. Tamaki H., Zhang R., Angly F.E., Nakamura S., Hong P.Y., Yasunaga T., Kamagata Y., Liu W.T. Metagenomic analysis of DNA viruses in a wastewater treatment plant in tropical climate. Environ. Microbiol. 2012, 14(2):441-452.
56. UNEP Overview on Land-based Sources and Activities Affecting the Marine Environment in the ROPME Sea Area 1999.
57. USEPA Exposure Factors Handbook 2011 2011, USEPA, Washington, DC.
58. Wang Q., Garrity G.M., Tiedje J.M., Cole J.R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73(16):5261-5267.
59. Wery N., Lhoutellier C., Ducray F., Delgenes J.P., Godon J.J. Behaviour of pathogenic and indicator bacteria during urban wastewater treatment and sludge composting, as revealed by quantitative PCR. Water Res. 2008, 42(1-2):53-62.
60. Winward G.P., Avery L.M., Stephenson T., Jefferson B. Chlorine disinfection of grey water for reuse: effect of organics and particles. Water Res. 2008, 42(1-2):483-491.
61. Yezli S., Shibl A.M., Livermore D.M., Memish Z.A. Antimicrobial resistance among Gram-positive pathogens in Saudi Arabia. J. Chemother. 2012, 24(3):125-136.
62. Zhang K., Farahbakhsh K. Removal of native coliphages and coliform bacteria from municipal wastewater by various wastewater treatment processes: implications to water reuse. Water Res. 2007, 41(12):2816-2824.
63. Zhang Y., Marrs C.F., Simon C., Xi C. Wastewater treatment contributes to selective increase of antibiotic resistance among Acinetobacter spp. Sci. Total Environ. 2009, 407(12):3702-3706.
64. Zhuang Y., Ren H., Geng J., Zhang Y., Zhang Y., Ding L., Xu K. Inactivation of antibiotic resistance genes in municipal wastewater by chlorination, ultraviolet, and ozonation disinfection. Environ. Sci. Pollut. Res. Int. 2014, 1-8.