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Detection of CTX-M-15 beta-lactamases in Enterobacteriaceae causing hospital- and community-acquired urinary tract infections as early as 2004, in Dar es Salaam, Tanzania

  • Joel Manyahi1, 2Email author,
  • Sabrina J. Moyo1, 2,
  • Marit Gjerde Tellevik3,
  • Faustine Ndugulile2,
  • Willy Urassa2,
  • Bjørn Blomberg1, 3 and
  • Nina Langeland1, 3
BMC Infectious DiseasesBMC series – open, inclusive and trusted201717:282

DOI: 10.1186/s12879-017-2395-8

Received: 18 February 2017

Accepted: 11 April 2017

Published: 17 April 2017

Abstract

Background

The spread of Extended Spectrum β-lactamases (ESBLs) among Enterobacteriaceae and other Gram-Negative pathogens in the community and hospitals represents a major challenge to combat infections. We conducted a study to assess the prevalence and genetic makeup of ESBL-type resistance in bacterial isolates causing community- and hospital-acquired urinary tract infections.

Methods

A total of 172 isolates of Enterobacteriaceae were collected in Dar es Salaam, Tanzania, from patients who met criteria of community and hospital-acquired urinary tract infections. We used E-test ESBL strips to test for ESBL-phenotype and PCR and sequencing for detection of ESBL genes.

Results

Overall 23.8% (41/172) of all isolates were ESBL-producers. ESBL-producers were more frequently isolated from hospital-acquired infections (32%, 27/84 than from community-acquired infections (16%, 14/88, p < 0.05). ESBL-producers showed high rate of resistance to ciprofloxacin (85.5%), doxycycline (90.2%), gentamicin (80.5%), nalidixic acid (84.5%), and trimethoprim-sulfamethoxazole (85.4%). Furthermore, 95% of ESBL-producers were multi-drug resistant compared to 69% of non-ESBL-producers (p < 0.05). The distribution of ESBL genes were as follows: 29/32 (90.6%) bla CTX-M-15, two bla SHV-12, and one had both bla CTX-M-15 and bla SHV-12. Of 29 isolates carrying bla CTX-M-15, 69% (20/29) and 31% (9/29) were hospital and community, respectively. Bla SHV-12 genotypes were only detected in hospital-acquired infections.

Conclusion

bla CTX-M-15 is a predominant gene conferring ESBL-production in Enterobacteriaceae causing both hospital- and community-acquired infections in Tanzania.

Keywords

ESBL Urinary tract infections Tanzania

Background

Extended Spectrum β-lactamases (ESBLs) have been observed in virtually all species of the family Enterobacteriaceae. Spread of ESBL-producing strains from general wards to intensive care units (ICU) and into the community can contribute to the further propagation of these resistant strains [1].

ESBLs are responsible for resistance against beta-lactam antibiotics such as penicillins, cephalosporins, monobactams and sometimes also carbapenems [2]. Organisms carrying ESBL enzymes often display co-resistance to other antibiotics including aminoglycosides, quinolones, trimethoprim-sulfamethoxazole and tetracycline [3, 4]. Spread of ESBL-producing bacterial isolates in the community has made empirical treatment of infections more difficult, and narrows the treatment options to expensive antibiotics like colistin and carbapenems.

Recent studies in Africa and Europe have found substantial increase in ESBL-producing Gram-negative bacteria causing community urinary tract infections, particularly harboring the bla CTX-M-15 allele [57]. Previously, studies in Tanzania have detected a substantial amount of ESBL-producing bacteria among the inpatients in intensive care and pediatric units in Tanzania [8, 9]. However, little is known regarding the frequency of ESBL-producers and ESBL genes in community-acquired (CA) and hospital-acquired (HA) urinary tract infections in Tanzania. A more recent study found a predominance of the bla CTX-M-15 genotype from human feces in a community setting [10].

Previous studies performed at Muhimbili National Hospital documented the presence of ESBL-producers, predominantly of the bla CTX-M-15 genotype, in hospital-acquired infections [8, 9]. Therefore, we decided to examine bacterial isolates collected prospectively for a period of six months in 2004 at Muhimbili National Hospital in Dar es Salaam, aiming at investigating whether ESBL-producers were present in the community setting, when hospital-acquired bla CTX-M-15 -producers were first reported in Tanzania. We also aimed to compare the ESBL genotypes circulating in the community to those found in the hospital setting.

Methods

Study setting and patient population

The study was conducted at Muhimbili National Hospital (MNH, Dar es Salaam, Tanzania. MNH is a tertiary health care facility that serves a population of about 4 million residents. The Department of Microbiology, MNH, receives samples from inpatients in the hospital wards, from the outpatient clinics and private health facilities in the city. Included in the study were samples from inpatients and outpatients with urinary tract infections seen at MNH between June 2004 and January 2005. Hospital-acquired infections were defined as those occurring in inpatients admitted at MNH for at least 72 h. Community-acquired infections were defined as those occurring in patients attending outpatient clinics at MNH. A UTI was defined as a positive urine culture of ≥105 CFU/ml of pure bacterial growth.

Clinical isolates

A total of 172 isolates of Enterobacteriaceae were collected, 84 and 88 isolates from hospital and community patients, respectively. All isolates were identified to the species level using established conventional procedures, the API 20E system (bioMérieux SA, Marcy l‵Etoile, France) or the Vitek 2 system (BioMérieux, Inc., Durham, N.C).

Antimicrobial susceptibility testing

All isolates were tested for antimicrobial susceptibility using the disk diffusion method according to the Clinical & Laboratory Standards Institute’s guidelines [11]. The antimicrobials tested included amoxicillin/clavulanic acid (20/10μg), gentamicin (10μg), chloramphenicol (30μg), trimethoprim/sulfamethoxazole (1.25/23.75μg), doxycycline (30μg), nitrofurantoin(30μg), nalidixic acid (30μg), imipenem (10μg), ciprofloxacin (5μg), cefotaxime (30μg), ceftriaxone(30μg) and ceftazidime (30μg). Multidrug-resistant (MDR) bacteria were those bacteria which showed resistance to three or more classes of antimicrobial agents [12], classes including β-lactam/β-lactamase inhibitors, cephalosporins (ceftriaxone, ceftazidime, cefotaxime), aminoglycosides, fluoroquinolones (ciprofloxacin), tetracycline, cabepenems, Nitrofurantoin and trimethoprim-sulfamethoxazole. For ESBL isolates classes defining MDR excluded Penicillins and cephalosporins.

ESBL detection

All isolates with reduced susceptibilities to ceftazidime (zone of inhibition < 22mm), ceftriaxone (zone inhibition <25 mm) and cefotaxime (zone inhibition <27 mm) disks according to CLSI guidelines [11], were tested for an ESBL using E-test ESBL strips as previously described [8] and PCR. Isolates with reduced susceptibilities to cephalosporin were confirmed ESBL by either using E-tests ESBL strips or PCR.

Detection and identification of ESBL genotypes

All strain with reduced susceptibility to cephalosporin were examined for the presence of the bla TEM, bla SHV and bla CTX-M genes by PCR, using genomic DNA isolated by boiling. For bla TEM amplification the primers described by Dubois et al. were used [13]. The cycling conditions were 95°C for 15 min, followed by 30 cycles of denaturation at 95°C for 1 min, annealing at 55°C for 1 min, elongation at 72°C for 1 min, followed by a final extension of 72°C for 10 min.

For bla SHV amplification the primers SHV-1F (5′ – CGG CCT TCA CTC AAG GAT G – 3′) and SHV-1R (5′ – CGG STT AGC GTT GCC AGT – 3′) were used. The cycling conditions were the same as for those of blaTEM, but with an annealing temperature of 60°C. In PCR amplification targeting the blaCTX-M gene the primer pairs described by Pagani et al. [14] were used. The cycling conditions for these two primer pairs were initial activation at 95°C for 15 min, followed by 30 cycles of denaturation at 95°C for 30 s, annealing at 50°C for 40 s, elongation at 72°C for 1 min, followed by a final extension at 72°C for 10 min, and initial activation at 95°C for 15 min, followed by 30 cycles of denaturation at 95°C for 50 s, annealing at 50°C for 40 s, elongation at 72°C for 1 min, followed by a final extension at 72°C for 10 min. HotStarTaq Master Mix Kit (Qiagen, Hilden, Germany) and 1 μM of each primer were used for all PCR amplifications.

The PCR products were purified using either QIAquick PCR Purification Kit (Qiagen, Hilden, Germany) or ExoSAP- IT (GE Healthcare). Both strands were sequenced using the same primers as for PCRs, and sometimes internal sequencing primers were added as described by Arpin et al., Bermudes et al. and Rasheed et al. [1517]. The BigDye® Terminator v3.1 Cycle Sequencing Kit (Applied Biosystems, Foster City, CA) were used for sequencing, followed by analysis by capillary electrophoresis with an ABI Prism 3700 DNA Analyzer (Applied Biosystems). Point mutations were accepted if present in both the forward and reverse sequences.

Data analysis

Data were analysed using SPSS software version 20.0 (IBM SPSS statistics 20.0, SPSS Inc., Chicago, IL, USA). Chi-square test was used to determine associations between categorical variables, p < 0.05 was considered statistically significant.

Results

Prevalence of ESBL isolates

During the study period a total of 172 bacterial isolates from hospital- and community-acquired urinary tract infections were consecutively collected. The most frequent bacteria isolated were Escherichia coli (64%), followed by Klebsiella pneumoniae (15.7%) and other Enterobacteriaceae accounted for 20.3%. Of the 172 bacterial isolates, 23.8% (41/172) were ESBL-producers (Table 1). ESBL-producing isolates were more frequent from the hospital setting 32% (27/84) than from the community setting (16%, (14/88); p < 0.05). The proportion of ESBL positive E. coli isolates was significantly higher in hospital-acquired infections (20.3%, 11/54) compared to community-acquired infections (7.1% (4/56); p < 0.05). In K. pneumoniae isolates, ESBL-production was equally frequent in hospital- and community-acquired infections (33.3% each). The proportion of Enterobacter cloacae isolates producing ESBL was significantly higher in the hospital setting (71% (5/7)) than in the community setting (25% (1/4); p > 0.05).
Table 1

Distribution of ESBL positive and ESBL negative bacteria isolated from hospital- and community-acquired urinary tract infections

Bacteria spp.

Hospitalized patients

Community patients

Total

ESBL (+)

ESBL (−)

Subtotal

ESBL (+)

ESBL (−)

Subtotal

E. coli

11

43

54(64.3)

4

52

56(64)

110(64)

K. pneumoniae

4

8

12(14.3)

5

10

15(17)

27(15.7)

E. cloacae

5

2

7(8.3)

1

3

4(4.5)

11(6.4)

C. freundii

3

2

5(6)

1

3

4(4.5)

9(5.2)

M. morganii

1

1

2(2.3)

1

4

5(5.6)

7(4.1)

P. mirabilis

3

1

4(4.8)

2

1

3(3.3)

7(4.1)

P. rettgeri

0

0

0

0

1

1(1.1)

1(0.6)

Total

27

57

84(100)

14

74

88

172(100)

HA hospital acquired, CA community-acquired

Antimicrobial susceptibility pattern

Overall, ESBL-producing isolates showed significantly higher rates of resistance towards ciprofloxacin (85.5%), doxycycline (90.2%), gentamicin (80.5%), nalidixic acid (84.5%) and trimethoprim-sulfamethoxazole (85.4%) (p < 0.05) compared to non-ESBL producers. All ESBL and non-ESBL-producers were susceptible to imipenem (Table 2). Multi-drug resistant was high (95%) of ESBL-producers compared to 69% of non-ESBL-producing bacteria (p < 0.05).
Table 2

Antimicrobial resistance pattern for ESBL and Non- ESBL bacteria isolates, (% of resistance isolates within each group)

Antibiotic

E. coli

K. pneumoniae

E. cloacae

C. freundii

P. mirabilis

M. morganii

P. rettgeri

 

ESBL(+)

(n = 15)

ESBL (−)

(n = 95)

ESBL (+)

(n = 9)

ESBL (−)

(n = 18)

ESBL (+)

(n = 6)

ESBL (−)

(n = 5)

ESBL (+)

(n = 4)

ESBL (−)

(n = 5)

ESBL (+)

(n = 5)

ESBL (−)

(n = 2)

ESBL (+)

(n = 2)

ESBL (−)

(n = 5)

ESBL (−)

(n = 1)

AMC

NA

14.7

NA

44.4

NA

80

NA

50

NA

0

NA

20

100

CTX

NA

0.0

NA

0

NA

0

NA

0

NA

0

NA

0

0

CTZ

NA

0.0

NA

0

NA

0

NA

0

NA

0

NA

0

0

CRO

NA

1.1

NA

0

NA

0

NA

0

NA

0

NA

0

0

IMP

0

0

0

0

0

0

0

0

0

0

0

0

0

CHL

26.7

37.9

88.9

50

83.3

20

75

0

100

0

100

60

100

CIP

86.7

27.4

66.7

22.2

83.3

0

50

0

100

0

100

60

0

DO

100

73.7

66.7

44.4

83.3

60

100

40

100

100

100

80

100

CN

80

18

88.9

22.2

50

0

75

0

100

0

100

20

0

NAL

86.7

37.9

66.7

27.8

75

20

100

0

100

0

100

80

100

NIT

33.3

10.5

77.8

33.3

83.3

60

75

20

100

100

100

100

100

SXT

93.3

72.6

66.7

72.2

83.3

20

75

20

100

0

100

80

0

AMC Amoxicillin-clavulanic acid, CTX cefotaxime, CTZ ceftazidime, CRO ceftriaxone, IMP imipenem, CHL chloramphenicol, CIP ciprofloxacin, DO doxycycline, CN gentamicin, NAL nalidixic acid, NIT nitrofurantoin, SXT trimethoprim-sulfamethoxazole

NA Not applicable

When comparing rates of resistance between HA and CA ESBL, we found that hospital-acquired E. coli and K. pneumoniae were more frequently resistant to ciprofloxacin, gentamicin and nalidixic acid than those isolated from community-acquired infections (Table 3).
Table 3

Antimicrobial resistance pattern of E. coli and K. pneumoniae isolates from Hospital-acquired and Community-acquired urinary tract infections (% of resistance isolates within each group)

Antibiotic

E. coli (n = 110)

K. pneumoniae (n = 27)

Hospital acquired

Community acquired

Hospital acquired

Community acquired

ESBL (+)

(n = 11)

ESBL (−)

(n = 43)

ESBL (+)

(n = 4)

ESBL (−)

(n = 52)

ESBL (+)

(n = 4)

ESBL (−)

(n = 8)

ESBL (+)

(n = 5)

ESBL (−)

(n = 10)

AMC

NA

11.6

NA

17.3

NA

62.5

NA

30.0

CTX

NA

0

NA

0

NA

0

NA

0

CTZ

NA

0

NA

0

NA

0

NA

0

CRO

NA

0

NA

0

NA

0

NA

0

IMP

0

0

0

0

0

0

0

0

CHL

27.3

41.9

25.0

34.6

75.0

62.5

100

40.0

CIP

90.9

32.6

75.0

23.1

100

25.0

40.0

20.0

DOX

100

69.8

100

76.9

75.0

62.5

60.0

30.0

CN

90.9

16.3

50.0

21.2

100

37.5

80.0

10.0

NAL

90.0

41.9

75.0

34.6

100

25.0

40.0

30.0

NIT

27.3

27.3

50.0

50.0

100

100

60.0

60.0

SXT

90.9

62.8

100

80.8

75.0

87.5

60.0

60.0

(+) = positive; (−) = negative

AMC Amoxicillin-clavulanic acid, CTX cefotaxime, CTZ ceftazidime, CRO ceftriaxone, IMP imipenem, CHL chloramphenicol, CIP ciprofloxacin, DO doxycycline, CN gentamicin, NAL nalidixic acid, NIT nitrofurantoin, SXT trimethoprim-sulfamethoxazole

Non-ESBL-producing E. coli and K. pneumoniae from hospital- and community-acquired infections were less frequently resistant to gentamicin, nalidixic acid and ciprofloxacin. However, non-ESBL-producing E. coli from outpatients showed moderately high rates of resistance to trimethoprim-sulfamethoxazole, nitrofurantoin and doxycycline compared to isolates from inpatients. Higher rates of resistance to amoxicillin-clavulanic acid and trimethoprim-sulfonamide were observed in hospital-acquired as compared to community-acquired isolates of non-ESBL-producing K. pneumoniae. (Susceptibility profile for other isolates see Additional file 1: Table S1).

Molecular characterization of ESBL producing bacteria

An ESBL genotype could be identified for 32 of the all ESBL confirmed isolates (Table 4). Among these, 90.6% (29/32) were bla CTX-M-15 positive, 6.25% (2/32) were bla SHV-12 positive and one isolate was found to carry both bla CTX-M-15 and bla SHV-12. None of the isolate carried bla TEM. Of the 29 isolates carrying bla CTX-M-15, 69% (20/29) were hospital isolates and 31% (9/29) from community settings. (All three isolates harboring bla SHV-12 were from hospital setting (E. coli, E. cloacae and Citrobacter freundii). All isolates carrying bla CTX-M-15 displayed high rates of resistance to non β-lactam agents, including ciprofloxacin (88%), gentamicin (81.5%) and trimethoprim-sulfamethoxazole (89%).
Table 4

ESBL genotypes in bacteria isolated from hospital-acquired and community-acquired urinary tract infections

Bacteria spp.

CTX-M-15

SHV-12

CTX-M-15/SHV-12

HA

CA

Subtotal

HA

CA

Subtotal

HA

CA

E. coli

10

4

14

0

0

0

1

0

K. pneumoniae

4

3

7

0

0

0

0

0

E. cloacae

3

1

4

1

0

1

0

0

C. freundii

2

0

2

1

0

1

0

0

M. morganii

1

1

2

0

0

0

0

0

Total

20

9

29

2

0

0

1

0

HA Hospital acquired, CA community acquired

Discussion

In recent years there has been an alarming increase in community acquired infections with ESBL-producing bacteria [5, 12, 18]. Spread of these strains in the community is a major concern to patient healthcare, since most display multidrug resistance, limiting outpatient treatment options. The resultant increasing use of broad-spectrum antibiotics to treat infections caused by ESBL-producers is expected to lead to further emergence of antimicrobial resistance. However, little data exist on molecular characterization of ESBL isolates causing community-acquired urinary tract infections in Tanzania and Africa. The current study shows that ESBL-producing isolates caused both community and hospital-acquired urinary tract infections in 2004, when CTX-M-15 was first reported in Tanzania.

The overall frequency of ESBL-producing Enterobacteriaceae among urinary tract pathogens in this study was 23.8%. The frequency of ESBL-producing pathogens was significantly higher in hospital-acquired compared to community-acquired uropathogens. Our finding is in agreement with other studies [1922] reporting higher frequency of ESBL-producers in hospital-acquired urinary tract infections compared to community-acquired infections. A possible explanation for this could be that hospital-acquired infections were more likely associated with prolonged hospitalization, comorbidities, previous antibiotic use and urinary catheterization which are well-known risk factors for acquisition of ESBL-producing pathogens [19]. However, the finding of ESBL-producing isolates in community urinary infections is worrisome because of the limited treatment options, considering most of these isolates display multidrug resistance.

Similar to other studies in Africa [4, 10, 22], we found that ESBL-producing isolates from both hospital and community settings displayed high rates of resistance to ciprofloxacin, trimethoprim-sulfamethoxazole, gentamicin, nalidixic acid and doxycycline. Resistance to commonly prescribed oral antimicrobials in these resource-limited settings, specifically to ciprofloxacin and trimethoprim-sulfamethoxazole, limits outpatient therapeutic options. Considering that most of the outpatients present with uncomplicated urinary tract infections, opting to injectable and expensive antimicrobials increases health-care burdens. We also found non-ESBL-producing E. coli from community-acquired urinary tract infections had moderate to high rates of resistance to trimethoprim-sulfamethoxazole, doxycycline and nitrofurantoin. This could be expected, since oral antimicrobials are inexpensive and easily available over the counter, and self-treatment is common in Africa; these are well known factors driving emergence of antimicrobial resistance bacteria.

Among 41 ESBL defined isolates, 78% were found to carry ESBL genes. Our finding of a predominance of CTX-M-15 is in line to previous and recent studies from hospital and community urinary tract infections [6, 7, 18, 23], and our finding concurs with those of studies from the same setting, which found CTX-M-15 as the dominant ESBL genotype [810, 24]. CTX-M types ESBLs, in particular CTX-M-15, are known for their rapid dissemination world-wide among the members of Enterobacteriaceae [6, 12, 23, 25, 26]. It has also been suggested that the widespread use of ceftriaxone and cefotaxime could be a reason of emergence and spread of CTX-M enzymes [27].

Our study had some limitations; one our isolates were collected in 2004 and may not imply the current situation. However, our findings shed lights on community spread of ESBL-producers and suggest existence in Tanzania at least since 2004. Second being a laboratory-based study, clinical information was not obtained, and we could not analyze risk factors for ESBL infections. Furthermore, epidemiological typing to assess clonality of the isolates was not performed, and this could have added value to the understanding of the epidemiological spread of ESBL genes.

Conclusion

In conclusion, we report the presence of Enterobacteriaceae harboring CTX-M-15 type ESBL causing community-acquired urinary tract infections in Tanzania as early as 2004. Furthermore, both ESBL and non-ESBL-producing isolates displayed high rates of multidrug resistance. Further investigation needs to be performed to understand the transmission dynamics of CTX-M type of ESBL resistance.

Declarations

Acknowledgement

We would like to acknowledge members of Department of Microbiology and Immunology, Muhimbili National Hospital, Dar es Salaam, Tanzania, the Department of Microbiology, Haukeland University Hospital, Bergen, Norway and the Department of Clinical Science, University of Bergen, Bergen, Norway, for their technical and financial support during the molecular study.

Availability of data and materials

The datasets analysed during this study are available from the corresponding author on request.

Authors’ contributions

JM, SM, MGT, FN, WU, BB, NL conceived and designed the study. FN collected study data. FN and MGT performed the experiments. JM drafted the manuscript. All authors read and approved the manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Ethical approval was obtained from the senate research and publications committee, Muhimbili University of Health and Allied Sciences, Tanzania.

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Authors’ Affiliations

(1)
Department of Clinical Science, University of Bergen
(2)
Department of Microbiology and Immunology, Muhimbili University of Health and Allied Sciences
(3)
National Centre for Tropical Infectious Diseases, Department of Medicine, Haukeland University Hospital

References

  1. Bosi C, Davin-Regli A, Bornet C, Mallea M, Pages JM, Bollet C. Most Enterobacter aerogenes strains in France belong to a prevalent clone. J Clin Microbiol. 1999;37:2165–9.PubMedPubMed CentralGoogle Scholar
  2. Paterson DL, Bonomo RA. Extended-spectrum beta-lactamases: a clinical update. Clin Microbiol Rev. 2005;18:657–86.View ArticlePubMedPubMed CentralGoogle Scholar
  3. Canton R, Coque TM. The CTX-M beta-lactamase pandemic. Curr Opin Microbiol. 2006;9:466–75.View ArticlePubMedGoogle Scholar
  4. Meier S, Weber R, Zbinden R, Ruef C, Hasse B. Extended-spectrum beta-lactamase-producing Gram-negative pathogens in community-acquired urinary tract infections: an increasing challenge for antimicrobial therapy. Infection. 2011;39:333–40.View ArticlePubMedGoogle Scholar
  5. Hammami S, Saidani M, Ferjeni S, Aissa I, Slim A, Boutiba-Ben Boubaker I. Characterization of extended spectrum beta-lactamase-producing Escherichia coli in community-acquired urinary tract infections in Tunisia. Microb Drug Resist. 2013;19:231–6.View ArticlePubMedGoogle Scholar
  6. Ibrahimagic A, Bedenic B, Kamberovic F, Uzunovic S. High prevalence of CTX-M-15 and first report of CTX-M-3, CTX-M-22, CTX-M-28 and plasmid-mediated AmpC beta-lactamase producing Enterobacteriaceae causing urinary tract infections in Bosnia and Herzegovina in hospital and community settings. J Infect Chemother. 2015;21:363–9.View ArticlePubMedGoogle Scholar
  7. Barguigua A, El Otmani F, Talmi M, Zerouali K, Timinouni M. Prevalence and types of extended spectrum beta-lactamases among urinary Escherichia coli isolates in Moroccan community. Microb Pathog. 2013;61–62:16–22.View ArticlePubMedGoogle Scholar
  8. Blomberg B, Jureen R, Manji KP, Tamim BS, Mwakagile DS, Urassa WK, et al. High rate of fatal cases of pediatric septicemia caused by gram-negative bacteria with extended-spectrum beta-lactamases in Dar es Salaam, Tanzania. J Clin Microbiol. 2005;43:745–9.View ArticlePubMedPubMed CentralGoogle Scholar
  9. Ndugulile F, Jureen R, Harthug S, Urassa W, Langeland N. Extended spectrum beta-lactamases among Gram-negative bacteria of nosocomial origin from an intensive care unit of a tertiary health facility in Tanzania. BMC Infect Dis. 2005;5:86.View ArticlePubMedPubMed CentralGoogle Scholar
  10. Mshana SE, Falgenhauer L, Mirambo MM, Mushi MF, Moremi N, Julius R, et al. Predictors of blaCTX-M-15 in varieties of Escherichia coli genotypes from humans in community settings in Mwanza, Tanzania. BMC Infect Dis. 2016;16:187.View ArticlePubMedPubMed CentralGoogle Scholar
  11. CLSI. Perfomance standards for antimicrobial susceptibility testing; fifteenth information supplement vol. CLSI document M100-S15. Clinical and Laboratory Standards Institute: Wayne; 2005.Google Scholar
  12. Woodford N, Ward ME, Kaufmann ME, Turton J, Fagan EJ, James D, et al. Community and hospital spread of Escherichia coli producing CTX-M extended-spectrum beta-lactamases in the UK. J Antimicrob Chemother. 2004;54:735–43.View ArticlePubMedGoogle Scholar
  13. Dubois V, Poirel L, Marie C, Arpin C, Nordmann P, Quentin C. Molecular characterization of a novel class 1 integron containing bla(GES-1) and a fused product of aac3-Ib/aac6’-Ib’ gene cassettes in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2002;46:638–45.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Pagani L, Luzzaro F, Ronza P, Rossi A, Micheletti P, Porta F, et al. Outbreak of extended-spectrum beta-lactamase producing Serratia marcescens in an intensive care unit. FEMS Immunol Med Microbiol. 1994;10:39–46.PubMedGoogle Scholar
  15. Arpin C, Labia R, Andre C, Frigo C, El Harrif Z, Quentin C. SHV-16, a beta-lactamase with a pentapeptide duplication in the omega loop. Antimicrob Agents Chemother. 2001;45:2480–5.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Bermudes H, Jude F, Chaibi EB, Arpin C, Bebear C, Labia R, et al. Molecular characterization of TEM-59 (IRT-17), a novel inhibitor-resistant TEM-derived beta-lactamase in a clinical isolate of Klebsiella oxytoca. Antimicrob Agents Chemother. 1999;43:1657–61.PubMedPubMed CentralGoogle Scholar
  17. Rasheed JK, Jay C, Metchock B, Berkowitz F, Weigel L, Crellin J, et al. Evolution of extended-spectrum beta-lactam resistance (SHV-8) in a strain of Escherichia coli during multiple episodes of bacteremia. Antimicrob Agents Chemother. 1997;41(3):647–53.PubMedPubMed CentralGoogle Scholar
  18. Kariuki S, Revathi G, Corkill J, Kiiru J, Mwituria J, Mirza N, et al. Escherichia coli from community-acquired urinary tract infections resistant to fluoroquinolones and extended-spectrum beta-lactams. J Infect Dev Ctries. 2007;1:257–62.PubMedGoogle Scholar
  19. Kader AA, Angamuthu K. Extended-spectrum beta-lactamases in urinary isolates of Escherichia coli, Klebsiella pneumoniae and other gram-negative bacteria in a hospital in Eastern Province, Saudi Arabia. Saudi Med J. 2005;26:956–9.PubMedGoogle Scholar
  20. Latifpour M, Gholipour A, Damavandi MS. Prevalence of Extended-Spectrum Beta-Lactamase-Producing Klebsiella pneumoniae Isolates in Nosocomial and Community-Acquired Urinary Tract Infections. Jundishapur J Microbiol. 2016;9:e31179.PubMedPubMed CentralGoogle Scholar
  21. Khanfar HS, Bindayna KM, Senok AC, Botta GA. Extended spectrum beta-lactamases (ESBL) in Escherichia coli and Klebsiella pneumoniae: trends in the hospital and community settings. J Infect Dev Ctries. 2009;3:295–9.PubMedGoogle Scholar
  22. Moyo SJ, Aboud S, Kasubi M, Lyamuya EF, Maselle SY. Antimicrobial resistance among producers and non-producers of extended spectrum beta-lactamases in urinary isolates at a tertiary Hospital in Tanzania. BMC Res Notes. 2010;3:348.View ArticlePubMedPubMed CentralGoogle Scholar
  23. Fam N, Leflon-Guibout V, Fouad S, Aboul-Fadl L, Marcon E, Desouky D, et al. CTX-M-15-producing Escherichia coli clinical isolates in Cairo (Egypt), including isolates of clonal complex ST10 and clones ST131, ST73, and ST405 in both community and hospital settings. Microb Drug Resist. 2011;17:67–73.View ArticlePubMedGoogle Scholar
  24. Mshana SE, Imirzalioglu C, Hain T, Domann E, Lyamuya EF, Chakraborty T. Multiple ST clonal complexes, with a predominance of ST131, of Escherichia coli harbouring blaCTX-M-15 in a tertiary hospital in Tanzania. Clin Microbiol Infect. 2011;17(8):1279–82.View ArticlePubMedGoogle Scholar
  25. Blanco VM, Maya JJ, Correa A, Perenguez M, Munoz JS, Motoa G, et al. [Prevalence and risk factors for extended-spectrum beta-lactamase-producing Escherichia coli causing community-onset urinary tract infections in Colombia]. Enferm Infecc Microbiol Clin. 2016;34(9):559–65.View ArticlePubMedPubMed CentralGoogle Scholar
  26. Rossolini GM, D’Andrea MM, Mugnaioli C. The spread of CTX-M-type extended-spectrum beta-lactamases. Clin Microbiol Infect. 2008;14 Suppl 1:33–41.View ArticlePubMedGoogle Scholar
  27. Wang H, Kelkar S, Wu W, Chen M, Quinn JP. Clinical isolates of Enterobacteriaceae producing extended-spectrum beta-lactamases: prevalence of CTX-M-3 at a hospital in China. Antimicrob Agents Chemother. 2003;47(2):790–3.View ArticlePubMedPubMed CentralGoogle Scholar

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