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Corrigendum: Floricoccus tropicus gen. nov., sp. nov. and Floricoccus penangensis sp. nov. isolated from fresh flowers of durian tree and hibiscus

Chuah LO, Yap KP, Shamila-Syuhada AK, Thong KL, Ahmad R, Liong MT, et al.

Int J Syst Evol Microbiol, 2018 03;68(3):974.
PMID: 29493487 DOI: 10.1099/ijsem.0.002582
Genetic relatedness, antimicrobial resistance and biofilm formation of Salmonella isolated from naturally contaminated poultry and their processing environment in northern Malaysia

Chuah LO, Shamila Syuhada AK, Mohamad Suhaimi I, Farah Hanim T, Rusul G

Food Res Int, 2018 03;105:743-751.
PMID: 29433269 DOI: 10.1016/j.foodres.2017.11.066

We investigated the genetic relatedness, antibiotic resistance and biofilm-producing ability of 114 strains of Salmonella, belonged to three serotypes (Corvallis, Brancaster and Albany), isolated from naturally contaminated poultry and their environment in wet markets and smale-scale processing plant from northern Malaysia. Pulsed-field gel electrophoresis revealed that Salmonella strains isolated from various wet markets were clonally related, suggesting the widespread dissemination of these three serotypes in northern Malaysia. All except one strain of Salmonella were resistant to more than two classes of antibiotics, hence regarded as multidrug resistant (MDR). Resistance to sulphonamide (96.5%), ampicillin (89.5%), tetracycline (85.1%), chloramphenicol (75.4%), trimethoprim (68.4%), trimethoprim-sulfamethoxazole (67.5%), streptomycin (58.8%) and nalidixic acid (44.4%) were observed. Resistance determinants, floR, cmlA, tetA, tetB, tetG, temB, blaPSE-1, sul1, sul2, qnrA, qnrS, strA and aadA were detected by PCR among MDR Salmonella strains. Seventy-six strains (66.7%) harboured class-I integrons. The gene cassettes identified were dfrA1, dfrA12, aadA2 and an open reading frame orfC with unknown function. All Salmonella strains produced biofilm and 69.3% of them were strong biofilm-producers. Our findings suggested that most likely, persistent Salmonella colonises various sites in the processing environment by producing biofilm, which leads to their widespread dissemination in wet markets located in northern Malaysia.
Fulltext Data on antibiogram and resistance genes harboured bySalmonellastrains and their Pulsed-field gel electrophoresis clusters

Chuah LO, Shamila Syuhada AK, Mohamad Suhaimi I, Farah Hanim T, Rusul G

Data Brief, 2018 Apr;17:698-702.
PMID: 29511712 DOI: 10.1016/j.dib.2018.01.098

This article describes the Pulsed-field gel electrophoresis clustering of the predominantSalmonellastrains (Salmonellaser. Albany,Salmonellaser. Brancaster, andSalmonellaser. Corvallis) isolated from poultry and processing environment in wet market and small-scale processing plant in Penang and Perlis, the northern states of Malaysia. Agar disk diffusion assay was performed to determine the phenotypic antibiotic resistance of theseSalmonellastrains. The most common antibiograms among the three predominantSalmonellaserovars were reported. The presence of integrase genes and antibiotic resistance genes conferring to resistance against β-lactams, aminoglycosides, tetracyclines, quinolones, sulphonamides and chloramphenicol, was detected via PCR amplification.
Physio-chemical, microbiological properties of tempoyak and molecular characterisation of lactic acid bacteria isolated from tempoyak

Chuah LO, Shamila-Syuhada AK, Liong MT, Rosma A, Thong KL, Rusul G

Food Microbiol, 2016 Sep;58:95-104.
PMID: 27217364 DOI: 10.1016/j.fm.2016.04.002

This study aims to determine physio-chemical properties of tempoyak, characterise the various indigenous species of lactic acid bacteria (LAB) present at different stages of fermentation and also to determine the survival of selected foodborne pathogens in tempoyak. The predominant microorganisms present in tempoyak were LAB (8.88-10.42 log CFU/g). Fructobacillus durionis and Lactobacillus plantarum were the dominant members of LAB. Other LAB species detected for the first time in tempoyak were a fructophilic strain of Lactobacillus fructivorans, Leuconostoc dextranicum, Lactobacillus collinoides and Lactobacillus paracasei. Heterofermentative Leuconostoc mesenteroides and F. durionis were predominant in the initial stage of fermentation, and as fermentation proceeded, F. durionis remained predominant, but towards the end of fermentation, homofermentative Lb. plantarum became the predominant species. Lactic, acetic and propionic acids were present in concentrations ranging from 0.30 to 9.65, 0.51 to 7.14 and 3.90 to 7.31 mg/g, respectively. Genotyping showed a high degree of diversity among F. durionis and Lb. plantarum isolates, suggesting different sources of LAB. All tested Lb. plantarum and F. durionis (except for one isolate) isolates were multidrug resistant. Salmonella spp., Listeria monocytogenes and Staphylococcus aureus were not detected. However, survival study showed that these pathogens could survive up to 8-12 days. The results aiming at improving the quality and safety of tempoyak.
Fulltext Genetic Relatedness of Salmonella Serovars Isolated from Catfish (Clarias gariepinus) and Tilapia (Tilapia mossambica) Obtained from Wet Markets and Ponds in Penang, Malaysia

Budiati T, Rusul G, Wan-Abdullah WN, Chuah LO, Ahmad R, Thong KL

J Food Prot, 2016 Apr;79(4):659-65.
PMID: 27052872 DOI: 10.4315/0362-028X.JFP-15-372

A total of 43 Salmonella enterica isolates belonging to different serovars (Salmonella Albany, Salmonella Agona, Salmonella Corvallis, Salmonella Stanley, Salmonella Typhimurium, Salmonella Mikawasima, and Salmonella Bovismorbificans) were isolated from catfish (Clarias gariepinus) and tilapia (Tilapia mossambica) obtained from nine wet markets and eight ponds in Penang, Malaysia. Thirteen, 19, and 11 isolates were isolated from 9 of 32 catfish, 14 of 32 tilapia, and 11 of 44 water samples, respectively. Fish reared in ponds were fed chicken offal, spoiled eggs, and commercial fish feed. The genetic relatedness of these Salmonella isolates was determined by random amplified polymorphic DNA PCR (RAPD-PCR) using primer OPC2, repetitive extragenic palindromic PCR (REP-PCR), and pulsed-field gel electrophoresis (PFGE). Composite analysis of the RAPD-PCR, REP-PCR, and PFGE results showed that the Salmonella serovars could be differentiated into six clusters and 15 singletons. RAPD-PCR differentiated the Salmonella isolates into 11 clusters and 10 singletons, while REP-PCR differentiated them into 4 clusters and 1 singleton. PFGE differentiated the Salmonella isolates into seven clusters and seven singletons. The close genetic relationship of Salmonella isolates from catfish or tilapia obtained from different ponds, irrespective of the type of feed given, may be caused by several factors, such as the quality of the water, density of fish, and size of ponds.
Microbiology of Chili Bo, a Popular Malaysian Food Ingredient

Leisner JJ, Rusul G, Wee BW, Boo HC, Muhammad K

J Food Prot, 1997 Oct;60(10):1235-1240.
PMID: 31207722 DOI: 10.4315/0362-028X-60.10.1235

The predominant microbial flora of a specific Malaysian food ingredient, chili bo (containing 9% ground dried chilies, 0.6% acetic acid, and 5 to 10% cornstarch, wt/vol) stored for up to 25 days at 28°C without added benzoic acid (product A) and with 7,000 ppm of added benzoic acid (product B) was examined. Aerobic plate counts for both products were initially 6.2 to 6.5 log CFU/g increasing to 8.5 log CFU/g for product A after 4 days. Aerobic plate counts for product B did not increase during storage. Lactic acid bacteria (LAB) counts increased in product A from 4.8 log CFU/g to 8.3 log CFU/g and in product B from 2.1 log CFU/g to 7 .6 log CFU/g after 17 days. Growth of yeast occurred in product A. Both products exhibited spoilage after 1 to 2 days of storage at 28°C indicated as accumulation of gas bubbles. In addition surface growth of molds (product A) or whitish discoloration (product B) was observed later in storage. For product A the predominant isolates were LAB, Bacillus pumilus , Bacillus subtilis , Staphylococcus spp., and yeasts. B. pumilus and B. subtilis predominated initially whereas the other types of microorganisms predominated after 25 days of storage. B. pumilus and B. subtilis were also predominant in product B, but after 25 days of storage a homofermentative LAB was found in higher numbers (7.6 log CFU/g). Isolates of heterofermentative LAB but not homofermentative LAB or B. pumilus or B. subtilis were able to produce gas during growth in chili bo sterilized by autoclaving at l2l°C for 15 min. Growth of heterofermentative LAB, B. pumilus , and B. subtilis was inhibited by acidifying agents, a nisin-containing supernatant, or incubation at low temperatures.
Genetic diversity of clinical and environmental strains of Salmonella enterica serotype Weltevreden isolated in Malaysia

Thong KL, Goh YL, Radu S, Noorzaleha S, Yasin R, Koh YT, et al.

J Clin Microbiol, 2002 Jul;40(7):2498-503.
PMID: 12089269

The incidence of food-borne salmonellosis due to Salmonella enterica serotype Weltevreden is reported to be on the increase in Malaysia. The pulsed-field gel electrophoresis (PFGE) subtyping method was used to assess the extent of genetic diversity and clonality of Salmonella serotype Weltevreden strains from humans and the environment. PFGE of XbaI-digested chromosomal DNA from 95 strains of Salmonella serotype Weltevreden gave 39 distinct profiles with a wide range of Dice coefficients (0.27 to 1.00), indicating that PFGE is very discriminative and that multiple clones of Salmonella serotype Weltevreden exist among clinical and environmental isolates. Strains of one dominant pulsotype (pulsotype X1/X2) appeared to be endemic in this region, as they were consistently recovered from humans with salmonellosis between 1996 and 2001 and from raw vegetables. In addition, the sharing of similar PFGE profiles among isolates from humans, vegetables, and beef provides indirect evidence of the possible transmission of salmonellosis from contaminated raw vegetables and meat to humans. Furthermore, the recurrence of PFGE profile X21 among isolates found in samples of vegetables from one wet market indicated the persistence of this clone. The environment in the wet markets may represent a major source of cross-contamination of vegetables with Salmonella serotype Weltevreden. Antibiotic sensitivity tests showed that the clinical isolates of Salmonella serotype Weltevreden remained drug sensitive but that the vegetable isolates were resistant to at least two antibiotics. To the best of our knowledge, this is the first study to compare clinical and environmental isolates of Salmonella serotype Weltevreden in Malaysia.
Detection of Escherichia coli O157:H7 in the beef marketed in Malaysia

Radu S, Abdul Mutalib S, Rusul G, Ahmad Z, Morigaki T, Asai N, et al.

Appl Environ Microbiol, 1998 Mar;64(3):1153-6.
PMID: 9501454

Twelve strains of Escherichia coli O157:H7 were isolated from 9 of 25 beef samples purchased from retail stores in Malaysia. These strains produced Shiga toxin 2 with or without Shiga toxin 1 and had the eae gene and a 60-MDa plasmid. The antibiograms and the profiles of the arbitrarily primed PCR of the strains were diverse, suggesting that the strains may have originated from diverse sources.
Identification of lactic acid bacteria from chili bo, a Malaysian food ingredient

Leisner JJ, Pot B, Christensen H, Rusul G, Olsen JE, Wee BW, et al.

Appl Environ Microbiol, 1999 Feb;65(2):599-605.
PMID: 9925588

Ninety-two strains of lactic acid bacteria (LAB) were isolated from a Malaysian food ingredient, chili bo, stored for up to 25 days at 28 degreesC with no benzoic acid (product A) or with 7,000 mg of benzoic acid kg-1 (product B). The strains were divided into eight groups by traditional phenotypic tests. A total of 43 strains were selected for comparison of their sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) whole-cell protein patterns with a SDS-PAGE database of LAB. Isolates from product A were identified as Lactobacillus plantarum, Lactobacillus fermentum, Lactobacillus farciminis, Pediococcus acidilactici, Enterococcus faecalis, and Weissella confusa. Five strains belonging to clusters which could not be allocated to existing species by SDS-PAGE were further identified by 16S rRNA sequence comparison. One strain was distantly related to the Lactobacillus casei/Pediococcus group. Two strains were related to Weissella at the genus or species level. Two other strains did not belong to any previously described 16S rRNA group of LAB and occupied an intermediate position between the L. casei/Pediococcus group and the Weissella group and species of Carnobacterium. The latter two strains belong to the cluster of LAB that predominated in product B. The incidence of new species and subspecies of LAB in chili bo indicate the high probability of isolation of new LAB from certain Southeast Asian foods. None of the isolates exhibited bacteriocin activity against L. plantarum ATCC 14917 and LMG 17682.
Detection of Vancomycin-Resistant Enterococcus Spp. (VRE) from Poultry

Toosa H, Radu S, Rusul G, Latif AR, Rahim RA, Ahmad N, et al.

Malays J Med Sci, 2001 Jan;8(1):53-8.
PMID: 22973157

Twenty-eight isolates of E. faecalis and 5 isolates of E. hirae were isolated from chicken samples obtained from markets in Sri Serdang, Selangor. They were tested for susceptibility to vancomycin and other antimicrobial agents. All of the isolates showed multiple resistance to the antibiotic tested. All Enterococcus spp. were resistant (100%) to ceftaxidime, cephalothin, erythromycin, gentamicin, kanamycin, nalidixic acid and streptomycin. Resistance was also observed to norfloxacin (97%), tetracycline (91%), penicillin (85%), bacitracin (82%), chloramphenicol (61%) and the least resistance was to ampicillin (27%). High prevalence to vancomycin resistance was detected among the E. faecalis (27of 28) and E. hirae (4 of 5) isolates. The multiple antibiotic resistance index ranging between 0.64 to 1.0 showed that all strains tested originated from high-risk contamination. Plasmid profile analysis of Enterococcus spp. revealed plasmid DNA bands ranging in size from 1.3 to 35.8 megadalton but some isolates were plasmidless. No correlation could be made between plasmid patterns and antibiotic resistance.
Fulltext Prevalence of Salmonella in poultry processing environments in wet markets in Penang and Perlis, Malaysia

Nidaullah H, Abirami N, Shamila-Syuhada AK, Chuah LO, Nurul H, Tan TP, et al.

Vet World, 2017 Mar;10(3):286-292.
PMID: 28435190 DOI: 10.14202/vetworld.2017.286-292

AIM: The aim of this study was to determine the prevalence of various Salmonella serotypes in chickens, carcass contact surfaces as well as environmental samples collected from wet markets and small scale processing plant.
MATERIALS AND METHODS: A total of 182 poultry and environmental samples were collected at random on separate occasions from wet markets and small scale processing plant, during the period of October 2014 to July 2015 in Penang and Perlis, Malaysia. The samples were analyzed for the presence of Salmonella using ISO 6579:2002 conventional culture-based method. Presumptive Salmonella colonies were subjected to various biochemical tests (such as triple sugar iron and lysine iron test), serologically confirmed using polyvalent O and H antisera and further serotyped at Public Health Laboratory, Ministry of Health, Perak, Malaysia.
RESULTS: Salmonella serotypes were isolated from 161 out of 182 samples (88.46%) with 100% prevalence in the whole chicken carcass and chicken cuts - as well as transport crate, cage, drum, knife, chopping board, display table, floor, bench wash water, wash water, and drain water. Salmonella was isolated from 91.67%, 83.33%, and 66.67% of defeathering machines, drain swabs, and apron, respectively. 17 serotypes were isolated in this study with Salmonella Albany (57/161), Salmonella Corvallis (42/161), and Salmonella Brancaster (37/161) being the predominant serovars.
CONCLUSION: The most carcass contact and environmental samples collected along the wet market chicken processing line were consistently contaminated with Salmonella. This indicates that Salmonella has established itself in poultry processing environments by colonizing the surfaces of the equipment and survives in these environments by establishing biofilms. Our results highlight the need of implementing strict hygiene and sanitation standards to reduce the incidence of Salmonella. The prevalence of Salmonella in poultry can be reduced effectively by identifying and eliminating the sources and contamination sites during slaughter and processing of poultry.

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