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Article

Antimicrobial Resistance in Escherichia coli Isolated from Marine Sediment Samples from Kuwait Bay

by
Hanan A. Al-Sarawi
1,*,
Afrah B. Najem
1,
Brett P. Lyons
2,
Saif Uddin
3 and
Mohammad A. Al-Sarawi
4
1
Kuwait Environment Public Authority (KEPA), P.O. Box 24395, Safat 13104, Kuwait
2
Centre for Environment, Fisheries and Aquaculture Science (Cefas), Weymouth Laboratory, Barrack Road, Weymouth DT4 8UB, Dorset, UK
3
Environment and Life Science Research Centre, Kuwait Institute for Scientific Research, P.O. Box 24885, Safat 13109, Kuwait
4
Department of Earth & Environmental Sciences, Faculty of Science, Kuwait University, P.O. Box 5969, Safat 13060, Kuwait
*
Author to whom correspondence should be addressed.
Sustainability 2022, 14(18), 11325; https://doi.org/10.3390/su141811325
Submission received: 3 August 2022 / Revised: 24 August 2022 / Accepted: 6 September 2022 / Published: 9 September 2022
(This article belongs to the Section Sustainable Oceans)
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Abstract

:
This study presents antimicrobial resistance (AMR) in Escherichia coli derived from marine sediment in Kuwait. In total, 395 isolates of E. coli obtained were screened for their potential resistance to five commonly deployed frontline antibiotics by using the disk diffusion method. The results demonstrated widespread resistance across all the sites and in 98% of isolates. The highest counts were recorded in the sediment collected from sites near outfalls associated with local hospitals, where 58% of isolates screened displayed resistance to different antibiotic classes. The resistance was highest to ampicilin (beta-lactame class) > cefpodoxime (3rd generation cephalosporin class) > ciprofloxacin (flouroqunolone class) with AMR observance at 95%, 67% and 50% respectively. The latter two are wide spectrum antibiotics heavily used in Kuwait. This study demonstrates the presence of AMR bacteria in Kuwait’s marine environment, suggesting a need for environmental surveillance for AMR to be adopted as part of a One Health approach to Kuwait’s developing AMR national action plan.

1. Introduction

Globally, antimicrobial resistance (AMR) has emerged as a significant threat to both animal and human health. The World Health Organization (WHO) has ranked AMR as one of the top 10 global public health threats humanity faces [1]. The issue spans to all classes of natural and synthetic antibiotics; the phenomenon has led to calls for a coordinated ‘One Health’ approach across the human, environment and animal health sectors [2,3,4]. With improved healthcare coverage, medications including antibiotics have been widely used to treat various diseases among humans and animals [5,6]. Indiscriminate medication use and poor waste regulation can adversely impact the microbial community [7,8,9,10,11]. With recent efforts directed toward assessing AMR, it has become evident that the abundance and diversity of antibiotic resistance in the environment has been underestimated, with potentially widespread ramifications for both human and animal health [11]. Studies have highlighted the marine environment’s role in accentuating drug resistance since it has a high concentration of microbes and is a sink for pharmaceuticals and other pollutants discharged from wastewater treatment plants [12,13,14]. Land-based pollution, especially wastewater effluent discharge, is impacting coastal zones [15,16,17,18,19,20,21]. The wastewater matrix is enriched with a wide array of chemical pollutants, including antimicrobials, metals [22,23] and biocides [24,25,26,27], some of which can trigger AMR [28]. A recently published work concluded that pharmaceutical concentrations, including antibiotics, derived from Kuwait’s coastal water [29] exceed those reported from the Spanish coast, the Hong Kong harbor, the Bohai and the Yellow seas [18].
Some recent reports have reaffirmed that sediments are reservoirs of antibiotic resistance genes (ARGs) that have the potential to drive their emergence in marine environments [28,30,31,32,33,34,35,36]. It is relevant to mention the frequent gremlin of sewage discharge in Kuwait Bay and along the Gulf coast [16,18,19,29,37,38,39,40,41,42,43,44,45,46,47].
Sediments have been suggested as a potential bacterial habitat and a source of water-borne fecal coliforms and E. coli [48]. The resuspension of these sediments can create elevated E. coli concentrations in water [48]. The coastal waters of Kuwait have considerable resuspension due to strong currents in the shallow coastal regions [49] resulting in high suspended particulate matter [50].
The emergence of AMR genes and bacteria is reported in the Gulf Cooperative Council (GCC) region, [13,51,52,53], but little attention has been paid to the role of the marine environment as an AMR sink. The AMR bacteria in fish, turtles and seawater have been reported from locations near to sewage discharges and in the effluent in Oman [54,55]. The presence of AMR has also been detected in seawater and biota (Venus clam, Circenita callipyga) samples collected from Kuwait’s coastline [52,53,56] and coastal waters of Bahrain, UAE and Oman [52]. However, in Kuwait, research into AMR has been predominantly restricted to clinical settings, with high levels of resistance observed against a range of front line antibiotics [57,58]. It has become increasingly recognized that the ability to survey the prevalence and characteristics of resistance in environmental bacteria is essential as part of a One Health approach to have a full understanding of AMR and the strategies required to curb its spread [59].
This study attempts to build the information base on AMR presence in the marine environment and report information on the prevalence of AMR within bacterial isolates collected from marine sediments from sites along Kuwait’s coastal area considering E. coli, an indicator for AMR surveillance [60,61]. E. coli has been studied in detail for its pathogenic potential and antimicrobial susceptibility [62,63]. Recently, the five pathotypes of diarrheagenic E. coli (DEC)-(enteropathogenic E. coli (EPEC), enterotoxigenic E. coli (ETEC), enteroinvasive E. coli (EIEC), shiga toxin-producing E. coli (STEC) and enteroaggregative E. coli (EAEC) and a relatively high prevalence of the extra-intestinal pathogenic E. coli (ExPEC) were observed in raw sewage in Kuwait [20]. E. coli could pose public health implications for using coastal waters for recreation due to its potential to cause intestinal and extra-intestinal infections [64], keeping in mind that approximately 25% of the sewage in Kuwait remains untreated and is discharged into the sea.

2. Materials and Methods

In total, 395 isolates of E. coli were isolated from sediment and screened for resistance against five antibiotics representing different classes of antibiotics using the disk diffusion method.

2.1. Sampling Sites

Sediment samples for AMR screening were collected during the winter (December 2019) from sites along the Kuwait coastline by grab sample. These sites were selected based on a priori knowledge of emergency outfalls and recreational beaches within Kuwait Bay. Sediment samples were collected from nine sites near known effluent discharge points (Al-Ghazali, Maternity Hospital, Chest Hospital, Sulaibkhat Bay Doha East and Doha West) and recreational beaches (Kuwait Petroleum Corporation (KPC), Sulaibkhat Sports club and Jabber city) in Kuwait Bay (Figure 1).

2.1.1. Sample Collection

In brief, grab samples were collected from each site (covering 10–15 cm deep sediment profile) using a sterile shovel and placed into pre-cleaned containers labeled with location name, date, and time of collection and were stored in ice. The holding time for these samples was less than six hours before they were transported to Kuwait Environment Public Authority (KEPA) laboratories. At each of the sampling sites, water temperature, pH and salinity were recorded using a portable multi-probe water quality instrument (Hanna instruments model no. HI 9828, Smithfield, RI, USA).

2.1.2. Enumeration of E. coli

Faecal coliform and E. coli were determined at each location to assess the level of sewage contamination at the site using a membrane filter technique [65]. At each site, 10 samples were collected and from each sample, and 1 g of sediment was diluted in 9 mL of 0.1% peptone water. Different volumes of 0.1, 1, 3 and 10 mL from serial dilutions (10−1, 10−3, 10−5) were filtered through 47 mm diameter, 0.45 µm pore size, nitrocellulose membrane filters (Millipore, Molsheim, France) and triplicate plates were prepared. Aseptic techniques were employed at all times and during subsequent procedures. For the feacal coliform enumeration, filter papers were placed separately on m-FC agar plates (OXOID, Basingstoke, Hampshire, UK) with 10 mL 1% Rosolic acid in 0.2 N NaOH, pH 7.4. The plates were incubated at 35 ± 2 °C for 18 h. The mean number of faecal bacteria and E. coli in seawater were expressed in colony-forming unities (CFU) per 100 mL.
For the isolation of E. coli from the sediment samples, the filter membrane was placed on a plate of Tryptone Bile X-Glucuronide Medium, TBX agar (OXOID, Basingstoke, Hampshire, UK), and incubated, inverted, at 30 °C for 4 ± 0.25 h then transferred to an incubator at 44 ± 0.5 °C and incubated for 21 ± 3 h. The number of positive (blue-green) (β-glucuronidase) colonies on each plate was counted [65]. These were regarded as E. coli. The combination of media selectivity, incubation temperature and the specificity of β-glucuronidase was sufficient for most practical confirmatory purposes. Blue-green colonies were picked off the plates using sterile loops, inoculated onto nutrient agar (OXOID, Basingstoke, Hampshire, UK) slants and incubated overnight at 44 °C. Blank and positive control (E. coli ATCC25922) samples were analysed in tandem with the field samples for quality control.

2.1.3. Antimicrobial Susceptibility Testing

The process for AMR screening was conducted using the disk diffusion method following the European Committee on Antimicrobial Susceptibility Testing (EUCAST) disk diffusion for antimicrobial susceptibility testing version 7.0. In total, 395 isolated E. coli were analyzed and screened for AMR by measuring the zone of inhibition diameter for interpretation. Isolates were considered resistant according to standards suggested by (EUCAST version 7.0). The test of each isolate was carried out in triplicate to make sure of the AMR phenotype pattern. Multidrug resistance was defined when an isolate shows the resistant phenotype to at least three or more classes of antibiotic [66]. Blank and positive control (E. coli ATCC25922) samples were analysed with the field samples for quality assurance and quality control.
Cultures were purified using further subculture steps before antimicrobial susceptibility testing was carried out. Suspension was prepared by removing each colony by cotton swap and then emulsifying it in sterile saline. The cultures were vortexed, and the concentration was adjusted to 0.5 McFarland (Hardy diagnostic, Santa Maria, CA, USA). A turbidity standard blank and positive control (E. coli ATCC25922) samples were analysed with the field samples for quality control. The Mueller-Hinton (MH) medium (OXOID, Basingstoke, Hampshire, UK), plates were inoculated by swabbing in three directions and evenly spread over the agar surface ensuring that there were no gaps between streaks. The five antibiotic disks were applied to the semi-dried (within 15 min of inoculation) inoculated plates. The antibiotics used were selected based on their mode of action, history of use, resistance and clinical relevance. The tested antibiotics were: ceftriaxone 30 µg (CRO) [S ≥ 25, R < 22], cefepime 30 µg (FEB 30) [S ≥ 14, R < 14], ampicillin 10 µg (AMP) [S ≥ 14, R < 14], ciprofloxacin 5 µg (CIP) [S ≥ 25, R < 22] and cefpodoxime 10 µg (CPD) [S ≥ 21, R < 21]. The plates were incubated at 35 ± 2 °C in for 18 ± 2 h. The diameter of the inhibition zones was measured and the results were interpreted as susceptible or resistant according to standards suggested by The European Committee on Antimicrobial Susceptibility Testing [67].

3. Results

The physical–chemical parameters (pH, water temperature and salinity) were measured across the sampling sites salinity (Mean 36 ± 2.0), water temperatures (mean 17.2 °C ± 2.0) and pH (mean 8.2 ± 0.2). The mean numbers of faecal coliform and E. coli in the sediments were expressed as colony-forming unities (CFU) per 100 mL (Table 1). The feacal coliform colonies were counted from all sites, which could give a sign of deterioration in microbial pollution in the sediment. The Sulaibkhat Bay, Maternity hospital, Chest Hospital, Al-Ghazali, Doha East and KPC recorded high numbers of faecal coliform among the sites (p-value < 0.01) (Table 1).
Table 2 shows the percentage of E. coli in the samples collected from the nine sites against the five tested antibiotics. Performing ANOVA tests in IBM SPSS statistics 25 applications on these data showed the significance level of all data (p < 0.05). The resistance patterns were widespread and crossed over all the sites. Among the sites, the counts of isolated AMR E. coli were significantly high in the samples collected near Chest Hospital (n = 106) and Maternity Hospital (n = 98) sites. Across the sites, the percentage of resistance observed in the isolates was highest against ampicillin followed by cefpodoxime. The E. coli derived from recreational beaches (KPC, Sulaibkhat Sports Club, and Jabber City) showed that resistance against the tested antibiotics might be attributed to the current water circulation and horizontal gene transfer beyond the point of sewage discharge. Due to accessibility issues, it was difficult to obtain samples from the Doha East and Doha West sites; hence the number of samples was limited [68].
The E. coli resistance patterns against all five tested antibiotics showed the highest levels of resistance to ampicillin with a value of 95% (n = 375) followed by cefpodoxime at 67% (n = 267), ciprofloxacin at 50% (n = 200), ceftriaxone at 41% (n = 163) and the lowest resistance profile was against cefepime with a value of 35% (n = 137) (p-value < 0.05), ANOVA, IBM SPSS 25 (North Harbour Portsmouth, Hampshire, UK) application (Figure 2). Among the total screened E. coli isolates (n = 395), only 2% (n = 8) were susceptible to all of the tested antibiotics that represent the different four classes of antibiotics (ceftriaxone and cefpodoxime are one class, 3rd third-generation cephalosporin) (Figure 3). A total of 17.2% (n = 68) were resistant to one class, and 27.6% (n = 109) were resistant to two antibiotics belonging to two different classes.
In this study, the dominant resistance pattern was to the three different antibiotics related to three different classes, and 33.4% (n = 132) and 19% (n = 78) were resistant to four antibiotics. Consequently, 53% of the isolates could be classified as Multi-drug resistant E. coli (MDR) as they were resistant to at least three different classes (Figure 3).

4. Discussion

Declining water quality driven by microbial pollution is one of the many vital challenges Kuwait’s marine environment is facing, and a growing number of studies are highlighting the scale of sewage pollution entering the country’s coastal waters [18,19,20,29,45,46,69]. One of the primary sources of AMR bacteria in the marine environment is sewage discharge, either from wastewater treatment plants (WWTPs) or direct inputs [70]. The WHO recommends integrated surveillance, where E. coli from different sectors is screened for AMR to help build a complete picture of transmission pathways and the likely risks, while monitoring the effectiveness of intervention strategies [71].
In this study, faecal coliform and E. coli were documented in all sites, and coliform counts ranged from 7.5 × 104–1 × 105 CFU/100 mL at most sites (six sites), which could be an indicator of untreated sewage discharge into Kuwait Bay by some acts such as illegal connections to stormwater outlets or via official releases dues to lack of treatment capacity.
However, there are no guidelines for sediment microbial quality to be followed in Kuwait’s Environmental Law. These findings further support the studies where sediment in coastal areas indicates a chronic sewage pollution problem in Kuwait Bay [19,20]. There is sufficient evidence of other pollutants with a known antimicrobial mode also being discharged with effluent through these outfalls [18,72]. As per published information, around 75% of the sewage in Kuwait is treated [73]. This study highlights that the presence of strains of E. coli in these sediments shows inapt sewage treatment processes [74]. The presence of faecal coliform and pharmaceutical compounds are reliable indications of fugitive discharges into the marine environment, which was further confirmed by the presence of extra-intestinal pathogenic E. coli in high concentrations [75].
The resistance patterns were widespread and cross over all the sites. In total, 395 E. coli strains were isolated from the sediment and screened for their potential resistance. Overall, the screening indicated that 98% of E. coli isolates were resistant to at least one antibiotic. The large spatial distribution of AMR E. coli exacerbates the concern that this is no longer restricted to emergency outfalls. The need to investigate pharmaceutical concentrations in the marine environment and the role of metals and biocides leading to AMR needs to be considered under the One Health Approach.
The results showed that 53% of the isolates were multi-drug resistant (MDR), displaying resistance to a minimum of three antibiotic classes. The findings were similar to that previously reported (35–56.6%) for seawater- and biota-isolated E. coli [13,52,56]. These findings demonstrate that AMR was present in all matrixes (water, sediment and biota) of Kuwait’s marine environment, similar to sediments collected from the Msimbazi river basin in Tanzania [76]. The E. coli in the sediment were highly resistant to ciprofloxacin (39.7%) and trimethoprim/sulfamethoxazole (38%), along with a high degree of multidrug resistance to antibiotics including the quinolone and carbapenem classes [76]. Similar findings have also been reported for isolates collected from aquaculture farms in Zhanjiang, China, where E. coli sampled from water, soil and sediment (n = 90) showed 100% resistance to multi-antimicrobial drugs [77].
Inferences can also be drawn from South-West Nigeria, where 100% of isolated E. coli (n = 98) from fish farms showed resistance to at least one antibiotic and were also metal-tolerant [78]. Linkages can also be established with a higher metal load [21] in sediments of the Kuwait marine area in promoting AMR.
In this current study, the numbers of resistant E. coli observed at the Chest hospital and Maternity hospitals sites were high, with resistance observed across the antibiotics tested. As expected, ampicillin resistance (95%) dominated the AMR profile across all the sites. These findings were higher than the previous reports of E. coli derived from Kuwait seawater and the biota sampled across both summer and winter seasons displayed high resistance rates (70% and 69%, respectively) to ampicillin [56]. A recently published study also reported 56.5% resistance to ampicillin for E. coli isolated from seawater samples collected in Kuwait. However, across the Gulf region, the total E. coli isolates collected displayed lower rates (29.6%) of ampicillin resistance [52]. Ampicillin (a class of aminoglycoside) is one of the older generations of drugs, and has the highest antibiotic resistance due to its long history of usage since 1930 [79]. It is also highly consumed in hospital settings, leading to widespread resistance [80].
The third generation class antibiotic cefpodoxime displayed the second-highest resistance profile (67%) in this current study with high resistance levels recorded in samples collected close to the Chest Hospital outlet. This could indicate that wastewater effluent from the hospital is reaching the local coastal waters, as cefpodoxime is used to treat bronchitis-related diseases. These values were higher than the values in seawater (25.1%) and biota (23.6%) previously reported for Kuwait [56]. Again, similar to the studies of Al Sarawi et al. [56] and Light et al. [52] sediment-derived E. coli also showed high rates of resistance to flouroquenolone-class ciprofloxacin (50%), third generation cephalosporin ceftriaxone (41%) and the fourth generation cephalosporin, cefepime (35%). Both classes of cephalosporin and quinolone are classified as wide-spectrum antibiotics used in the treatment of urinary tract infections (UTI) [81].
In the GCC region, previous discussion/opinion articles have highlighted the regional need for coordination to tackle AMR emergence due to generous healthcare and the discharge of effluent into the coastal waters. The GCC region is particularly susceptible to AMR threats due to demographic and environmental factors [13,51]. The data presented here confirmed that Kuwait’s marine environment is harboring antibiotic-resistant bacteria which are likely to have been derived from the input of wastewater.

5. Conclusions

To our knowledge, there are very few studies on the prevalence of AMR bacteria in the costal sediments of the Gulf region. This study contributes to our broader understanding of drug resistance in the marine environment. It also sheds light on the critical role the aquatic environment could play in spreading AMR in the region. Critical knowledge gaps remain, and more studies with an environmental perspective are needed to improve understanding of the AMR risks in Kuwait, including sources, other bacterial species, genotypic screening, transfer mechanisms and pathways. Further information, such as antibiotic dosing statistics, wastewater discharge sources and both clinical and environmental microbiological data, would help to determine the risks posed to both human and ecosystem health by these bacteria entering marine systems. Moreover, this study has highlighted the feasibility of developing and implementing coastal and marine environmental AMR surveillance and monitoring programs, which could be tailored to the existing routine microbial monitoring program. There is an eminent need to embed a One Health approach into Kuwait’s national action plan, which is currently under active consideration.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su141811325/s1.

Author Contributions

Conceptualization, H.A.A.-S., S.U.; Data curation, H.A.A.-S., A.B.N. and M.A.A.-S.; Methodology, H.A.A.-S. and A.B.N.; Supervision, H.A.A.-S. and M.A.A.-S.; Writing—original draft, H.A.A.-S.; Writing—review & editing, H.A.A.-S., B.P.L. and S.U. All authors have read and agreed to the published version of the manuscript.

Funding

Authors are thankful to Kuwait University for funding the study ISBN:978-99906-1-764-1.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data is available as Supplementary Materials to this publication.

Conflicts of Interest

The authors declare there is no conflict of interest.

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Figure 1. Map of sampling locations around the coastline of Kuwait bay. The sites were: (1) Kuwait Petroleum Corporation (KPC), (2) Al-Ghazali, (3) Chest hospital, (4) Maternity hospital, (5) Sulaibkhat Bay, (6) Sulaibkhat Sports club, (7) Jabber city, (8) Doha east and (9) Doha west.
Figure 1. Map of sampling locations around the coastline of Kuwait bay. The sites were: (1) Kuwait Petroleum Corporation (KPC), (2) Al-Ghazali, (3) Chest hospital, (4) Maternity hospital, (5) Sulaibkhat Bay, (6) Sulaibkhat Sports club, (7) Jabber city, (8) Doha east and (9) Doha west.
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Figure 2. The resistance pattern of E. coli derived from sediment against the tested antibiotics.
Figure 2. The resistance pattern of E. coli derived from sediment against the tested antibiotics.
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Figure 3. The percent of E. coli isolates resistant to antibiotic classes in sediment samples collected from Kuwait’s marine environment.
Figure 3. The percent of E. coli isolates resistant to antibiotic classes in sediment samples collected from Kuwait’s marine environment.
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Table
Table 1. The number of faecal coliform colonies in sediment samples obtained from each location (mean values and standard deviation.), CFU = Colony Forming Unit/100 mL.
Table 1. The number of faecal coliform colonies in sediment samples obtained from each location (mean values and standard deviation.), CFU = Colony Forming Unit/100 mL.
Number of LocationName of LocationNo. of Colonies CFU/100 mL
Mean ± SD
1KPC9 × 103 ± 0.4 × 103
2Al-Ghazali7.5 × 104 ± 1.5 × 104
3Maternity Hospital1.06 × 105 ± 0.2 × 105
4Chest Hospital9.8 × 104 ± 0.21 × 104
5Sulaibkhat Bay54 × 104 ± 0.2 × 104
6Sulaibkhat Sport Club367 ± 2
7Jaber City967 ± 2.1
8Doha East8.4 × 103 ± 1.4 × 103
9Doha West167 ± 1.5
Table
Table 2. The percent of E. coli derived from Kuwait’s marine environment (sediment) from nine sites against the five tested antibiotics.
Table 2. The percent of E. coli derived from Kuwait’s marine environment (sediment) from nine sites against the five tested antibiotics.
Percent of Resistant E. coli
Site No.Antibiotics SitesCeftriaxoneCefepimeAmpicillinCiprofloxacinCefpodoxime
1KPC (n = 9)0010033.00
2Al-Ghazali (n = 75)3628965179
3Chest Hospital (n = 106)4442.5994370.75
4Maternity Hospital (n = 98)5354995863.2
5Sulaibkhat Bay (n = 54)44.420.496.370.463
6Sulaibkhat Sport Club (n = 10)30401005070
7Jabber City (n = 29)27.513.765.52455
8Doha East (n = 9)11.1010033.3100
9Doha West (n = 5)20010060100
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Al-Sarawi, H.A.; Najem, A.B.; Lyons, B.P.; Uddin, S.; Al-Sarawi, M.A. Antimicrobial Resistance in Escherichia coli Isolated from Marine Sediment Samples from Kuwait Bay. Sustainability 2022, 14, 11325. https://doi.org/10.3390/su141811325

AMA Style

Al-Sarawi HA, Najem AB, Lyons BP, Uddin S, Al-Sarawi MA. Antimicrobial Resistance in Escherichia coli Isolated from Marine Sediment Samples from Kuwait Bay. Sustainability. 2022; 14(18):11325. https://doi.org/10.3390/su141811325

Chicago/Turabian Style

Al-Sarawi, Hanan A., Afrah B. Najem, Brett P. Lyons, Saif Uddin, and Mohammad A. Al-Sarawi. 2022. "Antimicrobial Resistance in Escherichia coli Isolated from Marine Sediment Samples from Kuwait Bay" Sustainability 14, no. 18: 11325. https://doi.org/10.3390/su141811325

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