Public eating places like restaurants and canteens, fast foods, and popular foods on street have become today the major elements of urban development. They allow more than 80% of the cities’ populations to satisfy their nutritional needs . There is no law or legislation on the universities’ public restaurants. Despite their social-economic importance, the hygienic affairs in the common eating places systems are still a major worry for the consumers. In fact, taking into account the huge quantity of daily cooked foodstuffs, low instruction, and training of manpower, the hygiene rules are most of the time neglected in our African countries particularly, where the lower level of training is recorded .
If the universities’ public eating places are kept up and continue to grow, this means an increase in needs. However, the multiplication of serious food-infected diseases has been reported in recent years in several African countries, related to the proliferation of restaurants according to the WHO in 2009. Actually, more than 250 diverse diseases coming from food poisoning are described and the bacteria are reported to be the cause of 2/3 of these epidemics . Among the predominant bacteria, enterobacteria are involved in these diseases. Enterobacteria are the normal hosts found in human and animal digestive tubes .
Klebsiella pneumoniae is an important enterobacteria. It is an opportunistic pathogen causing several diseases and is acquiring resistance to several antibiotics [5,6]. This organism is responsible for about one-third of all Gram-negative infections such as urinary tract infections, cystitis, pneumonia, surgical wound infections, endocarditis, and septicemia [7–9]. It also causes necrotizing pneumonia, pyogenic liver abscesses, and endogenous endophthalmitis [10,11]. Klebsiella pneumoniae can be found in the respiratory and intestinal tracts of humans and animals. It is frequently isolated from foods, including fresh legumes, powder foods for babies, meats, fish, and street foods [12–14]. Infections with K. pneumoniae can be transmitted through contaminated food or water and can be associated with community-acquired infections or between persons and animals involved in hospital-acquired infections.
The emergence of antimicrobial resistance is causing serious health problems nowadays worldwide. In Côte d’Ivoire, bacteria resistance to antibiotics and the emergence of bacteria producing the ELSB are becoming a serious public health problem [15–17]. Some previous works had reportewd the presence and expansion of human enterobacteria strains producing ELSB [18,19]. Klebsiella pneumoniae has developed resistance to several antibiotics through the production of enzymes such as extended-spectrum β-lactamase (ESBLs) and carbapenemase [20,21]. The production of ESBLs is encoded by several genes such as blaSHV, blaTEM, and blaCTM [22,23].
The aim of this study was to determine the prevalence, identify the antimicrobial resistance genes, and determine the resistance profile of K. pneumoniae isolated from cooked and sold food samples.
2. MATERIALS AND METHODS
2.1. Sample Collection
This study was conducted from June to September 2017 and then from November 2017 to February 2018. It was carried out on 160 of cooked and sold food samples of rice and cassava powder called “attiéké,” fish soups, fried fish, and raw fresh vegetables collected from the public and private restaurants of the two main public universities, Nangui Abrogoua University (UNA) and Félix HouphouëtBoigny University (UFHB). The choice of the private collective restaurants was based on their attendance by the students and the choice of meals consumed by them. The samples were taken in sterile bowls and sent to the laboratory for analysis.
2.2. Isolation and Identification of K. pneumoniae
Ten (10) g of each sample was suspended in aseptic conditions in 90 ml of buffered peptone water previously autoclaved for 15 minutes at 121°C. The sample suspensions were homogenized for 30 seconds. From the suspension, a serial dilution was conducted up to 10−5. From each fold dilution, 0.1 ml was streaked directly onto VRBG agar plates and incubated for 24 hours at 37°C. Red violet colonies of 0.5 mm in size were transferred to nutrient agar plates. All the suspected K. pneumoniae isolates were checked for their Gram-staining reaction, indole production, and motility. The selected colonies were further identified by biochemical tests using API 20E kits (BioMérieux, France).
2.3. Molecular Characterization of Beta-Lactamase Genes
The presence of acquired extended-spectrum beta-lactamase genes (blaTEM, blaSHV, and blaCTX-M15) was investigated by multiplex polymerase chain reaction (PCR) assays. Representative colonies of K. pneumoniae were cultured on nutritive broth at 37°C for 24 hours. Then, the cell pellet was centrifuged at 13,000 rpmfor 10 minutes. The supernatant was discarded and 400 μl of lysed buffer was added to the cell pellet and then mixed for 1 minute. Three hundred microliters of chloroform was added and then mixed again for 1 minute. Twenty μl of sodium acetate and 400 μl of ethanol were added to the supernatant and incubated at −20°C for 1 hour. The mixture was centrifuged at 12,000 rpm for 10 minutes. The supernatant is discarded, and 200 μl of isopropanol was added to the cell pellet and then centrifuged at 12,000 rpm for 10 minutes. The next step was the elimination of alcohol by drying the pellet at room temperature or for 30 minutes. Finally, 50 μl of TE buffer was added to the pellet and incubated at −20°C until use. The total DNA in the supernatant was thereafter precipitated with 70% ethanol and used as the template for PCR.
All the oligonucleotide primers have been synthesized by Sangon Biotech (Table 1). The mixture (25 μl) used for PCR included 12.5 μl of Dream Taq TM Green PCR Master Mix (Fermentas, Waltham, MA), 2 μl of primers, and 3 μl of the template DNA. PCR amplification was carried out in a thermocycler, Bio-Rad PTC-200 (Bio-Rad, Hercules, CA), according to the following cycles: initial denaturation at 95°C for 5 minutes, followed by 40 cycles at 95°C for 30 seconds; for SHV gene, 40 cycles of hybridization for 30 seconds at 53°C; for TEM gene, 40 cycles of hybridization at 50°C for 30 seconds; for CTX-M-15 gene, 40 cycles of hybridization at 49°C for 30 seconds; and the initial elongation at 72°C for 1 minute and one final elongation cycle at 72°C for 5 minutes in a thermocycler. Klebsiella pneumoniae T300, obtained from Pasteur Institute of Abidjan, was used as a positive control. The amplified products were analyzed by electrophoresis on 1.5% agarose gel composed by Gold View (0.005% v/v) (SBS Genentech, Beijing, Chine) in Tris-buffered saline (TBS) buffer 1× (Tris-HCl 40 mM, 1,18 ml acetate acid, ethylenediaminetetraacetic acid (EDTA) 2 mM pH 8,0), and the bands were visualized using a system of capture, Image Quant 350 (GE Healthcare, Waukesha, WI).
|Table 1: Primers used for PCR amplification.|
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2.4. Antibiotic Susceptibility Tests
The susceptibility test of K. pneumoniae to antibiotics was determined on Mueller Hinton agar by diffusion method on disk Kirby–Bauer according to Clinical and Laboratory Standards Institute instructions. Commercially available antimicrobial discs that were used included amoxicillin (30 μg), amoxicillin + clavulanic acid (30 μg), ticarcillin + clavulanic acid (30 μg), ceftriaxone (30 μg), cefotaxime (30 μg), ertapenem (30 μg), gentamicin (15 μg), tetracycline (10 μg), and ciprofloxacin (30 μg). The measurement of the inhibition zone diameter around the antibiotic discs was carried out and compared with the Tables of international measurements.
|Table 2: Identification of enterobacteria.|
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3.1. Identification of K. pneumoniae
A total of 24 strains of K. pneumoniae out of 118 enterobacteria were isolated from cooked rice, “attiéké,” fried fish, fish soup, and raw fresh Vegetables (Table 2).
3.2. Contamination Rate of Food Samples with K. pneumoniae Isolates
The contamination rates of K. pneumoniae in cooked and sold food at the universities’ private and public restaurants are presented in Table 3. In total, 160 cooked food samples were tested in this study, and K. pneumoniae was isolated from 24 samples. Overall, 15% of the food samples were positive for K. pneumoniae. Klebsiella pneumoniae was isolated from 8.3% of rice samples, 20.8% of fish soup samples, 4.2% of “attiéké” samples, 37.5% of raw fresh vegetable samples, and 29.2% of fried fish samples.
At UNA, 13 (54.2%) K. pneumoniae strains were isolated from public and private restaurants. Klebsiella pneumoniae was mostly isolated from all the food samples: rice samples [2 (8.3%)], fish soup samples [4 (16.7%)], “attiéké” [1 (4.2%)], raw fresh vegetables [3 (12.5%)], and fried fish [1 (4.2%)] from private restaurants. Klebsiella pneumoniae was isolated only from fried fish samples [2 (8.3%)] from the public restaurant. At UFHB, 11 (45.8%) K. pneumoniae strains were isolated from public and private restaurants. Klebsiella pneumoniae was mostly isolated from three food samples fish soup samples [1 (4.2%)], raw fresh vegetables [2 (8.3%)], and fried fish [1 (4.2%)] from private restaurants. Klebsiella pneumoniae was isolated from two food samples, raw fresh vegetables [4 (16.7%)] and fried fish samples [3 (12.5%)] from public restaurants (Table 4).
|Table 3: Contamination rates of K. pneumoniae isolates from all the food samples.|
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|Table 4: Contamination rates of K. pneumoniae isolates per sold food from universities restaurants.|
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|Table 5: Contamination rates of K. pneumoniae isolates per sold food from private and public restaurants.|
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The contamination rates of K. pneumonia isolates per meal served in private and public restaurants were reported in Table 5. In the public restaurants, K. pneumoniae was isolated only from 2 (8.3%) and 7 (29.2%) of “attiéké”–vegetables–fried fish samples from UNA and UFHB, respectively. K. pneumonia was isolated from 6 (25%) of rice–fish soup samples and 5 (20.8%) of “attiéké”–vegetables–fried fish samples served in the private restaurants of UNA. Klebsiella pneumoniae was isolated from 1 (4.2%) of rice–fish–soup samples and 3 (12.5%) of “attiéké”–legume–fried fish samples served in the private restaurants of UFHB.
3.3. Antimicrobial Resistance Determinants of the K. pneumoniae Isolates
According to the results of antimicrobial susceptibility testing, 24 strains were tested for ESBL genes and 3 β-lactamase genes were amplified. As shown in Figure 1, 13 out of 24 strains isolated carried only the blaSHV gene. BlaTEM and blaCTX-M-15 genes were not detected in these isolates.
3.4. Antibiotic Resistance Profile of K. pneumoniae
Antimicrobial susceptibility testing was conducted for the 13K. pneumoniae isolates producing the blaSHV gene, and detailed information on the resistance rates to all of the tested antimicrobials is listed in Table 6. The susceptibility profile of K. pneumoniae strains revealed high resistances to beta-lactams: amoxicillin (92.3%), amoxicillin + clavulanic acid (76.9%), ticarcillin + clavulanic acid (76.9%), ceftriaxone (92.2%), cefotaxime (92.2%), and ceftazidime (92.2%). The resistance rates observed for the other antibiotics were 61.5% to aminosids and 92.2% to quinolones. None of the strains were resistant to tetracycline (84.7%) and ertapenem (67.9%).
|Table 6: Antimicrobial resistance rate of (n = 13) K. pneumoniae ESBL isolated. |
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|Figure 1: Electrophoretic profile indicating the presence of the gene in K. pneumoniae isolates MT: marker height (100–1,000 bp), lines 1–17: isolates tested, and T+: positive control.|
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This study revealed a high prevalence of enterobacteria with a dominance of K. pneumoniae in cooked and sold foods in private and public restaurants of the two universities. Haryani et al.  also found a high prevalence of K. pneumoniae in street foods. According to Mélanie , the high prevalence of K. pneumoniae was due to the lack of hygiene in the cooking of foods and to the contamination of raw products (hand preparation, use of poor water quality, and insufficient cleaning of fish and vegetable). Barro et al.  reported that, in collective food, the hygiene rules are most of the time neglected in accordance with the enormous quantity of foods daily cooked and the low level of education of restaurant staff. According to Tereza Gelbí?ová et al. , Klebsiella spp is not generally considered as a major foodborne pathogen but a hygiene indicator with regard to food production. Our study revealed the presence of K. pneumoniae in cooked food from private and public restaurants. According to the Public Health Agency of Canada  and Sri Harminda et al. , this may result from its thermotolerance. These authors found that complete inactivation of the bacteria may not always occur at 60°C.
A high prevalence of K. pneumoniae was observed in the samples of “attiéké” with vegetables (tomato, pepper, and onion) and fried fish in the public and private restaurants of the two universities. These results are in agreement with the results from the survey of Falomir et al.  on ready-to-eat food samples, which showed that K. pneumoniae was detected in mixed vegetables rice dishes (25%, 13 out of 52). Anoman  also reported the presence of pathogens into “garba” (a kind of “attiéké”) with raw fresh vegetables and fried tuna fish sold in Côte d’Ivoire. Belomaria et al.  also found that fresh vegetables are more involved in toxic food poisoning. Consumption of raw or slightly cooked vegetables can increase the risk of foodborne disease. According to some researchers [33,34], poor hygienic practices and improper handling and cooking are considered major factors for contamination of foods. The presence of K. pneumoniae in the cooked and sold foods by the university restaurants indicated potential fecal contamination, possible cross-contamination between food handlers, food preparation, surfaces, and the food itself . The attiéké meal is also served with fried tuna or horse mackerel fish. These types of fish can be contaminated with harmful enteric bacteria. According to Duflos , histamine-producing bacteria such as enterobacteria are commonly found in tuna fish. Insufficient cooking and improper handling and storage after cooking by the kitchen staff can contaminate the fish product. Also, K. pneumoniae may be spread from person to person or from person to item during food preparation and serving.
In our study, 13 strains of K. pneumoniae isolates harbored the blaSHV gene only. Perilli et al.  and Dayan et al.  also found that the blaSHV gene was the most dominant ESBL genotype in their studies carried out in Italy and Spain, respectively. However, ESBL blaCTX-M is the most prevalent gene found in a high proportion of samples from different parts of the world [38,39]. But in our study, blaCTM was not detected in the isolates. Finding K. pneumoniae isolates that carry antimicrobial resistance genes could potentially be an indirect public health hazard, regardless of their pathogenicity, because the available genetic pool of resistance is increased . Interestingly, 13 out of 24 strains of K. pneumoniae isolates positive for the blaSHV gene were resistant to beta-lactams (amoxicillin, amoxicillin + clavulanic acid, ticarcillin + clavulanic acid, ceftriaxone, and cefotaxime). These data corroborate the finding of Gadou  who reported that 96.7% of K. pneumoniae strains were resistant to ceftriaxone and 95.6% to cefotaxime. Mathlouthi et al.  also reported that 84% of K pneumoniae strains were resistant to ceftriaxone and 97% to cefotaxime. This study reports that K. pneumoniae from cooked food samples can be resistant to multiple antibiotics. The major reasons for K. pneumoniae resistance to antibiotics including beta-lactam antibiotics are the production of a broad-spectrum beta-lactamase (ESBL), the changing of the permeability barrier or the target site represented by penicillin-binding protein, or alteration of outer membrane protein . Additionally, K. pneumoniae have many efflux pumps that expel the antibiotic to the outside [44,45]. In this study, K. pneumoniae was also found to be highly resistant to quinolones at the rate of 92.2% and to aminosids at 61.5%. The resistance of K pneumoniae to aminosids and quinolones has also been reported by Gadou , at the respective resistance rates of 90% and 86.7%. Kouassi-M’bengué et al.  also found that the resistance rates were 85.7% for quinolones and 66.7% for aminosids. These results were in disagreement with those of Zhang et al.  who found that more than 90% of 61 K. pneumoniae isolates from retail foods in China were susceptible to quinolone antibiotics, including ciprofloxacin. The resistance of K. pneumoniae to most of the tested antibiotics mostly the beta-lactams may be the consequence of the abusive consumption of antibiotics in Côte d’Ivoire. Beta-lactams have always been the drugs of choice for the treatment of Klebsiella infections in healthcare institutions around the world, because aminoglycoside-modifying enzymes, macrolides esterases, and efflux systems render many other classes of drugs ineffective .
This study shows that K. pneumoniae recovered from cooked and sold foods by private and public restaurants of two universities of Côte d’Ivoire harbored the blaSHV gene and were resistant to beta-lactams. Food containing antimicrobial-resistant K. pneumoniae has the potential to become a public health risk to consumers. The study also shows the importance of good hygiene and handling practices during food preparation to reduce the risk of consumers being contaminated by antimicrobial-resistant K. pneumoniae. Authorities of universities should undertake sanitation control and prevention strategies in order for restaurants to improve the food quality and hygiene of the restaurant environment and staff. Restaurant staff should be trained in good hygiene practices.A study of the pathogenicity of different species of K. pneumoniae isolated from foods should be undertaken to better estimate the risk associated with their consumption.
The authors thank the directors of the various restaurants for their collaboration.
7. CONFLICTS OF INTEREST
No funding was availed for this study.
9. ETHICAL APPROVALS
This study does not involve experiments on animals or human subjects.
10. PUBLISHER’S NOTE
This journal remains neutral with regard to jurisdictional claims in published institutional affiliation.
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