Characterization of Carbapenem-Resistant Enterobacteriaceae with High Rate of Autochthonous Transmission in the Arabian Peninsula

Sonnevend, Ágnes; Ghazawi, Akela; Hashmey, Rayhan; Jamal, Wafaa; Rotimi, Vincent O.; Shibl, Atef M.; Al-Jardani, Amina; Al-Abri, Seif; Tariq, Waheed Uz Zaman; Weber, Stefan; Pál, Tibor

doi:10.1371/journal.pone.0131372

Cited by 82 publications

(108 citation statements)

References 42 publications

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“…In one study which aimed to establish the role of local transmission versus possible pathogen import due to global travel, it was determined that patients carrying bla NDM-1 -positive K. pneumoniae had no prior documented foreign exposure, hence suggesting a high rate of autochthonous infections (52). Even though the isolation frequency for E.…”

Section: Discussionmentioning

confidence: 99%

Isolation and Characterization of NDM-Positive Escherichia coli from Municipal Wastewater in Jeddah, Saudi Arabia

Mantilla‐Calderon

Jumat

Wang

et al. 2016

Antimicrob Agents Chemother

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bThe emergence of resistance to last-resort antibiotics is a public health concern of global scale. Besides direct person-to-person propagation, environmental pathways might contribute to the dissemination of antibiotic-resistant bacteria and antibiotic resistance genes (ARGs). Here, we describe the incidence of bla NDM-1 , a gene conferring resistance to carbapenems, in the wastewater of the city of Jeddah, Saudi Arabia, over a 1-year period. bla NDM-1 was detected at concentrations ranging from 10 4 to 10 5 copies/m 3 of untreated wastewater during the entire monitoring period. These results indicate the ubiquity and high incidence of bla NDM-1 in the local wastewater. To track the bacteria carrying bla NDM-1 , we isolated Escherichia coli PI7, a strain of sequence type 101 (ST101), from wastewater around the Hajj event in October 2013. Genome sequencing of this strain revealed an extensive repertoire of ARGs as well as virulence and invasive traits. These traits were further confirmed by antibiotic resistance profiling and in vitro cell internalization in HeLa cell cultures. Given that this strain remains viable even after a certain duration in the sewerage, and that Jeddah lacks a robust sanitary infrastructure to fully capture all generated sewage, the presence of this bacterium in the untreated wastewater represents a potential hazard to the local public health. To the best of our knowledge, this is the first report of a bla NDM-1 -positive E. coli strain isolated from a nonnosocomial environment in Saudi Arabia and may set a priority concern for the need to establish improved surveillance for carbapenem-resistant E. coli in the country and nearby regions.

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Section: Discussionmentioning

confidence: 99%

Isolation and Characterization of NDM-Positive Escherichia coli from Municipal Wastewater in Jeddah, Saudi Arabia

Mantilla‐Calderon

Jumat

Wang

et al. 2016

Antimicrob Agents Chemother

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“…QMRA was performed to assess the risks associated with K. pneumoniae and A. baumannii because these two microbial agents have been reported to be common causative agents in nosocomial and non‐nosocomial infections in Saudi Arabia (Sonnevend et al, ; Uz Zaman et al, ; Yezli, Shibl, Livermore, & Memish, ). The two bacteria were isolated at different frequencies in the three types of examined produce.…”

Section: Resultsmentioning

confidence: 99%

Varying occurrence of extended‐spectrum beta‐lactamase bacteria among three produce types

Toh

Bokhari

Kutbi

et al. 2017

Journal of Food Safety

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A monitoring effort that spanned across 1.5 years was conducted to examine three types of produce‐associated microbiota. The average amount of antibiotic‐resistant bacteria recovered from lettuce, tomato, and cucumber was 1.02 × 1010, 2.05 × 107, and 4.78 × 109 cells per 50 g of each produce, respectively. A total of 480 bacterial isolates were obtained and identified from their 16S rRNA genes, revealing isolates that were ubiquitously recovered from all three types of produce. However, sporadic presence of Klebsiella pneumoniae and Acinetobacter baumannii was detected on lettuce and cucumbers but not tomatoes. End‐point PCR revealed that the K. pneumoniae and A. baumannii isolates were positive for genes encoding extended spectrum beta‐lactamase. Whole genome sequencing of two of the K. pneumoniae isolates further suggested the presence of the blaCTX‐M‐15 gene in a conjugative plasmid, as well as other antibiotic resistance genes and virulence‐associated traits in either conjugative plasmids or the chromosomal genome. Quantitative microbial risk assessment indicated varying levels of ingestion risk associated with different types of produce. In particular, the risk arising from ESBL‐positive K. pneumoniae in lettuce, but not in cucumbers or tomatoes, was higher than the acceptable annual risk of 10−4. Practical applications Three types of vegetables were sampled and evaluated over 1.5 years to determine differences in their associated bacterial isolates. Particular emphasis was placed on identifying pathogenic strains that were positive for extended spectrum beta‐lactamase (ESBL). Quantitative estimates of the microbial risk associated with the ESBL‐positive pathogens showed that different produce types may incur varying levels of ingestion risk. Most of the currently reported ESBL‐positive bacterial isolates have been identified in nosocomial environments. However, the carriage of such drug‐resistant bacteria in vegetables suggests a possible connection between our daily diet and human health.

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“…Enterobacteriaceae possessing two carbapenemases have previously been observed worldwide (16) and in the region as well (6,17,18). It is of particular concern that representatives of the K. pneumoniae ST147 clone, well known for its epidemic potential (4,6), not only are present in the UAE as dual-carbapenemase-producing isolates but also develop resistance to the last-resort antibiotic, colistin, by insertion of a functional carbapenemase gene into the mgrB gene.…”

Section: Pan-resistant Klebsiella Pneumoniae Clone In the Uaementioning

confidence: 99%

“…It is of particular concern that representatives of the K. pneumoniae ST147 clone, well known for its epidemic potential (4,6), not only are present in the UAE as dual-carbapenemase-producing isolates but also develop resistance to the last-resort antibiotic, colistin, by insertion of a functional carbapenemase gene into the mgrB gene. Apart from the earlier report on MS6671 (12), a similar ISEcp1-driven insertional mutation of mgrB in K. pneumoniae has been observed in a single isolate in France, but in that case, an extended-spectrum betalactamase gene (bla CTX-M-15 ) was coded on the insertion, and the strain remained susceptible to an array of antibiotics (19).…”

Section: Pan-resistant Klebsiella Pneumoniae Clone In the Uaementioning

confidence: 99%

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Multihospital Occurrence of Pan-Resistant Klebsiella pneumoniae Sequence Type 147 with an IS Ecp1 -Directed bla _OXA-181 Insertion in the mgrB Gene in the United Arab Emirates

Sonnevend

Ghazawi

Hashmey

et al. 2017

Antimicrob Agents Chemother

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The emergence of pan-resistant Klebsiella pneumoniae strains is an increasing concern. In the present study, we describe a cluster of 9 pan-resistant K. pneumoniae sequence type 147 (ST147) isolates encountered in 4 patients over nearly 1 year in 3 hospitals of the United Arab Emirates (UAE). The isolates exhibited highly similar genotypes. All produced chromosomally encoded OXA-181, and the majority also produced the NDM-5 carbapenemase. As with the previously described single isolate from the UAE, MS6671, the mgrB was disrupted by a functional, ISEcp1-driven bla OXA-181 insertion causing resistance to carbapenems. The mutation was successfully complemented with an intact mgrB gene, indicating that it was responsible for colistin resistance. bla NDM-5 was located within a resistance island of an approximately 100-kb IncFII plasmid carrying ermB, mph(A), bla TEM-1B , rmtB, bla NDM-5 , sul1, aadA2, and dfrA12 resistance genes. Sequencing this plasmid (pABC143-NDM) revealed that its backbone was nearly identical to that of plasmid pMS6671E from which several resistance genes, including bla NDM-5 , had been deleted. More extensive similarities of the backbone and the resistance island were found between pABC143C-NDM and the bla NDM-5 -carrying IncFII plasmids of two K. pneumoniae ST147 isolates from South Korea, one of which was colistin resistant, and both also produced OXA-181. Notably, one of these strains was isolated from a patient transferred from the UAE. Our data show that this pan-resistant clone has an alarming capacity to maintain itself over an extended period of time and is even likely to be transmitted internationally.

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Characterization of Carbapenem-Resistant Enterobacteriaceae with High Rate of Autochthonous Transmission in the Arabian Peninsula

Cited by 82 publications

References 42 publications

Isolation and Characterization of NDM-Positive Escherichia coli from Municipal Wastewater in Jeddah, Saudi Arabia

Isolation and Characterization of NDM-Positive Escherichia coli from Municipal Wastewater in Jeddah, Saudi Arabia

Varying occurrence of extended‐spectrum beta‐lactamase bacteria among three produce types

Multihospital Occurrence of Pan-Resistant Klebsiella pneumoniae Sequence Type 147 with an IS Ecp1 -Directed bla _OXA-181 Insertion in the mgrB Gene in the United Arab Emirates

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Characterization of Carbapenem-Resistant Enterobacteriaceae with High Rate of Autochthonous Transmission in the Arabian Peninsula

Cited by 82 publications

References 42 publications

Isolation and Characterization of NDM-Positive Escherichia coli from Municipal Wastewater in Jeddah, Saudi Arabia

Isolation and Characterization of NDM-Positive Escherichia coli from Municipal Wastewater in Jeddah, Saudi Arabia

Varying occurrence of extended‐spectrum beta‐lactamase bacteria among three produce types

Multihospital Occurrence of Pan-Resistant Klebsiella pneumoniae Sequence Type 147 with an IS Ecp1 -Directed bla OXA-181 Insertion in the mgrB Gene in the United Arab Emirates

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Product

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Multihospital Occurrence of Pan-Resistant Klebsiella pneumoniae Sequence Type 147 with an IS Ecp1 -Directed bla _OXA-181 Insertion in the mgrB Gene in the United Arab Emirates