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 Table of Contents  
Year : 2018  |  Volume : 2  |  Issue : 2  |  Page : 56-61

Bacillus cereus as an emerging public health concern in Libya: Isolation and antibiogram from food of animal origin

1 Department of Food Hygiene and Control Faculty of Veterinary Medicine, University of Tripoli, Tripoli, Libya
2 Department of Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Tripoli, Tripoli, Libya
3 Department of Food Hygiene and Control, Faculty of Veterinary Medicine, Suez Canal University, Ismailia, Egypt
4 Department of Food Hygiene and Control, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt
5 Department of Genomics, The Lombardy and Emilia Romagna Experimental Zootechnic Institute (IZSLER), Brescia, Italy

Date of Web Publication29-Jun-2018

Correspondence Address:
Prof. Ibrahim M Eldaghayes
Department of Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Tripoli, P. O. Box 13662, Tripoli
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/LJMS.LJMS_5_18

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Background: This study was conducted to investigate the presence of Bacillus cereus in meat, meat products, and some seafood in Libya. Materials and Methods: One hundred and thirty-one samples were collected from different geographic localities in Libya. The samples were subjected to microbiological analysis for enumeration and isolation of B. cereus by conventional cultural, biochemical, and molecular identification using polymerase chain reaction (PCR) and partial sequencing of 16S rDNA techniques. Results: Of 131 samples, only 38 (29%) isolates were found to be B. cereus based on their cultural characteristics on Mannitol Egg-Yolk Polymyxin (MYP) medium that included 30% beef, 38.2% beef products (minced, burger, kabab, and sausage), 31.8% camel meat, and 48% chicken products (burger, sausage, kabab, and liver). However, B. cereus was not detected from mutton and seafood samples. Seventeen isolates were subjected to molecular identification using PCR and partial sequencing of 16S rDNA technique and confirmed to be B. cereus. The confirmed B. cereus strains were tested for their antibiotic sensitivity profiles and showed a high percentage of multiresistance phenotype. Conclusions: The results provide a better understanding of B. cereus isolated from food of animal origin in Libya and suggest that meat and meat products might play an important role in the spreading of B. cereus through the food chain with antimicrobial resistance characteristics.

Keywords: 16S rDNA, antibiogram, Bacillus cereus, Libya, meat products

How to cite this article:
Naas HT, Zurghani MM, Garbaj AM, Azwai SM, Eshamah HL, Gammoudi FT, Abolghait SK, Moawad AA, Barbieri I, Eldaghayes IM. Bacillus cereus as an emerging public health concern in Libya: Isolation and antibiogram from food of animal origin. Libyan J Med Sci 2018;2:56-61

How to cite this URL:
Naas HT, Zurghani MM, Garbaj AM, Azwai SM, Eshamah HL, Gammoudi FT, Abolghait SK, Moawad AA, Barbieri I, Eldaghayes IM. Bacillus cereus as an emerging public health concern in Libya: Isolation and antibiogram from food of animal origin. Libyan J Med Sci [serial online] 2018 [cited 2023 Mar 26];2:56-61. Available from: https://www.ljmsonline.com/text.asp?2018/2/2/56/235697

  Introduction Top

Bacillus cereus is a Gram-positive, rod-shaped, large size in single or short chains, facultative anaerobes, motile, β-hemolytic and mesophilic bacteria that produce heat-resistant endospores with a growth range of 10°C–48°C, with optimal growth at 28°C–35°C. In addition, it can grow in a broad pH range of 4.9–9.3.[1],[2] It is a ubiquitous microorganism found in soils, water, dust, plants, animals, and humans. It is also isolated from contaminated foods of both plant and animal origins such as cereals, vegetables, milk and milk products, and meat and meat products causing foodborne illnesses in humans.[3] The occurrence of B. cereus as a meat contaminant was reported by some investigators, not only in raw meat but also in meat products.[4],[5],[6]

B. cereus has been isolated from the stools of 43% of healthy children and adults, at various concentrations.[7]B. cereus is an important foodborne pathogen, which causes two distinct types of food poisoning, i.e., diarrhea and emesis caused by two different types of toxins.[8],[9] Three types of enterotoxins are associated with the diarrheal form of disease: three-component enterotoxin hemolysin BL, three-component nonhemolytic enterotoxin, and the single-component enterotoxin cytotoxin K. After consumption of contaminated food with B. cereus, the enterotoxins are released into the small intestine during vegetative growth following spore germination and by any surviving vegetative cells.[10] The diarrheal syndrome is caused by diarrheal toxins produced during the growth of the bacteria in the small intestine, while emetic syndrome is caused by emetic toxin produced by the bacteria during the growth phase in the food.[11] The incidence of the disease data related to B. cereus is extremely limited in Libya, because the disease associated with B. cereus may be underreported as very few of those affected seek medical attention owing to the mild nature and short duration of symptoms.[12]B. cereus was reported as a major causative agent of foodborne illness in the Netherlands in 2006 (causing 5.4% of the foodborne outbreaks) and in Norway in 2000 (causing 32% of foodborne outbreaks).[13] Scallan et al.[14] estimated that in the United States (US), B. cereus caused 0.7% of foodborne illness among 31 major pathogens. The Centers for Disease Control and Prevention reported on domestically acquired foodborne illness in the US that estimated number of episodes of B. cereus illness annually was given as 63,400 cases. Other outbreaks may go unreported or are misdiagnosed because of symptomatic similarities to Staphylococcus aureus intoxication (B. cereus vomiting type) or Clostridium perfringens food poisoning (B. cereus diarrheal type). The objectives of this study were to enumerate and isolate B. cereus from meat and meat products of different animal species and some seafood from different areas in Libya, to compare the cultural and molecular techniques as a tool for B. cereus confirmation, and to test the confirmed isolates for their antimicrobial susceptibility.

  Materials and Methods Top

Collection and preparation of samples

A total of 131 samples [Table 1] including 49 raw meat samples of different species (beef, camel, chicken, and mutton), 59 meat products (beef products [minced, burger, kabab, and sausage] and chicken products [burger, kabab, sausage, and liver]), and 23 seafood (fish, clam, and shrimp), were collected from different cities in Libya (Tripoli, Regdalin, Janzour, and Tobruk). The samples were packed in sterile plastic bags, stored in an insulated icebox, and transferred to Food Hygiene and Control Laboratory Department, Faculty of Veterinary Medicine, University of Tripoli, on the same day of sample collection. All samples were subjected to B. cereus microbiological enumeration and isolation techniques followed by molecular identification by polymerase chain reaction (PCR) and partially sequencing of 16S rDNA. Decimal dilutions, culturing, and enumeration techniques of the samples were performed according to the methods described by the American Public Health Association.[15] Briefly, 25 g from each sample was aseptically transferred into a sterile stomacher bag (Seward Medicals, UK) and homogenized (Stomacher 400, Seaward Medicals, UK) with 225 mL of sterile 0.1% (w/v) peptone water (Park Scientific, UK) at 230 rpm for 2 min.
Table 1: Bacillus cereus in meat, meat products, and seafood samples (CFU/g)

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Enumeration and isolation of Bacillus cereus

Enumeration and isolation of B. cereus were performed using B. cereus selective differential MYP Agar Base (Park Scientific ltd. Co., UK).[16] MYP plates were surface plated by spreading of 0.1 mL of appropriate tissue homogenate serial dilutions and then incubated at 37°C for 24 h. MYP plates were examined for the presence of colonies surrounded by precipitate zone, which indicates that lecithinase is produced. B. cereus colonies are usually a pink color surrounded by precipitate zone with the same color [Figure 1]. Countable plates were those containing 15–150 colonies.[17]
Figure 1: (a and b) Typical colonies of Bacillus cereus grown on Mannitol Egg-Yolk Polymyxin agar plate (pink colonies surrounded by a zone of precipitation [lecithinase-positive], after overnight incubation at 37°C])

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Identification of Bacillus cereus by polymerase chain reaction and partial sequencing of 16S rDNA

Seventeen randomly selected positive B. cereus isolates on MYP medium were sent for sequencing of partial amplification 16S rDNA (464 bp) of isolated B. cereus strains using the universal oligonucleotide primers.

DNA extraction and amplification of 16S rDNA

DNA extraction of B. cereus isolates was performed by GF-1 bacterial DNA extraction kit (Cat. # GF-BA-100, Vivantis, Malaysia) as described in a previous study.[18] The 16S rDNA was amplified using the universal oligonucleotide primers; forward: S-D-Bact-0341-b-S-17 5′-CCTACGGGNGGCWGCAG-3′ and Reverse: S-D-Bact-0785-a-A-21 5′-GACTACHVGG GTATCTAATCC-3′.[19]

Electrophoresis, gel extraction, and DNA sequencing

The amplified 16S rDNA PCR fragment (464 bp) was excised from the gel, and the DNA was purified using GF-1 Ambi Clean kit (Cat. # GF-GC-100, Vivantis, Malaysia) as described previously.[18] The purified 16S rDNA amplicons underwent cycle sequencing with BigDye® Terminator v1.1 kit (AB Applied Bioscience, TECHNE, TC-512, USA) and were sequenced on four capillary ABI PRISM® 3130-Avant Genetic Analyzer at IZSLER Istituto Zooprofilattico Sperimentale Della Lombardia e dell'Emilia Romagna, Italy. Sequences were assembled and edited using the SeqMan module within Lasergene package (DNA Star Inc., Madison, WI, USA). The obtained consensus sequences were subjected to BLAST search both at NCBI (http://www.ncbi.nlm.nih.gov/pubmed) and at 16S bacterial cultures Blast Server for the identification of prokaryotes (http://bioinfo.unice.fr/blast/).

Biochemical identification of isolated strains

The identified B. cereus strains by PCR technique were examined for their typical biochemical reactions (hemolysin, lecithinase, sugar fermentation: arabinose, mannitol, and xylose).[20]

Strains preparation for antibiogram

On confirmation by PCR and partial sequencing of 16S rDNA gene, isolated strains of B. cereus were preserved by freezing at −80°C in vials containing brain–heart Infusion broth (BHI, Oxoid, UK) supplemented with 30% (v/v) glycerol (DBH, UK). To propagate the frozen culture, vial was thawed at room temperature, and 0.5 mL of thawed culture was transferred to 5 mL of BHI broth and incubated for 24 h at 37°C. The inoculum was prepared from the second transfer of that culture (0.5 mL) to another 5 mL of BHI broth then incubated for 16–18 h at 37°C.

Antibiogram assay

After the overnight incubation of tested strain, Mueller Hinton agar plates (Oxoid, UK) were surface swabbed.[21] The selection of antibiotics (24) was based on their common use in human and animals which included amoxycillin (10 μg), amoxycillin/clavulanic acid (30 μg), ampicillin (10 μg), bacitracin (10 μg), penicillin G (10 μg), methicillin (5 μg), erythromycin (15 μg), gentamicin (10 μg), kanamycin (30 μg), lincomycin (10 μg), tobramycin (10 μg), vancomycin (10 μg), levofloxacin (5 μg), clindamycin (2 μg), cefotaxime (30 μg), doxycycline (30 μg), ciprofloxacin (5 μg), cloxacillin (5 μg), nitrofurantoin (300 μg), oxytetracycline (30 μg), streptomycin (10 μg), tetracycline (30 μg), chloramphenicol (30 μg), and sulfamethoxazole/trimethoprim (25 μg). All antibiotics used were obtained from Oxoid, except gentamicin (10 μg) and methicillin (5 μg) which were obtained from Bioanalyse, Turkey. Under aseptic condition, antibiotic discs were dispensed and lightly pressed onto the agar surface and then incubated overnight at 37°C. The bacterial growth around each disc was observed. The clear zones around antibiotic discs that have no growth, referred to as the zone of inhibition, were measured and scored as sensitive, intermediate (reduced susceptibility), or resistant according to the CLSI 2014 guidelines.[22] The antibiotic resistance index (ARI) and multiple antibiotic resistance (MAR) index for all the isolated bacteria were calculated as follows:[23],[24]


and interpreted according to Krumperman.[24] MAR index ≤0.2 was considered low risk and ≥0.2 was considered as high risk.

  Results Top

Enumeration and isolation of Bacillus cereus

One hundred and thirty-one samples from various regions of Libya comprising raw meat (49), meat products of different species (59), and seafood (23) were tested for the presence of B. cereus using MYP medium [Figure 1]. B. cereus was isolated from 41 samples of raw meat (beef, chicken, and camel meat) – 30%, 33.3%, and 31.8% with mean counts 8 × 103, 1.2 × 103, and 4.4 × 104 CFU/g, respectively. B. cereus was not isolated from mutton and seafood samples. For meat products (59), isolation rate of B. cereus on MYP agar plates of beef product samples was 38.2% with counts ranging from 9 × 102 to 2.7 × 104 CFU/g and of chicken meat products was 48% with counts ranging from 6.4 × 102 to 2.1 × 104 CFU/g [Table 1] and [Table 2]. The occurrence of B. cereus was 25% in beef burger with mean count of 7.6 × 103 CFU/g. Meanwhile, in beef kabab, the isolation rate was 80% [Table 2] with mean count of 2 × 104 CFU/g. Detection of B. cereus in chicken burger was 30% with mean count of 8.7 × 103 CFU/g. However, in chicken kabab, the incidence rate was 60% with mean count of 1.9 × 104 CFU/g.
Table 2: Prevalence of suspected Bacillus cereus in meat, meat products, and seafood samples

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Identification of Bacillus cereus

Of 38 suspected B. cereus isolates from MYP plates, 17 (45%) were randomly selected [Table 2] and sent for partial sequencing of 16S rDNA (464 bp) of B. cereus using the universal oligonucleotide primers [Figure 2]. All seventeen suspected isolates were confirmed to be B. cereus by partial sequencing of 16S rDNA technique.
Figure 2: Representative gel of partial amplification of 16S rDNA (464 bp) products of isolated Bacillus cereus strains using the universal oligonucleotide primers. First and last lanes contain DNA marker

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Antibiotic resistance phenotype

All confirmed B. cereus isolates showed resistance to amoxycillin, amoxicillin/clavulanic acid, ampicillin, bacitracin, penicillin G, cefotaxime, and cloxacillin, while 94% of isolates were resistant to lincomycin and 88% to methicillin and sulfamethoxazole/trimethoprim. However, more than 80% of the isolates were sensitive to gentamicin, tobramycin, vancomycin, ciprofloxacin, nitrofurantoin, tetracycline, and chloramphenicol. Levofloxacin and doxycycline were effective against all tasted isolates. The calculated ARI for the tested isolates was 0.03, while the MAR indicates MDR [Table 3].
Table 3: Antibiogram Results for 17 Bacillus cereus isolated form meat and meat products

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  Discussion Top

Fresh raw meat and meat products are susceptible to biochemical changes due to the microbial growth at ambient temperatures 20°C–35°C, which are high in some countries (Libya). The meat products should be kept at low temperature (refrigerating or freezing) to extend their shelf life.[25]

In general, the incidence of B. cereus all over the collected samples of beef and beef products was 36.4% (16/44) [Table 2]. The results of this study are similar to the results obtained by Tewari [26] (27.8%). Whereas the results of other studies were very low compared to the results of this study as that with Konuma [27] (6.6%) and Perera and Ranasinghe [28] (1%). These differences may be due to the exposure to many sources of contamination during slaughtering, dressing and storage process. Currently, no data have been published on the incidence of B. cereus in camel meat as recorded in this study. The incidence of B. cereus in camel meat was 31.8% (7/22) with count ranged from 3.5 × 103 to 8.5 × 104 with mean value of 4.4 × 104 ± 4 × 104 CFU/g. This study failed to detect B. cereus strains from mutton samples that may be due to low bacterial load. Meanwhile, Akhlaq [29] isolated B. cereus from both goat and mutton samples and noted that the level of B. cereus was highest among all species of studied bacteria and significantly greater than the other pathogenic strains found in mutton and goat meat samples.

The incidence of B. cereus in beef kabab and minced beef was less than the results obtained by Fang et al.[30] Smykal and Rokoszewska [31] indicated that over a 7-year period (1964–1971), the prevalence of B. cereus was 13.3% in meat and meat products. The incidence and count of B. cereus in the beef sausage samples were in agreement with the data reported by Nortjé et al.[32] The results recorded by Eglezos et al.[12] for cooked sausage rolls were lower compared with the results obtained from this study. However, it has been proved that the occurrence rate of B. cereus is often much higher in raw or undercooked products compared with cooked ones because of the absence of heating process in order to reduction of microbial load.[33] These differences as a high incidence in the current investigation in red meat products may also be due to cross-contamination during production and preparation of meat or due to type of preparation of the product, defects in hygienic measures, or kind of additives and spices.[20]

In general, the incidence of B. cereus in chicken meat samples was lower than the results recorded by Sharma et al.,[34] and greater than the results reported by Nortjé et al.[32] The results in this study were similar with the results reported by Perera and Ranasinghe.[28] Furthermore, the incidence of B. cereus in chicken products (kabab, sausage, and liver) was high compared to the results reported by Raja et al.,[35] whereas the results reported by Sooltan et al.[36] were lower than that of the current study. On the other hand, the results recorded by Abostate et al.[37] were similar to the results of this study, except in minced chicken. The results of this study were lower than that found by Smith et al.[38] These variations in the results were attributed to the quality of raw materials and the hygienic state during preparation and processing of the product. The presence of B. cereus in processed poultry products is due to surviving of spores from raw poultry and added ingredients and contamination with either spores or cells during processing.[20]

All of 17 randomly selected positive B. cereus isolates on MYP medium that sent for sequencing of partial amplification 16S rDNA (464 bp) of isolated B. cereus strains using the universal oligonucleotide primers were identified as B. cereus (100%) by PCR technique. These results showed that MYP media could be used as selective and differential media for B. cereus because no other microorganism could grow on it. In another study, among the 150 food samples (raw meats and meat products) analyzed, 40% (60) were positive for isolation and 39.33% (59) turned out positive by direct PCR (targeting sequence within gyrB gene).[39]

Regarding antibiotic susceptibility, all isolated strains of B. cereus in this study from meat and meat products were resistant to 7 out of 24 (29%) antibiotics and β-lactam antibiotics were not effective in all B. cereus isolates similar to other published data.[34],[40] Of 24 antibiotics, 2 (8.3%) were highly effective against all isolates characterized in this study (levofloxacin and doxycycline); this finding was lower than the sensitivity percentage of doxycycline 88.23% reported by Luna et al.,[41] but levofloxacin sensitivity was similar. The current results showed that the β-lactam antibiotics were not effective in all B. cereus isolates as a consequence of β-lactamase action which secreted by B. cereus also in the presence of clavulanic acid, but amoxycillin/clavulanic acid was highly sensitive as confirmed by Pirzada et al.[42] The results obtained from this study showed multidrug resistance of B. cereus isolates according to the data published by Floriştean et al.[20] Variations in the percentages of susceptibility to antibiotics may be due to the differences in the concentrations of antibiotic agents, differences in the sources of isolates, drug resistance transfer, and the widespread misuse of the antibiotics in the field.[43]

  Conclusions Top

Our results showed that the isolation of B. cereus from Libyan meat and meat products of different species and some seafood represents an important aspect for food safety. The results provide a better understanding of B. cereus isolated from food of animal origin in Libya and suggest that meat and meat products might play an important role in the spreading of B. cereus through the food chain with antimicrobial resistance characteristics. This high incidence in meat products could be attributed to low hygienic practices, contaminated additives, and cross-contamination during the preparation of such products. Thus, hygienic slaughter of animals in slaughterhouses could improve the safety of carcasses and raw meat used in meat product formulation.

Financial support and sponsorship

This research was part of a project titled "Genetic authentication of bacterial isolates from meat and milk products in Libya and establishing the FLBC" that was supported by a grant provided by Authority of Natural Science Research and Technology (Former name: The Libyan Authority for Research, Science and Technology).

Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Table 1], [Table 2], [Table 3]

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