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. 2018 Sep 28;6(3):118–125. doi: 10.14252/foodsafetyfscj.2018002

Prevalence of Antibiotics Resistant Listeria monocytogenes Strains in Nigerian 
Ready-to-eat Foods

Daniel O Ebakota 1,✉, Onilude A Abiodun 2, Obayagbona O Nosa 3
PMCID: PMC7004927  PMID: 32038898

Abstract

The Listerial flora and Listeria monocytogenes bio-load associated with 411 ready-to-eat (RTE) foods sold at several locations in southern Nigeria was evaluated using phenotypic procedures which included serial dilution and pour plate techniques. Selected L. monocytogenes strains phenotypically identified from the RTE foods were further identified using virulence gene markers and 16srRNA amplification procedures. All the 90 L. monocytogenes strains cultured from the RTE foods were subjected to antibiogram analysis using disc diffusion. Some of the antibiotics employed included; Ceftazidine, cefuroxime, gentamicin, ofloxacin, augumentin, tetracycline and erythromycin. L. monocytogenes L. ivanovii, L. grayi, L.welshimeri, L. seeligeri and L. innocua were detected in the RTE foods. Haemolysin (hlyA) gene, Internalin gene (inlA) and invasive gene (iap) were detected in all L. monocytogenes isolates. L. monocytogenes LMEW70 with accession number KY053295 was 93% similar to L. monocytogenes L1846. All the L. monocytogenes isolates were resistant to amoxicillin, cloxacillin, augumentin and ceftazidime.

Key words: : ready-to-eat; Listeria monocytogenes; antibiotic resistance; Southern Nigeria,

Introduction

The desire to consume healthy foods is a demanding request of consumers. On the average, a consumer tries to improve his/her daily diet based on medical reasons or personal preference. On the whole, consumers require foods that are low in calories, fat, and sodium, high in fiber, and safe to consume. The safety of ready-to-eat (RTE) products not only worries the general public, but is of great concern to the food industries. Processors use series of techniques including chlorine sprays, washing methods, organic acid sprays and steam treatment procedures to reduce the microbial load on products1). Still, these methods have not reduced the number of food recalls and food-borne outbreaks occurring as a result of microbial contamination of foods.

Listeria monocytogenes represents the Listeria species most commonly associated with disease in humans. As a facultative bacterium, L. monocytogenes can live in soil and decaying vegetation, but once it gets into a human host, it can cause severe disease. The majority (99%) of the infections caused by L. monocytogenes are food-borne being ingestion of contaminated food especially contaminated RTE products that do not undergo subsequent reheating2). L. monocytogenes also has the ability to colonize surfaces, forming biofilms that remain attached to equipment used in food production3). Listeria can grow at temperatures from 1°C to 45°C, low water activity, low pH4), as well as in refrigerated vacuum packed food products5).

L. monocytogenes is resistant to drying, freezing and heating. They can tolerate sodium chloride content of 20% and are resistant to multiple antibiotics, making them difficult to treat6). The virulence of Listeria monocytogenes is serotype - dependent with serotypes 1/2a, 1/2c, 1/2b and 4b being involved in 98% of documented human listeriosis cases7). Numerous reports have implicated different food types such as milk and milk products, meat and meat products, raw vegetables and sea foods as sources of food borne listeriosis. The changes in life style have resulted into more foods being eaten away from home which is evident by the increasing number of food vending outlets and food hawkers. The hygiene practices involved in these food vending outlets still remain an issue of concern since contamination of foods can occur during harvesting, processing, equipment usage, transportation and human handling8). L. monocytogenes has recently assumed lot of interest as a result of its association with several outbreaks of listeriosis across the world through implication of different variety of foods, both raw and processed. The presence and prevalence of these microorganisms in RTE consumed in Nigeria has not been well studied. This research was aimed at the isolation and identification of antibiotics resistant L. monocytogenes from different RTE food using phenotypic and genotypic methods.

Materials and Methods

Sample Collection

The study was conducted along terrestrial locations on the main federal highway connecting Lagos to Port Harcourt, Rivers State, Southern Nigeria. The sampling points covered Ore and parts of 3 out of 6 South South states of Nigeria (Edo, Delta and Bayelsa states) (Fig. 1). The choice of sampling point was based on the areas (both large and make shift restaurants) where travelers stop to eat and purchase foods for their loved ones at home. Furthermore, areas where hawkers hawk their food and snacks were also sampled.

Fig. 1.

Fig. 1

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Map showing locations of sample areas (red points). Ondo, Edo, Delta, and Bayelsa States are South South states of Nigeria.

Samples were purchased from 30 food outlets. The samples collected were salads (Cabbage, carrot, sweet corn and mayonnaise with lettuce as optional ingredient), meat pies (potatoes and minced meat with carrots as optional ingredients), fried snails and roasted edible worms. The sample size was 411 collected between February and September 2015. The samples comprised of 124 edible worm samples, 85 salads, 108 snails and 94 meat pies. All the RTE food samples were purchased fresh and then transported to the laboratory for immediate analysis.

Detection of Listeria species

Prior to the evaluation of the presence of Listeria spp. in the food samples, the samples were crushed in a clean laboratory mortar with pestle. One g of each sample was aseptically weighed and homogenized (vortex) with 9 mL of sterilized peptone water to produce a stock homogenate. The homogenate was incubated at 37°C using Surgifield medical incubator (SM 9082A) for 4 hours. Ten-fold serial dilutions were made aseptically from the homogenate after which 1mL of aliquot was pour-plated in duplicate Listeria selective agar plates (Oxford formulation). The inoculated Listeria selective agar (LSA) plates were incubated at 37°C for 24-48 hours. All Listeria species hydrolyze aesculin as evidenced by a blackening of the medium hence discrete Listeria colonies appeared gray with black holo zones surrounding it. Suspected Listeria sp was sub-cultured and then subjected to number of biochemical and morphological tests and Oxoid Biochemical Identification System (O.B.I.S.) mono colorimetric test.

Detection of Virulence Genes in 
L. monocytogenes isolates

The genomic DNA of all suspected L. monocytogenes isolates were subjected to PCR using primers targeting haemolysin (hlyA) gene, internalin gene (inlA) and invasive gene (iap). The reaction mixture contained inquaba PCR PreMix (Inquaba, South Africa), which is premixed ready-to-use solution containing Tag DNA polymerase, dNTP, and MgCl. The reaction mixture was prepared in 0.2 mL PCR tubes with 25 μL reaction volumes (12.5 μL PreMix, 8.5 μL nuclease free water, 0.5 μL forward primer, 0.5 μL reverse primer and 3.0 μL template DNA) and done under the following thermocycling conditions in a GeneAmp PCR system (Geneamp, Singapore) at 94°C for 4 minutes for initial denaturation then 31 cycles, each at 94°C for 45 seconds, at 54°C for 1 minute, and at 68°C for 1 minute and final extension at 68°C for 8 minutes after which PCR products were separated in 1.5% agarose gel which was stained with ethidium bromide. PCR products on gel were visualized under UV light9). The primers used for hlyA, inlA and iap were as follows:

F-CGGAGGTTCCGCAAAAGATG and R-CCTCCAGAGTGATCGATGTT (hlyA) 234bp;

F-AATCTAGCACCACTGTCGGG and R-TGTGACCTTCTTTTACGGGC (inlA) 733bp;

F-TTATACGCGACCGAAGCCAAC and R-CAAACTGCTAACACAGCTACTA (iap) 660bp.

Isolation of L. monocytogenes genomic DNA and 16sRNA Amplification

The genomic DNA of selected L. monocytogenes cultures were extracted with the aid of QIAamp DNA Mini Kit (250) cat no 51306 with qiagen DNA extraction protocol as described by Di Pinto et al10). Extracted DNA templates were subjected to PCR using set (Forward and Reverse) of primers which targeted the 16sRNA of L .monocytogenes. PCR was performed with 27F-AGAGTTTGATCMTGGGTCAG and 1492R-GGTTACCTTGTTACGACTT, the primers allowed amplification of the 16sRNA genes of the L. monocytogenes. Thermocycling conditions was rapid thermal ramp to 96°C, at 96°C for 1 minute for initial denaturation, then 25 cycles, each of rapid thermal ramp to 96°C, at 96°C for 10 seconds, rapid thermal ramp to 50°C, at 50°C for 5 seconds, and rapid thermal ramp to 60°C, at 60°C for 4minutes and finally rapid thermal ramp to 4°C until ready for purification. Rapid thermal ramp used was 1°C/second. The PCR product was purified according to procedure described by Di Pinto et al10). The product from the purification process was loaded on the 3130xl genetic analyzer (Applied Biosystems) to give the sequences. MEGA6 was used to view and analyze the obtained data.

Antibiogram Profiling

The antibiotic susceptibility of the isolates was determined by the disk diffusion method on Mueller-Hinton Agar (Oxoid Basingstoke, UK)11). The antibiotics utilized were; ceftazidine (30 µg CAZ), cefuroxime (30 µg CRX), gentamycin (10 µg GEN), cloxacillin (10 µg CXC), ofloxacin (5 µg OFL), augumentin (30 µg AUG), nitrofuranton (200 µg NIT), ciprofloxacin(10 µg CPX), ceftrizone (30 µg CRO), amoxicillin (25 µg AMX), streptomycin (10 µg STR), pefloxacin (5 µg PEF), tetracycline (30 µg TET), and erythromycin (5 µg ERY). Pure cultures of isolates of L. monocytogenes were streaked on Muller-Hinton Agar after which the impregnated disks were aseptically placed on the inoculated plates and incubated at 37°C for 24 hours. After incubation, the diameter (in mm) of the zone around each disk was measured and interpreted in accordance with the Clinical and Laboratory Standards Institute Standards guidelines (sensitive; >20 mm, intermediate; 15-19 mm and resistant ≤14 mm)

Results

The Percentage frequency of occurrence of identified cultured food borne Listeria species is presented in Fig. 2. L. monocytogenes had the highest frequency of occurrence (36.37%) while L. ivanovii had the lowest frequency of isolation (4.08%). L. grayi, L.welshimeri, L. seeligeri and L. innocua occurred 20.82%, 9.39%, 10.20% and 18.78% respectively.

Fig. 2.

Fig. 2

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Percentage frequency of occurrence of food associated Listeria species

The occurrence of L. monocytogenes isolated from different RTE foods from South South Nigeria is represented in Table 1. Of 115 Listeria sp isolated from edible worms only 55 representing 47.42% were identified as L. monocytogenes. For salads, snails and meat pies, there were 50, 45 and 35 isolated Listeria species respectively of which L. monocytogenes represented 30% of salads, 33.3% in snails, and 14.29% in meat pie. Highest positive sample of 47.82% L. monocytogenes was seen in edible worms and lowest percentage of 14.29% L. monocytogenes presence was seen in meat pies.

Table 1. Occurrence of L. monocytogenes isolated from different RTE foods.

Sample No. of Listeria sp. isolated No. positive for L. monocytogenes (%)
Edible worm 115 55 (47.82)
Salads 50 15 (30.00)
Snails 45 15 (33.30)
Meatpie 35 5 (14.29)
Total 245 90 (36.73)
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Haemolysin (hlyA) gene, internalin gene (inlA) (Fig. 3) and invasive gene (iap) were detected in all L. monocytogenes isolated.

Fig. 3.

Fig. 3

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Agarose gel separation of amplified internalin A (inlA) gene from L. monocytogenes isolated from RTE foods

KEY; Lane A and J: 100bp Ladder, Lane B: L. monocytogenes ATCC19155, Lane C: LMEW20, Lane D: LMEW24, Lane E: LMEW70, Lane F: LMEW94, Lane G: LMSN47, Lane H: LMSN108, Lane I: LMSA55

The molecular identity of selected L. monocytogenes isolated from RTE foods sampled in southern Nigeria was revealed in Table 2. L. monocytogenes LMEW70 with accession number KY053295 was 93% similar to L. monocytogenes L1846, L. monocytogenes LMSN47, LMSA55, LMMP96, LMEW24 was 90%, 90% 89% and 94% similar to L. monocytogenes L2625, LM850658, 19113, and CFSAN023463, respectively (Table 2).

Table 2. Molecular identification of L. monocytogenes isolated from RTE foods sampled from southern Nigeria.

Isolate code Accession No. Percentage Similarity (%) Relative Identity
LMEW20 KY053299 89        L. monocytogenes J0161
LMEW24 KY053300 94        L. monocytogenes CFSAN023463
LMEW70 KY053295 93        L. monocytogenes L1846
LMEW94 KY053296 90        L. monocytogenes La111
LMSN47 KY053298 90        L. monocytogenes L2625
LMSN108 KY053302 91        L. monocytogenes L2074
LMSA55 KY053294 90        L. monocytogenes LM850658
LMSA104 KY053301 92        L. monocytogenes JXH-150
LMMP96 KY053297 89        L. monocytogenes 19113
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The antibiotic resistance/susceptibility spectrum of the food borne L. monocytogenes isolates is shown in Table 3. All the L. monocytogenes isolates were resistant to amoxicillin, cloxacillin, augumentin and ceftazidime while 18.88%, 20%, 57.77%, 24.44% and 13.33% of the L. monocytogenes were sensitive to nitrofurantoin, gentamicin, ofloxacin, erythromycin, and cefuroxime respectively (Table 3). Also, 50%, 66.66%, 53.33 and 27.77% of the L. monocytogenes isolates had intermediate zones of susceptibility toward streptomycin, pefloxacin, erythromycin and cefuroxime.

Table 3. Antibiotic resistance/susceptibility spectrum of the food borne L. monocytogenes isolates.

Listeria monocytogenes spectrum
Group Antimicrobial agent Susceptible (%) Intermediate (%) Resistant (%)
Nitrofurantoins Nitrofurantoin 17 (18.88) 52 (55.55) 21 (23.33)
Aminoglycosides Gentamicin 18 (20.00) 60 (66.66) 12 (13.33)
Streptomycin 15 (16.66) 45 (50.00) 30 (33.33)
Fluoroquinolones Ofloxacin 52 (57.77) 38 (42.22) NIL
Ciprofloxacin 30 (33.33) 48 (53.33) 12 (13.33)
Pefloxacin 18 (20.00) 60 (66.66) 12 (13.33)
ẞ- lactams Amoxycillin NIL NIL 90(100)
Cloxacillin NIL NIL 90(100)
Augumentin NIL NIL 90(100)
Tetracycline Tetracycline 25 (27.77) 35 (38.88) 30 (33.33)
Macrolides Erythromycin 22 (24.44) 48 (53.33) 20 (22.22)
Cephems Cefuroxime 12 (13.33) 25 (27.77) 43 (47.77)
Ceftazidine NIL NIL 90(100)
Ceftriazone NIL 48 (53.33) 42 (46.66)
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Discussion

In this study, a total of 90 L. monocytogenes was isolated and characterized from salads, meat pies, fried snails and roasted edible worms purchased from different vendors located at different parts of southern Nigeria. This finding could represent a major threat to human safety as these foods are relatively cheap and are consumed by many people of varying age groups, gender and ethnic groups making them prone to listeriosis, an infection commonly associated with consumption of foods contaminated with L. monocytogenes. The presence of L. monocytogenes in this research could be attributed to poor sanitary conditions of the food vendors, the use of unclean utensils, unhygienic conditions of the production area and the nature and source of water supplied for washing. L. monocytogenes is likely introduced into food production facilities due to their inherent properties that allow them to survive and effectively compete with other microbes in food processing environments. They have the ability to grow at low pH, refrigeration temperatures, are resistant to freezing, high salt concentrations and can adapt to stresses that exist at times in food production facilities12). Moreover, the tropical weather is warm and humid all year round in Nigeria and this could favor the growth and proliferation of Listeria in foods since most foods are sold in the open especially RTE foods. Environmental studies of Listeria in Nigeria have shown that the organism is known to occur in soil, lakes, veterinary surgical material13), Naira currency notes14), a snack made by sun-drying beef15), kunu (a popular traditional drink made mainly from millet16)), wara (a type of soft cheese made from coagulating fresh cows’ milk17)), vegetables18), and frozen poultry19).

All L. monocytogenes isolates displayed resistance toward cloxacillin, augumentin, amoxicillin and ceftrizone but they exhibited varying degrees of susceptibility to gentamicin, tetracycline, ofloxacin, pefloxacin, streptomycin, ciprofloxacin, erythromycin, cotrimozazole, nitrofuratin and ceftazidine in this study. Adetunji and Adegoke stated that the resistance shown by L. monocytogenes strains to common drugs of choice in Nigeria may be due to the abuse of drugs in animal husbandry leading to mutation and appearance of new strains17). These results are consistent with reports of emergence of resistance in Listeria sp. and the need to emphasize further studies for the genotypic characterization of antibiotic resistance in Listeria to determine their resistance mechanisms and their potential as reservoirs of transferable resistance genes. Low resistance of L. monocytogenes to ciprofloxacin and gentamicin seen in this study has also been reported by other studies from Sokoto Nigeria and Iran9,20) where over 80.0% of isolates from various sources were found to be susceptible to each of these antimicrobial agents. There are, however, increasing reports of Listeria strains isolated from various sources being resistant to penicillin, ampicillin, tetracycline, streptomycin, clindamycin, oxacillin and vancomycin. A research has recorded high resistance to ampicillin (92.9%)21) and the other research also reported 100% resistance to ampicllin from L. monocytogenes obtained from isolates in milk and processed meat22). Although all strains of L. monocytogenes in this study were resistant to augumentin, Umoh et al reported all strains as augumentin susceptible which suggested that genetic differences may occur within the strains of L. monocytogenes23). Kayel et al and Troxler et al reported that newer generations of cephalosporins, like ceftriaxone, had no in vitro bactericidal effect on L. monocytogenes and attributed the resistance to the lack of specific penicillin-binding proteins 3 and 5 in the Listeria cytoplasmic membrane24,25). Moreover, resistance to tetracycline and ciprofloxacin has been reported in L. monocytogenes isolated from foods26,27). Godreuil et al suggested that the acquired resistance to ciprofloxacin may be due to the acquisition of the Listeria drug efflux (lde) gene that could pump the drug out of the cell before its concentration is high enough to be bactericidal7).

The multiple drug resistance exhibited by the respective L. monocytogenes obtained in this study is similar to an earlier report, which stated that 20.0% of the isolates from dairy products were resistant to more than two antimicrobial agents and none of the isolates was resistant to less than one antimicrobial agent 28). This observation is in tandem with the result obtained in this study wherein 100.0% of the isolates were observed to be resistant to more than two antimicrobial agents and 64.3% of the isolates were resistant to more than four antimicrobial agents. Lotfollahi et al. also reported multiple antibiotic resistances in some human isolates of L. monocytogenes from blood, urine, vaginal swab, rectal swab and placental bit28).

The inlA was detected in all L. monocytogenes strains in this study. The inlA, also known as internalin is essential for L. monocytogenes entry into the human intestinal epithelial cell line29). The inlA plays a fundamental role in the invasion of L. monocytogenes into many cells. There is evidence which confirms that LLO (listeriosin) is the primary virulence factor associated with L. monocytogenes infection, in particular escape from the primary phagosome24). LLO is responsible for escape from the primary phagosome formed by initial internalization event; also the double membrane secondary phagosome associated with cell to cell infection30). These findings commensurate with the published work detecting LLO in L. monocytogenes31,32).

The presence of antibiotic resistant L. monocytogenes in the sampled RTE foods was established. Further surveillance of the prevalence of L. monocytogenes in other RTE foods should be carried out to enable the recognition of contaminated foods. There is also the need for coordinated research between universities and relevant institutions or agencies as regards to L monocytogenes and a cooperative effort of public health agencies, physicians, veterinarians, scientists, the food industries, regulatory agencies, research institutes and consumers to prevent and possibly control this organism.

Acknowledgment

The authors are grateful to the International Institute of Tropical Agriculture (IITA) where the sequencing was done and to the central laboratory, Benson Idahosa University, where most of the research was carried out.

Abbreviations: RTE: ready-to-eat

Footnotes

Conflict of interest: The authors have no conflict of interest.

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