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beta-Lactam resistance phenotype determination in Escherichia coli isolates from University Malaya Medical Centre

Wong JS, Mohd Azri ZA, Subramaniam G, Ho SE, Palasubramaniam S, Navaratnam P

Malays J Pathol, 2003 Dec;25(2):113-9.
PMID: 16196367

beta-Lactamases have been identified as the major cause of antimicrobial resistance to beta-lactam antibiotics in Escherichia coli. The activities of ampicillin-sulbactam and amoxicillin-clavulanate as well as a range of beta-lactam antibiotics were studied with 87 clinical E. coli isolates from patients of the University Malaya Medical Center using the disc diffusion technique. Susceptible, intermediate and resistant categories were established based on the diameter of zones of inhibition set by the National Committee for Clinical Laboratory Standards (NCCLS). The isolates were then classified into 6 phenotypes according to the criteria stated in the methodology: S (susceptible to all beta-lactams); TL (resistant to aminopenicillins; amoxicillin-clavulanate susceptible and susceptible or intermediate to ampicillin-sulbactam); TI (resistant to aminopenicillins and ampicillin-sulbactam; susceptible to amoxicilin-clavulanate); TH-IRT (resistant to aminopenicillins; intermediate or resistant to amoxicillin-clavulanate; resistant to ampicillin-sulbactam); ESBL (resistant to aminopenicillins and oxyimino cephalosporins; positive results with the double-disc diffusion test); and CP (resistant to aminopenicillins, beta-lactam-beta-lactamase inhibitor combinations, oxyimino cephalosporins and cephamycins). Results showed that the TL phenotype was the commonest (40.2% of the isolates) followed by S (31%), TH-IRT (16.1%), ESBL and CP (3.4% each) and TI (2.3%). One isolate showed both ESBL and CP phenotypes while two isolates were classified as inconclusive. Representatives from each phenotype were further analysed for the presence of beta-lactamases which revealed a predominance of TEM and SHV enzyme producers. PCR-SSCP analysis of the SHV gene from all the ESBL and CP isolates revealed the predominance of SHV 5-type enzyme which was concurrent with our previous studies.
Fulltext Transcriptional profiles of the response of methicillin-resistant Staphylococcus aureus to pentacyclic triterpenoids

Chung PY, Chung LY, Navaratnam P

PLoS One, 2013;8(2):e56687.
PMID: 23437212 DOI: 10.1371/journal.pone.0056687

Staphylococcus aureus is an important human pathogen in both hospital and the community that has demonstrated resistance to all currently available antibiotics over the last two decades. Multidrug-resistant isolates of methicillin-resistant S. aureus (MRSA) exhibiting decreased susceptibilities to glycopeptides has also emerged, representing a crucial challenge for antimicrobial therapy and infection control. The availability of complete whole-genome nucleotide sequence data of various strains of S. aureus presents an opportunity to explore novel compounds and their targets to address the challenges presented by antimicrobial drug resistance in this organism. Study compounds α-amyrin [3β-hydroxy-urs-12-en-3-ol (AM)], betulinic acid [3β-hydroxy-20(29)-lupaene-28-oic acid (BA)] and betulinaldehyde [3β-hydroxy-20(29)-lupen-28-al (BE)] belong to pentacyclic triterpenoids and were reported to exhibit antimicrobial activities against bacteria and fungi, including S. aureus. The MIC values of these compounds against a reference strain of methicillin-resistant S. aureus (MRSA) (ATCC 43300) ranged from 64 µg/ml to 512 µg/ml. However, the response mechanisms of S. aureus to these compounds are still poorly understood. The transcription profile of reference strain of MRSA treated with sub-inhibitory concentrations of the three compounds was determined using Affymetrix GeneChips. The findings showed that these compounds regulate multiple desirable targets in cell division, two-component system, ABC transporters, fatty acid biosynthesis, peptidoglycan biosynthesis, aminoacyl-tRNA synthetase, ribosome and β-lactam resistance pathways which could be further explored in the development of therapeutic agents for the treatment of S. aureus infections.
Fulltext Synergistic antimicrobial activity between pentacyclic triterpenoids and antibiotics against Staphylococcus aureus strains

Chung PY, Navaratnam P, Chung LY

Ann Clin Microbiol Antimicrob, 2011;10:25.
PMID: 21658242 DOI: 10.1186/1476-0711-10-25

There has been considerable effort to discover plant-derived antibacterials against methicillin-resistant strains of Staphylococcus aureus (MRSA) which have developed resistance to most existing antibiotics, including the last line of defence, vancomycin. Pentacyclic triterpenoid, a biologically diverse plant-derived natural product, has been reported to show anti-staphylococcal activities. The objective of this study is to evaluate the interaction between three pentacyclic triterpenoid and standard antibiotics (methicillin and vancomycin) against reference strains of Staphylococcus aureus.
Surveillance study of bacteraemic episodes in febrile neutropenic children

Ariffin H, Navaratnam P, Lin HP

Int J Clin Pract, 2002 May;56(4):237-40.
PMID: 12074201

We prospectively studied the type, frequency and outcome of infections in 513 patients with 762 consecutive episodes of febrile neutropenia (FN) over a five-year period between 1995 and 1999 in a single paediatric oncology unit. The findings were then compared with a similar study carried out in our unit between 1990 and 1994. The types of bacterial isolates and sensitivity patterns were also studied to identify trends and to gauge the suitability of antibiotics chosen for empirical therapy. Bacteraemia was documented in 35.4% of FN episodes, although 70% of patients did not have an obvious site of sepsis. The majority of isolates (61.9%) were gram-negative bacteria, a consistent finding throughout the study period. Resistance to ceftazidime, amikacin and imipenem among gram-negative bacteria was 26.3%, 21.2% and 0.7%, respectively. Methicillin resistance among gram-positive bacteria was 26.3%, while no vancomycin-resistant bacteria were encountered. There were 36 sepsis-related deaths. Factors associated with a fatal outome were prolonged capillary refill time, hypotension, fever above 39 degrees C and pneumonia. Rapid neutrophil recovery was associated with a good prognosis. A change to our current choice of empirical antibiotics for FN, comprising ceftazidime/ceftriaxone and amikacin appears necessary because of the relatively high resistance rates found.
Simultaneous species identification and detection of methicillin resistance in staphylococci using triplex real-time PCR assay

Sabet NS, Subramaniam G, Navaratnam P, Sekaran SD

Diagn Microbiol Infect Dis, 2006 Sep;56(1):13-8.
PMID: 16650954

For rapid identification of methicillin-resistant Staphylococcus aureus, molecular methods are generally targeting mecA and species-specific genes. Sa442 DNA fragment is a popular species-specific target. However, recently, there have been few reports on S. aureus isolates that are negative for Sa442 fragment; therefore, use of single gene or DNA-fragment-specific polymerase chain reaction (PCR) for identification of microbial isolate may result in misidentification. This study includes CoA gene in parallel with Sa442 marker for identification of S. aureus. This further improves the specificity of the assay by checking for 2 determinants simultaneously for the identification of S. aureus and can prevent misidentification of S. aureus isolates lacking Sa442 DNA fragment. In this study, the newly developed triplex real-time PCR assay was compared with a quadruplex conventional gel-based PCR assay using the same primer sets in both assays. The dual-labeled TaqMan probes (ProOligo, France) for these primers were specifically designed and used in a real-time PCR assay. The clinical isolates (n = 152) were subjected to both PCR assays. The results obtained from both assays proved that the primer and probe sets were 100% sensitive and 100% specific for identification of S. aureus and detection of methicillin resistance. This triplex real-time PCR assay represents a rapid and powerful method for S. aureus identification and detection of methicillin resistance.
SHV-5 extended-spectrum beta-lactamases in clinical isolates of Escherichia coli in Malaysia

Subramaniam G, Palasubramaniam S, Navaratnam P

Indian J Med Microbiol, 2006 Jul;24(3):205-7.
PMID: 16912441

Escherichia coli isolates resistant to ceftazidime isolated in the University Malaya Medical Center (UMMC) Kuala Lumpur, Malaysia, between the years 1998 and 2000 were studied for extended-spectrum beta-lactamase (ESBL) production. All strains were analysed phenotypically and genotypically and found to be ESBL-producing organisms harbouring SHV-5 beta-lactamase. This was confirmed by PCR-SSCP and nucleotide sequencing of the blaSHV amplified gene. As there was no evidence of ESBL activity in E. coli prior to this, coupled with the fact that there was a predominance of SHV-5 beta-lactamases in Klebsiella pneumoniae isolates in UMMC, we postulate that the E. coli obtained the SHV-5 beta-lactamase genes by plasmid transfer from the ESBL-producing K. pneumoniae.
Resistance to extended-spectrum beta-lactams by the emergence of SHV-12 and the loss of OmpK35 in Klebsiella pneumoniae and Escherichia coli in Malaysia

Palasubramaniam S, Muniandy S, Navaratnam P

J Microbiol Immunol Infect, 2009 Apr;42(2):129-33.
PMID: 19597644

In addition to beta-lactamase production, loss of porins confers resistance to extended-spectrum beta-lactams in Klebsiella pneumoniae and Escherichia coli infection. This study describes the detection of SHV-12 extended-spectrum beta-lactamase (ESBL) subtype and the loss of OmpK35 porin in 4 strains of K. pneumoniae and E. coli.
Reinfection and duodenal ulcer relapse in south-east Asian patients following successful Helicobacter pylori eradication: results of a 2-year follow-up

Goh KL, Navaratnam P, Peh SC

Eur J Gastroenterol Hepatol, 1996 Dec;8(12):1157-60.
PMID: 8980932

OBJECTIVES: To determine the reinfection rate of Helicobacter pylori and duodenal ulcer relapse rate in a group of patients followed up long term.
DESIGN: Prospective study.
PATIENTS AND METHODS: Patients were followed up endoscopically at 3, 6, 12 and 24 months after successful H. pylori eradication and duodenal ulcer healing. H. pylori status was determined by culture, rapid urease test, Gram's stain of a fresh tissue smear and histological examination of antral biopsies and rapid urease test and histological examination of corpus biopsies.
MAIN OUTCOME MEASURES: Duodenal ulcer healing, H. pylori reinfection.
RESULTS: Thirty-eight patients with duodenal ulcer disease (35 active, 3 healed) had successfully eradicated H. pylori following treatment with omeprazole/amoxycillin (n = 11), omeprazole/amoxycillin/metronidazole (n = 16) and colloidal bismuth subcitrate/ amoxycillin/metronidazole (n = 11). All patients with active duodenal ulcer had healed ulcers at the end of therapy. Thirty-five of 38 patients were seen according to schedule up to 2 years; two patients were seen up to 12 months and one up to 6 months only. Reinfection with H. pylori was not recorded in any of our patients. Shallow duodenal ulcers were noted in three patients at 1-year follow-up, two of whom admitted to taking non-steroidal anti-inflammatory drugs (NSAIDs); H. pylori status was negative in all three. Subsequent follow-up revealed spontaneous healing of the ulcers in all three patients. At 2 years, one patient whose H. pylori status was negative had recurrence of duodenal ulcer. All of the three patients who defaulted subsequent to follow-up were negative for H. pylori and had healed ulcers on follow-up endoscopy at 6 and 12 months.
CONCLUSION: Reinfection rate with H. pylori was zero in a group of South-East Asian patients who had successfully eradicated the infection. Duodenal ulcer relapse was also low (2.9%) in this group of patients at 2 years.
Rapid detection of non-enterobacteriaceae directly from positive blood culture using fluorescent in situ hybridization

Wong EH, Subramaniam G, Navaratnam P, Sekaran SD

Indian J Med Microbiol, 2007 Oct;25(4):391-4.
PMID: 18087092

Fluorescent in situ hybridization (FISH) was carried out using two different oligonucleotide probes specific for Pseudomonas spp. and Acinetobacter spp. These probes were tested against different organisms and were found to be highly specific. Sensitivity testing showed that the probes were able to detect as low as 10 3 CFU/mL. In addition, FISH was carried out directly on positive blood culture samples and the detection of microorganisms took less than 2 h. We believe that FISH is a rapid method that can be used as a routine laboratory diagnostic technique for the detection of Acinetobacter spp. and Pseudomonas spp. in clinical samples.
Rapid detection of ESBL-producing Klebsiella pneumoniae in blood cultures by fluorescent in-situ hybridization

Palasubramaniam S, Muniandy S, Navaratnam P

J Microbiol Methods, 2008 Jan;72(1):107-9.
PMID: 18054098

Multi-resistant Enterobacteriaceae pose a serious threat of hospital acquired infections and their rapid identification is important for better clinical outcome. This study describes the rapid identification of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae of the sulphydryl variable-type by fluorescent in-situ hybridization. The method which rapidly identifies the target genes within 1 h could be a potentially rapid bacterial diagnostic tool.
Potential targets by pentacyclic triterpenoids from Callicarpa farinosa against methicillin-resistant and sensitive Staphylococcus aureus

Chung PY, Chung LY, Navaratnam P

Fitoterapia, 2014 Apr;94:48-54.
PMID: 24508863 DOI: 10.1016/j.fitote.2014.01.026

The evolution of antibiotic resistance in Staphylococcus aureus showed that there is no long-lasting remedy against this pathogen. The limited number of antibacterial classes and the common occurrence of cross-resistance within and between classes reinforce the urgent need to discover new compounds targeting novel cellular functions not yet targeted by currently used drugs. One of the experimental approaches used to discover novel antibacterials and their in vitro targets is natural product screening. Three known pentacyclic triterpenoids were isolated for the first time from the bark of Callicarpa farinosa Roxb. (Verbenaceae) and identified as α-amyrin [3β-hydroxy-urs-12-en-3-ol], betulinic acid [3β-hydroxy-20(29)-lupaene-28-oic acid], and betulinaldehyde [3β-hydroxy-20(29)-lupen-28-al]. These compounds exhibited antimicrobial activities against reference and clinical strains of methicillin-resistant (MRSA) and methicillin-sensitive S. aureus (MSSA), with minimum inhibitory concentration (MIC) ranging from 2 to 512 μg/mL. From the genome-wide transcriptomic analysis to elucidate the antimicrobial effects of these compounds, multiple novel cellular targets in cell division, two-component system, ABC transporters, fatty acid biosynthesis, peptidoglycan biosynthesis, aminoacyl-tRNA synthetases, ribosomes and β-lactam resistance pathways are affected, resulting in destabilization of the bacterial cell membrane, halt in protein synthesis, and inhibition of cell growth that eventually lead to cell death. The novel targets in these essential pathways could be further explored in the development of therapeutic compounds for the treatment of S. aureus infections and help mitigate resistance development due to target alterations.
Molecular characterization of genes encoding the quinolone resistance determining regions of Malaysian Streptococcus pneumoniae strains

Kumari N, Subramaniam G, Navaratnam P, Sekaran SD

Indian J Med Microbiol, 2008 5 1;26(2):148-50.
PMID: 18445951

Genes encoding the quinolones resistance determining regions (QRDRs) in Streptococcus pneumoniae were detected by PCR and the sequence analysis was carried out to identify point mutations within these regions. The study was carried out to observe mutation patterns among S. pneumoniae strains in Malaysia. Antimicrobial susceptibility testing of 100 isolates was determined against various antibiotics, out of which 56 strains were categorised to have reduced susceptibility to ciprofloxacin (>or=2 microg/mL). These strains were subjected to PCR amplification for presence of the gyrA, parC , gyrB and parE genes. Eight representative strains with various susceptibilities to fluoroquinolones were sequenced. Two out of the eight isolates that were sequenced were shown to have a point mutation in the gyrA gene at position Ser81. The detection of mutation at codon Ser81 of the gyrA gene suggested the potential of developing fluoroquinolone resistance among S. pneumoniae isolates in Malaysia. However, further experimental work is required to confirm the involvement of this mutation in the development of fluoroquinolone resistance in Malaysia.
Molecular analysis of Salmonella enteritidis by pulsed-field gel electrophoresis and ribotyping

Thong KL, Ngeow YF, Altwegg M, Navaratnam P, Pang T

J Clin Microbiol, 1995 May;33(5):1070-4.
PMID: 7615707

A total of 61 isolates of Salmonella enteritidis were analyzed by the techniques of pulsed-field gel electrophoresis (PFGE) and ribotyping. Twenty-three of the isolates were from Zurich, Switzerland, and 38 isolates were from the University Hospital, Kuala Lumpur, Malaysia. Five of the Malaysian isolates were hospital-related outbreak strains and were shown to be indistinguishable by PFGE analysis following digestion with three different restriction endonucleases, XbaI (5'-TCTAGA-3'), SpeI (5'-ACTAGT-3'), and AvrII (5'-CCTAGG-3'). The PFGE pattern of an isolate from a suspected carrier staff nurse was found to be identical to those of the hospital outbreak isolates. These isolates were also indistinguishable by ribotyping with SmaI and SphI. The same single PFGE pattern was also detected in 29 of 32 sporadic isolates of S. enteritidis. Four closely related ribotypes were detected among these 29 isolates. Similarly, outbreak-related strains from Switzerland showed close genetic identity by PFGE and ribotyping. Strains obtained from poultry showed more variations in their PFGE patterns and ribotypes, although the patterns were still closely related. In addition, SphI ribotypes A and D among the Swiss strains correlated with phage types 4 and 8, respectively. No correlation of phage types with PFGE pattern was noted. Both PFGE and ribotyping indicate that the S. enteritidis strains circulating in Malaysia and Switzerland are very similar and may be clonally related. Comparison of the PFGE patterns with the ribotypes for 23 Swiss and 16 Malaysian isolates showed that there was a 69% concordance in the grouping of isolates. We conclude that the close genetic similarity observed between epidemiologically unrelated and outbreak-related isolates of S. enteritidis suggests that both PFGE and ribotyping are of limited value in the epidemiological analysis of these particular isolates, possibly because of the highly clonal nature of pathogenic strains of S. enteritidis.
Identification, by gene expression profiling analysis, of novel gene targets in Staphylococcus aureus treated with betulinaldehyde

Chung PY, Chung LY, Navaratnam P

Res. Microbiol., 2013 May;164(4):319-26.
PMID: 23385141 DOI: 10.1016/j.resmic.2013.01.005

Staphylococcus aureus has become a serious concern in hospitals and community due to rapid adaptation to existing antimicrobial agents. Betulinaldehyde [3β-hydroxy-20(29)-lupen-28-al (BE)] belongs to pentacyclic triterpenoids that are based on a 30-carbon skeleton comprising four six-membered rings and one five-membered ring. In a preliminary study, BE exhibited antimicrobial activity against reference strains of methicillin-resistant and methicillin-sensitive S. aureus. However, the response mechanism of S. aureus to this compound is not known. In this study, the global gene expression patterns of both the reference strains in response to sub-inhibitory concentrations of BE were analyzed using DNA microarray to identify gene targets, particularly essential targets in novel pathways, i.e. not targeted by currently used antibiotics, or novel targets in existing pathways. The transcriptome analysis revealed repression of genes in the aminoacyl-tRNA synthetase and ribosome pathways in both the reference strains. Other pathways such as cell division, two-component systems, ABC transporters, fatty acid biosynthesis and peptidoglycan biosynthesis were affected only in the reference strain of methicillin-resistant S. aureus. The findings suggest that BE regulates multiple desirable targets which could be further explored in the development of therapeutic agents for the treatment of S. aureus infections.
High Helicobacter pylori resistance to metronidazole but zero or low resistance to clarithromycin, levofloxacin, and other antibiotics in Malaysia

Goh KL, Navaratnam P

Helicobacter, 2011 Jun;16(3):241-5.
PMID: 21585611 DOI: 10.1111/j.1523-5378.2011.00841.x

OBJECTIVE: Bacterial resistance to antibiotics is the single most important determinant of treatment success. The objective of this study was to determine the prevalence of Helicobacter pylori resistance to clarithromycin, amoxicillin, metronidazole, tetracycline, levofloxacin, rifabutin, and furazolidone in our local bacterial strains.
METHODS: Samples from consecutive ninety patients were obtained for culture and sensitivity testing. Resistance to individual antibiotics were tested using the E-test and MIC(90) read from the strips. Resistance to rifampicin and nitrofurantoin were used as a surrogate for rifabutin and furazolidine.
RESULTS: There was a high prevalence of resistance to metronidazole 68/90 (75.5%). No male (34/45 (75.5%) versus female (35/45 (77.7%) difference in frequency of metronidazole resistance was noted (p = 1.000). There was zero resistance (0) to clarithromycin, levofloxacin, amoxicillin, and nitrofurantoin/furazolidone. Resistance to rifampicin/rifabutin was for breakpoints of 1 and 4 μg/mL of 14.4 and 2.2% respectively.
CONCLUSIONS: Although there was high bacterial resistance to metronidazole, the absence of resistance particularly to the key antibiotics used in H. pylori eradication therapy: clarithromycin and levofloxacin is reassuring to note. Continued monitoring of antibiotic resistance should be carried out.
Helicobacter pylori eradication with short-term therapy leads to duodenal ulcer healing without the need for continued acid suppression therapy

Goh KL, Navaratnam P, Peh SC, Wong NW, Chuah SY, Rahman NA, et al.

Eur J Gastroenterol Hepatol, 1996 May;8(5):421-3.
PMID: 8804868

To determine whether duodenal ulcers continue to heal following successful Helicobacter pylori eradication with short-term eradication therapy without further acid suppression therapy.
HUITAI rapid urease test: a new ultra-rapid biopsy urease test for the diagnosis of Helicobacter pylori infection

Goh KL, Cheah PL, Navaratnam P, Chin SC, Xiao SD

J Dig Dis, 2007 Aug;8(3):139-42.
PMID: 17650225

The gastric biopsy urease test is an accurate and robust diagnostic test for Helicobacter pylori infection. Large endoscopy units use their own homemade unbuffered ultra-rapid urease test for diagnosis of H. pylori infection but several commercial rapid urease tests are available.
Exotoxin profiles of clinical isolates of Aeromonas hydrophila

Vadivelu J, Puthucheary SD, Navaratnam P

J Med Microbiol, 1991 Jun;34(6):363-7.
PMID: 2056519

Eighty-six clinical isolates of Aeromonas hydrophila were studied for their ability to produce four exotoxins: a haemolysin active against rabbit erythrocytes, cytotoxin and enterotoxin detectable with Vero cell cultures, and the cholera toxin-like factor detected by an enzyme-linked immunosorbent assay. At least one exotoxin was produced by 80% of enteric and 96% of non-enteric isolates. The exotoxin profiles of non-enteric isolates were more restricted than those of enteric isolates, with haemolysin and cytotoxin producers preponderant. Although haemolysin and cytotoxin were produced by isolates from all sources, the enterotoxin and cholera toxin-like factor were more common amongst enteric isolates. The production of haemolysin and cytotoxin were closely related but the association between the enterotoxin and the cholera toxin-like factor was not significant.
Evaluation of the routine use of the anaerobic bottle when using the BACTEC blood culture system

Karunakaran R, Raja NS, Quek KF, Hoe VC, Navaratnam P

J Microbiol Immunol Infect, 2007 Oct;40(5):445-9.
PMID: 17932606

The established practice of sending blood cultures in an aerobic-anaerobic pair of bottles has been questioned in recent years, and this study was conducted to evaluate the routine use of an anaerobic bottle in the BACTEC blood culture set at the University of Malaya Medical Centre, Kuala Lumpur, from January to December 2004. A total of 11,663 paired blood culture sets were received, of which 3326 were from pediatric patients and 8337 were from adult patients. The overall positive isolation rate was 15%; the positive isolation rate on excluding the anaerobic bottles was 13%. Overall, there were significantly more organisms isolated from the aerobic bottle (p<0.05); however, the best yield was obtained on using the paired aerobic-anaerobic bottles. Among the positive blood culture sets, organisms were isolated from the anaerobic bottle alone in 15.2% of the pediatric sets and in 18.1% of the adult sets. Organisms that grew more frequently in the anaerobic bottle were anaerobes and some facultative anaerobes; however, the difference was not statistically significant except for anaerobes in the adult sets. We recommend that when culturing blood, an aerobic-anaerobic pair of bottles be used rather than an aerobic-aerobic pair, to optimize the recovery of a wider spectrum of organisms, including obligatory anaerobes.
Evaluation of the monoclonal stool antigen test for Helicobacter pylori in an Asian population with dyspepsia

Bhewa Y, Hilmi I, Cheah PL, Navaratnam P, Goh KL

J Dig Dis, 2007 Nov;8(4):207-10.
PMID: 17970878

Although well established in the West, stool antigen tests (SAT) are not widely used in Asia. Data on the accuracy of this test in Asia is sparse and, to date, there have been no studies looking at the more refined monoclonal SAT. The aim of this study is to validate the diagnostic accuracy of a stool antigen test, Hp STAR, for the detection of Helicobacter pylori.

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