Emergence of ciprofloxacin-resistant extended-spectrum β-lactamase-producing enteric bacteria in hospital wastewater and clinical sources
Introduction
Hospital wastewater is considered one of the major reservoirs of pathogenic bacteria. Wastewater or natural water supplies into which wastewater has been discharged are likely to contain pathogenic organisms mainly coming from human excreta [1]. Furthermore, antibiotics used in hospitals and their release into effluents and municipal sewage via patient excreta or direct deposition impose a selection pressure on bacteria leading to emergence of resistance to different classes of antibiotics in micro-organisms in the aquatic environment [2]. Besides this, wastewater from hospitals constitutes a route of dissemination of antibiotic-resistant bacteria to human and animal populations through various ecological modes of transmission including food, water and insects vectors. Moreover, in developing countries, the chance of transmission of pathogenic bacteria is more common owing to lack of adequate hygiene, poor water quality and inadequate management of human and hospital wastes [1]. Considering the impact of hospital-acquired infections, national evidence-based guidelines for preventing healthcare-associated infections in National Health Service (NHS) hospitals were commissioned by the Department of Health in England. These guidelines focused on hospital environmental hygiene, hand hygiene, the use of personal protective equipment, and the safe use and disposal of sharps; preventing infections associated with the use of short-term indwelling urethral catheters; and preventing infections associated with central venous catheters [3].
The occurrence of drug-resistant micro-organisms in hospital wastewater and clinical sources creates immense clinical and public health problems. Currently, extended-spectrum β-lactamase (ESBL)-producing enteric bacteria are globally recognised problematic multidrug-resistant (MDR) bacteria. ESBLs confer resistance to β-lactam antibiotics containing an oxyimino group (e.g. ceftazidime, cefotaxime and aztreonam). ESBL-producing organisms have been associated with various community- and hospital-acquired infections, including urinary tract infections, bacteraemia, peritonitis, nosocomial pneumonia, intra-abdominal infections and meningitis [4]. Ciprofloxacin has been regarded as a potent antimicrobial recommended for the treatment of various diseases caused by ESBL-producing enteric bacteria [4], [5]. As the use of fluoroquinolones in treatment strategies is increasing, resistance to fluoroquinolones has emerged and has been documented globally. A recent surveillance study, the Study for Monitoring Antimicrobial Resistance Trends (SMART), included 38 hospitals from 10 countries in the Asia-Pacific region and found 48.6% resistance to ciprofloxacin with wide variation among different countries, being as high as 76.2% in Vietnam and 72.0% in China [6].
However, the incidence of fluoroquinolone resistance in ESBL-producing enteric bacteria is less explored in India [7]. Therefore, the aim of this study was to investigate the prevalence of ciprofloxacin resistance and ESBL production among enteric bacteria from hospital wastewater as well as clinical sources and to emphasise the impact of this potential problem on human health.
Section snippets
Isolation and characterisation of enteric bacteria and growth conditions
Enteric bacteria from clinical sources were isolated from urine samples of patients with urinary tract infection and from stool samples of patients with gastrointestinal tract infection (mainly diarrhoea) at Jawaharlal Nehru Medical College, Aligarh Muslim University (Aligarh, India) and Ashok Pathology and Research Centre (Aligarh, India). Wastewater samples were collected from the Jawaharlal Nehru Medical College Hospital wastewater discharging point during the months December 2011 to
Results
A total of 183 isolates comprising E. coli (n = 101), K. pneumoniae (n = 17), Enterobacter spp. (n = 21), Salmonella spp. (n = 18), Shigella spp. (n = 9) and Proteus spp. (n = 17) were isolated, of which 80 were from clinical sources and 103 were isolated from hospital wastewater (Supplementary Table S1).
The incidence of antibiotic resistance against individual antibiotics was determined for 16 antibacterial agents. Overall, the bacterial isolates
Discussion
The prevalence of antibiotic resistance among bacteria has been increasing in recent years. In this study, a greater incidence of resistance to antibiotics and the MDR nature of the test isolates revealed that there was a continuous selective pressure of commonly used antibiotics in the hospital environment. Moreover, non-antibiotic toxic compounds in the environment may also help in the development and selection of co-resistance to antibiotics [13].
Production of ESBL is the most prevalent
Funding
MM has received financial assistance from Aligarh Muslim University (Aligarh, India) in the form of a non-NET-UGC Fellowship of the University Grants Commission.
Competing interests
None declared.
Ethical approval
Not required.
Acknowledgments
The authors are grateful to Prof. Abida Malik (Jawaharlal Nehru Medical College, Aligarh Muslim University, Aligarh, India) and Dr Ashok Kumar (Ashok Pathology and Research Centre, Aligarh, India) for providing the clinical isolates.
References (16)
Recommendation for treatment of severe infections caused by Enterobacteriaceae producing extended-spectrum β-lactamases (ESBLs)
Clin Microbiol Infect
(2000)- et al.
Antimicrobial resistance and resistance mechanisms of Enterobacteriaceae in ICU and non-ICU wards in Europe and North America: SMART 2011–2013
J Glob Antimicrob Resist
(2015) Excreta-related infections and the role of sanitation in the control of transmission
Hospital wastewater containing pharmaceutically active compounds and drug-resistant organisms: a source of environmental toxicity and increased antibiotic resistance
J Residuals Sci Technol
(2008)- et al.
epic2: National evidence-based guidelines for preventing healthcare-associated infections in NHS hospitals in England
J Hosp Infect
(2007) - et al.
Clinical importance and epidemiology of quinolone resistance
Infect Chemother
(2014) - et al.
Identification of extended-spectrum β-lactamase and quinolone resistance genes in Escherichia coli isolated from hospital wastewater from central India
J Antimicrob Chemother
(2012) Enterobacteriaceae: introduction and identification
Cited by (37)
Combating antibiotic resistance using wastewater surveillance: Significance, applications, challenges, and future directions
2024, Science of the Total EnvironmentEnvironmental antimicrobial resistance and its drivers: a potential threat to public health
2021, Journal of Global Antimicrobial ResistanceCitation Excerpt :Recently, MRSA has become a major community-acquired pathogen with enhanced virulence and transmission characteristics to become a serious nosocomial pathogen [35–37]. Antibiotic-resistant Gram-negative bacteria, mainly members of the Enterobacteriaceae family, have been increasingly reported from hospital wastewater [38–40]. These reports describe that the use of almost every antibiotic eventually results in the development of resistant strains, proving the extreme flexibility, hostility and wide-range adaptability of the bacterial genome.
Physical, chemical, and biological impact (hazard) of hospital wastewater on environment: presence of pharmaceuticals, pathogens, and antibiotic-resistance genes
2020, Current Developments in Biotechnology and Bioengineering: Environmental and Health Impact of Hospital WastewaterBioactive extracts of Carum copticum L. enhances efficacy of ciprofloxacin against MDR enteric bacteria
2019, Saudi Journal of Biological SciencesCitation Excerpt :Another report of SMART study in the Asia-Pacific region have shown greater incidence of fluoroquinolones resistance (ciprofloxacin 82.5% and levofloxacin 79.3%) among ESβL producers than resistance in non-ESβL producing isolates to those agents (31.2% and 28.6%, respectively) (Lu et al., 2012). Similarly, studies from India have also shown high prevalence of ciprofloxacin resistance among ESβL producers in clinical as well as environmental isolates (Tripathi et al., 2012; Maheshwari et al., 2016a, 2016b; Bajaj et al., 2016; Diwan et al., 2012). This is likely due to rise in demand for fluoroquinolones, particularly to treat potentially fatal infections (Wener et al., 2010).
Detection of TEM and CTX-M genes from ciprofloxacin resistant Proteus mirabilis and Escherichia coli isolated on urinary tract infections (UTIs)
2018, Microbial PathogenesisCitation Excerpt :However, the result proved that the partial inhibition of ciprofloxacin and other discs was intimated that the pathogens enhance the resilient effect (MDRs) by loss of ability in antibiotics and may able to produce ESBL. The recent study of Maheswari et al. [27] reported that the relationship between ESBL production and ciprofloxacin resistance is more significant in clinical isolates by intensive use of fluoroquinolones. The resistance among ESBL producers to fluoroquinolones (ciprofloxacin 82.5% and levofloxacin 79.3%) was far greater than the rates of resistance in non-ESBL-producing isolates to the above agents (31.2% and 28.6%, respectively).