POSSIBLE TRANSMISSION OF DRUG-RESISTANT SALMONELLA TYPHIMURIUM AND LISTERIA MONOCYTOGENES WITHIN THE BEEF INDUSTRY IN ABUJA, NIGERIA

POSSIBLE TRANSMISSION OF DRUG-RESISTANT SALMONELLA TYPHIMURIUM AND LISTERIA MONOCYTOGENES WITHIN THE BEEF INDUSTRY IN ABUJA, NIGERIA

1. Oladosu ¹, M. I. Aboh ^*1, N. Amaeze ², E.C. Mmaju ², O. Anuforom ¹ and M. Emeje ³

National Institute for Pharmaceutical Research and Development ¹, Department of Microbiology and Biotechnology, University of Abuja, Faculty of Science ², Department of Biological Sciences ³, Centre for Nanomedicine and Biophysical Drug delivery, Abuja, Nigeria

ABSTRACT: Background: Widespread use of antibiotics in livestock production in large-scale across the globe has become of public and veterinary health importance because of its implication in antibiotic resistance. Adequate data in this area of research is not readily available in Nigeria; this study was undertaken in view of the possible link between antimicrobial resistance in farm animals and humans. Methods: We collected fifty samples of raw beef from different vendors and slaughter houses within Abuja and screened them for the presence of Listeria monocytogenes and Salmonella typhimurium using standard microbiological methods. The total bacterial and fungal counts, susceptibility of the isolates to different antibiotics and heat sensitivity at 55, 60 and 65ºC for 15 minutes were determined. Results: Our results show that ten isolates of Listeria monocytogenes and eighteen isolates of Salmonella typhimurium were isolated from the samples.  The total viable bacteria count range was 1x 10⁹ - 8x 10⁹cfu/g while the fungal count was 1x 10³ - 9x 10⁹cfu/g.  One (10 %) of the Listeria monocytogenes isolates was resistant to all antibiotics tested while all the Listeria monocytogenes isolates were resistant to cefuroxime. Eight (44.4%) of the Salmonella typhimurium isolates were resistant to at least three antibiotics. All the Listeria monocytogenes and Salmonella typhimurium isolates did not survive beyond 60 ^oC upon heat treatment. Conclusions: Our results indicate high prevalence of Salmonella typhimurium and Listeria monocytogenes in selected beef in Abuja. Beef therefore may represent a large reservoir for antimicrobial-resistant Salmonella typhimurium and Listeria monocytogenes

Infectious disease,

raw beef, antibiotic susceptibility, heat treatment

INTRODUCTION: Beef is the flesh of a slaughtered cow, steer or bovine animal ¹. Although, these animals may be sold to be slaughtered as young as one to two years, finest quality beef is gotten from animals between the ages of three to four years. The use of antimicrobial agents in livestock is fast growing ² and several reasons have been put forward to justify this including to avert and treat infections or to enhance growth ³.

Many of these antimicrobial agents are similar to the antimicrobials used in humans. In the production of livestock, separate animals may be treated; however it is usually more cost effective to treat whole groups by introducing drugs into their feed or water. For certain animals, like fish and poultry, bulk medication is the most practicable way of treatment ⁴. World-wide ingestion of antimicrobials in livestock production had been estimated at 63,151 (±1,560) tons in 2010 and is anticipated to increase by 67%, to 105,596 (±3,605) tons, by 2030 ².

The risk to human wellbeing following wrong antibiotic use in food animals is noteworthy and has become a subject of public health discuss among scientists, especially in the developing countries. Pathogenic-resistant organisms propagated in these livestock are poised to enter the food supply and could be widely disseminated in food products posing serious danger to public health.

Antimicrobial resistance has been partly attributed to the extensive use of antimicrobials in livestock. It is opined by some researchers that, such resistance largely occur through natural selection with its attendant consequences to public health ². The occurrence of drug resistance has been detected after the introduction of every new class of antimicrobial agents. This danger is compounded by a dawdling drug development channel and insufficient investment in the innovation and development of novel antimicrobial agents. Commensal bacteria found in livestock are frequently present in fresh meat products and may serve as reservoirs for resistant genes that could potentially be transferred to pathogenic organisms in humans ⁵.

Although previous studies have reported contamination of beef with Salmonella typhi and Listeria monocytogenes, in other parts of Nigeria and worldwide, there is no data on the presence of these pathogenic bacteria in raw beef sold in Abuja, North Central Nigeria. Salmonella is a foremost food borne pathogen, responsible for an estimated 98.3 million cases of gastroenteritis worldwide ⁶. This organism has frequently been associated with poultry ⁷. However, other sources of meat such as pork and lamb have also been implicated as sources of contamination ^{8, 9}. The pathogen Listeria has been recognized as the causative agent of Listeriosis. Annually, this organism is estimated to cause 2,500 illnesses and 500 associated deaths ¹⁰. Typical foodstuff implicated as sources of the organism include salad, cooked and fermented meat and raw meat such as beef, pork, lamb, poultry ^{11, 12, 9}. Usually a Listeria infection is linked to a well-defined high risk groups such as the immuno-compromised or pregnant women ¹³.

Timely recognition of emerging infections requires early warning systems to detect problems so that they may be promptly investigated and controlled before they evolve into public health crises. Adequate data in this area of research is not readily available in Nigeria; this study was undertaken in view of the possible link between antimicrobial resistance in farm animals and humans. This study was designed to investigate the presence of Salmonella typhimurium and Listeria monocytogenes on beef, its antibiotics susceptibility and thermal resistance during subsequent heat treatment.

 MATERIALS AND METHODS:

Antibiotics: All antibiotic discs were obtained from Oxoid, UK. Amoxicillin / clavulanic acid (20/10 µg), nalidixic acid (30 µg), tetracycline (30 µg), gentamycin (10 µg), streptomycin (10 µg), choramphenicol (30 µg), erythromycin (15 µg), cefuroxime (30 µg), nitrofurantoin (300 µg), and ciprofloxacin (5 µg).

 Media:

All media were obtained from Oxoid, UK. Xylose Lysine Deoxycholate agar (XLD), Tetrathionate broth,   Oxford agar,   Listeria selective broth, Nutrient agar,   buffered peptone water, Sabouraud dextrose agar, API test kits.

 Sampling procedure:

Fifty raw beef samples were procured at random from vendors in slaughter houses and meat stalls located in the Six Administrative Councils of the Federal Capital Territory, Abuja, Nigeria. The samples were transported to the laboratory in sterile bags. Analysis was carried out within 6 hours after sampling. However, where immediate microbiological evaluation was to be delayed, the samples were refrigerated at 4°C and analyzed within 24 hours of collection ¹⁴.

 Processing of samples:

Twenty-five grams each of the meat sample was weighed aseptically and immersed in 225 mL buffered peptone water. These meat samples were kept in the incubator 37 °C for 24 h.  One milliliter of ten-fold serially diluted sample was inoculated on nutrient agar for bacteria enumeration and incubated at 37 °C for 24 h and onto Sabouraud dextrose agar for fungal enumeration at 25 °C for 72 h. All bacterial and fungal counts were recorded as cfu/g.

 Isolation and identification of Salmonella typhimurium: The method by Erol et al. (2013) ¹⁵ was adopted with slight modifications; simply, 1 mL of pre-enriched culture was transferred into 9 mL of tetrathionate broth supplemented with freshly prepared iodine solution and incubator at 37°C for 24 h. Presumptive Salmonella spp colonies were streaked onto xylose lysine deoxycholate (XLD) agar and incubated at 37 ± 2 °C for 18-24 h.

Typical black colonies with yellow halo were picked and archived on nutrient agar slants until when needed. For identification, presumptive Salmonella typhimurium were streaked onto tryptone soy agar supplemented with 5 % sheep’s blood on soy agar and incubated at 37 °C for 24 h. Confirmatory tests included: Gram stain, triple sugar agar tests, urease tests and sugar tests via API 20E test kits. Isolates showing reactions typical of Salmonella were confirmed by agglutination tests.

 Isolation and identification of Listeria monocytogenes:

The method by Moustafa et al., (2011) ¹⁶ was adopted with slight modifications; one millilitre of the pre-enriched culture was added to 9 mL of listeria selective broth and further incubated for 24 h at 30 °C. The broth culture (after incubation) was streaked onto plates of Oxford agar and incubated at 37 °C for 48 h. Gray colonies surrounded with black centres were presumed to be Listeria monocytogenes. Presumptive Listeria colonies were picked and purified by streaking onto tryptone soy agar supplemented 5 % sheep’s blood. Non sporolating Gram positive cocobacilli were subjected to further identification tests: motility test, CAMP test, haemolysin production, fermentation of xylose, rhamnose, mannitol.

Susceptibility Testing:

Susceptibility test was performed according to Bauer-Kirby method of disc diffusion using Muller Hinton agar ¹⁷. Overnight culture of pure isolates grown on appropriate solid media was inoculated into sterile normal saline with turbidity matching 0.5 McFarland standard. The standardized culture was then streaked on the surface of Muller Hinton agar and the inoculated plates allowed to stand for 30 min, before standard antibiotic discs were placed equidistantly from each other using sterile forceps. The plates were inverted and incubated at 37^oC for 24 h. Isolates resistant to at least three different classes of antibiotics were termed multi-drug resistant (MDR) ¹⁸.

Thermal resistance testing:

Glass tubes containing the heating menstruum (9 mL tryptic soy broth) were placed in different water baths at 55, 60, 65 and 70 °C. When the heating menstruum reached the desired temperatures, one millilitre of standardized culture of multi drug resistant isolates were inoculated into the glass tubes containing the heating menstruum such that the initial counts were 1.0 x 10⁷ -1.0 x 10⁸cfu/mL.

The menstruum in the tubes was heated for 5, 10 and 15 minutes. Enumeration of organism surviving the heating was carried out on the appropriate media, after incubation at 37 °C for 48 h. The number of organisms surviving was plotted against the heating times to yield a curve of rate of inactivation at four different temperatures. Based on the curve, the D values, i.e. time (minutes) at certain temperatures to reduce the number of organism by 1 log cycle was calculated from the equation D = -1/slope.

A Thermal Death Time (TDT) curve was made to establish the relationship between D (minutes) with temperatures (^oC). The Z values, i.e. temperature intervals to reduce D value by 1 log cycle was also determined from the curve ¹⁹.

RESULTS:

Confirmation of microorganisms:

The results of the biochemical and confirmatory tests confirmed 10 isolates to be pure cultures of Listeria monocytogenes while 18 isolates were confirmed to be pure cultures of Salmonella typhimurium (Table 1). Isolates were designated as Q for Salmonella isolates and P for Listeria. Initial count for Salmonella ranged from 1.5 – 2.4 x 10¹⁰ with Q3 and Q9 showing the highest number of counts with 2.4 × 10¹⁰cfu/g while initial count for Listeria monocytogenes ranged from 1.4 – 2.2 x 10¹⁰cfu/g with P5 showing the highest number of counts of 2.2 × 10¹⁰cfu/g (Table 2).

TABLE 1: FREQUENCY AND PREVALENCE RATE OF THE ISOLATED PATHOGENS

TABLE 2: INITIAL TOTAL COUNTS OF SALMONELLA TYPHI AND LISTERIA MONOCYTOGENES IN BEEF SAMPLES COLLECTED.

Antibiotics susceptibility of isolated bacteria: Drug susceptibility assay revealed that isolate P₁ was resistant to all antibiotics tested. Cefuroxime was the least effective antibiotic tested, as it inhibited only the growth of isolate P4. Gentamicin inhibited the growth of isolates P1 and P3 (8/10) while chloramphenicol inhibited all except P4 and P10 (2/10). Isolate P­4 was susceptible to all the antibiotics tested, while the other isolates were resistant to one or more of the antibiotics used (Table 3). Drug susceptibility assay showed that streptomycin and gentamicin were the most effective in inhibiting the growth of all Salmonella isolates, followed by ciprofloxacin, nalidixic acid nitrofurantoin, tetracycline and chloramphenicol, while cefuroxime showed the least efficacy against the isolates.  Isolate Q14 showed the highest resistance to the antibiotics, while Isolates Q4 and Q5 were most susceptible to all antibiotics tested (Table 4).

TABLE 3: ANTIBIOTICS SUSCEPTIBILITY TEST FOR ISOLATED LISTERIA MONOCYTOGENES

Keys: Gen = gentamicin, Cxm = cefuroxime, Ery = erythromycin, Tet = tetracycline, Cip = ciprofloxacin, Cam = chloramphenicol, Amx = amoxicillin, - = no inhibition.

TABLE 4: ANTIBIOTICS SUSCEPTIBILITY TEST FOR ISOLATED SALMONELLA.

Keys: Str = streptomycin, Nal = nalidixic acid, Cip = ciprofloxacin, Tet = tetracycline, Cam= chloramphenicol, Gen = gentamicin, Nit = nitrofurantoin, - = no inhibition.

Heat treatment of Listeria monocytogenes and Salmonella typhi isolates: Tables 5 and 6 show the colony count of surviving cells of Listeria monocytogenes and Salmonella typhi after being subjected to varying degrees of heat at 5, 10 and 5 minutes respectively.  Generally, cell death increased with increase in temperature. All isolates of listeria except P7 were killed upon exposure to heat at 60 ^oC for 5 minutes. For Salmonella, isolates Q3 and Q10 were the most resistant to heat, and were observed to survive at 60 ^oC for 15 minutes.

TABLE 5: EFFECT OF HEAT TREATMENT ON LISTERIA MONOCYTOGENES ISOLATE

 TABLE 6: EFFECT OF HEAT TREATMENT ON SALMONELLA TYPHI ISOLATES

Decimal reduction time (D-value) of isolates: The D values of Listeria monocytogenes and Salmonella typhi for five minutes at 55 and 60 ^oC are shown in tables 7 and 8. There was a decrease in the values as temperature increased.  Isolate P8 of Listeria was the only colony that retained its viability at 55 ^oC with a D value of 32.67 S, while Salmonella typhi isolates Q3 and Q10 were viable at 55 ^oC with D values of 32.01 and 33.18 seconds respectively.

TABLE 7: DECIMAL REDUCTION VALUE FOR LISTERIA MONOCYTOGENES

TABLE 8: DECIMAL REDUCTION VALUE FOR SALMONELLA TYPHI

DISCUSSION: Food borne disease caused by Listeria monocytogenes and Salmonella typhi represent a major public health problem especially in the developing countries where infectious diseases predominates due largely to poor or inadequate health facilities and hygiene. It has been established that these pathogens are transmitted through contaminated livestock products such as beef. Contamination of beef begins during slaughter of the animal due to poor hygienic conditions and handling processes of the slaughter houses or abattoir. The reliance on beef as a source of dietary proteins enhances the transfer of these disease causing pathogens to humans ²⁰. The consumption of contaminated meat and meat products is therefore a major vehicle in the transfer of pathogenic organisms to man.

In this study, it was evident from the bacteriological analysis of the investigated samples that Salmonella typhimurium and Listeria monocytogenes contaminate a large percentage of meat products. We discovered that 36 % (18/50) of all samples collected were positive for Salmonella and 20 % (10/50) were positive for Listeria monocytogenes. Compared to other studies, we report higher levels of Salmonella contaminants in meat samples. Lukasz et al. (2014) ²¹, showed that 10.4 % (11/106) of meat products were found to be positive for Salmonella. Ukut et al., (2010) ²² reported that 11 % meat samples from Calabar were contaminated with Salmonella, Adesiji et al., (2011) ²³ reported 2 % contamination in samples from Oshogbo.

Tafida et al., (2012) ²⁴ showed that Salmonella was isolated from 2.93 % of meat samples collected from Zaria. We also showed that Listeria was present in 35 % of interrogated samples. Listeria monocytogenes has also been found in different kinds of raw meat including beef, 20.8 % ²⁵ and 30 % of samples ²⁶. Previously, Daniel et al., (2015) ²⁷ reported a 17.15 % rate contamination for Listeria in fresh and frozen chicken from markets in Makurdi, Nigeria.  This larger contamination levels recorded for Abuja may be attributed to its strategic national status in Nigeria; being the administrative headquarter of Nigeria, the city plays host to the 3 arms of government, foreign diplomats as well as national and international investors. This cosmopolitan nature of the city encourages increase importation and consumption of varieties of meat and meat products in Abuja. According to the Centre for Disease and Control (CDC) ^28, with increasing resistance to fluoroquinolones and third-generation cephalosporin, Salmonella is now responsible for about 94 million cases of gastroenteritis and 115,000 deaths globally. It has been postulated that although Listeria is not as common as other food borne pathogens such as Salmonella and Escherichia coli, it is one of the deadliest and adaptable bacteria found in food²⁹. It is reported to cause up to 23,150 infections and 5,463 deaths worldwide.

The antibiotics susceptibility result for our study indicated resistance frequencies for Salmonella typhimurium and Listeria monocytogenes.  We observed that most Salmonella isolates were resistant to one or more of the antibiotics, while isolates Q4 and Q5 showed no resistance to the antibiotics tested. Streptomycin and gentamicin inhibited the growth of all 18 Salmonella isolates. Previous reports by Kakatka et al., (2011) ³⁰ have also found Salmonella typhimurium isolates from Indian foods to be sensitive to ampicillin and ciprofloxacin. Our data showed that all isolates of Listeria except P4 showed resistance to one or more of the tested antimicrobial drugs, this observation is consistent with previous studies such as those of Rahimi et al (2012) ³¹; Carmago et al (2015) ³² and Wieczorek et al (2012) ³³. These authors reported significant levels of antimicrobial resistant Listeria isolates from meat and hides circulating in Iran, Brazil and Poland respectively. Cefuroxime showed the lowest efficacy against Salmonella and Listeria isolates.

The low efficacy of cefuroxime against the isolates may be attributed to the easy hydrolysis of the β-lactam ring by most bacteria ³⁴.  On the other hand, gentamycin was most effective in inhibiting the growth of the isolates. Gentamycin, a bactericidal aminoglycoside acts by irreversibly binding to the 30S subunit of bacterial ribosome, interrupting protein synthesis in the bacteria leading to cell death³⁵.

Food borne pathogens can acquire resistance in response to antimicrobial drug use in food and animal contaminated food products at the time of slaughter and possibly transmit the resistant genes to human via the food chain ³⁶. According to Narfarnda et al., (2012) ³⁷ administration of antimicrobial drugs close to time of slaughter leads to the occurrence of antimicrobial residues in up to 89 % of animal tissue in beef samples from Abuja. The presence of pathogens resistant to a number of antibiotics as reported in this study can be linked to residual antibiotics in the animal tissues. The persistence of antimicrobial drug residues is a possible factor in driving antimicrobial resistance in bacteria isolated from livestock. A call by the US FDA for prudent use of antibiotics in both human and animal medicine has been issued for years with some positive results (FDA, 2000) ³⁸. In 2005 US Food and Drug administration (FDA) placed a ban on the use of enrofloxacin (a fluoroquinolone drug structurally related to ciprofloxacin) in poultry because of the risk that it promotes drug-resistant bacteria that are harmful to human health.

We discovered and report herein a high incidence of Salmonella and Listeria in beef being consumed in Abuja, the Federal Capital City of Nigeria.  It is recommended that meat products purchased from markets should be cooked thoroughly to kill bacteria and toxins before consumption as earlier suggested by Adeyanju and Ishola (2014) ³⁹. In order to establish scientific evidence and justify the suggestion to cook the products well before consumption, the isolates from our study were subjected to heat treatment to analyse the effect of heat on the viability of isolated bacteria. None of the isolates of Salmonella or Listeria survived beyond exposure to heat at 55^oC.

An average figure for the D values of Salmonella at D55 and D60 were 41.90 and 35.84 seconds respectively, while Listeria had corresponding average values of 41.52 and 30.63. Our observation is consistent with that of Murphy, et al., (2004) ⁴⁰. In their study, the D value for Salmonella at 55 and 70^oC were reported to be 43.33 and 43.76 s respectively, while the corresponding values for Listeria monocytogenes were 38.94 and 34.05 s. In a separate study on ready-to-eat turkey bologna by McCormwick et al., (2012) ⁴¹, that the D values for Salmonella typhimurium isolates  at 57 and 60 ^oC were reportedly 278 and 57 s respectively, while  D values for L. monocytogenes  at 61 and 65 ^oC were 124 and 16.2 s respectively. The differences between D values in this study and those previously reported may be due to different bacteria species, physiological conditions of the cells or use of cultures at different growth phases as previously argued by Juneja and Eblen (2002) ⁴².

 CONCLUSION: We confirm the role of raw beef as a reservoir of not just microorganism but also of microorganisms that are antibiotics resistant.  The results of this study show intermediate to high resistance to antimicrobial drugs in isolates of S. typhimurium and L. monocytogenes from beef marketed in Abuja. We suggest that this high resistance to antimicrobial drugs also correlated with increased survival when exposed to heat. The application of hygiene practices in meat processing centres and the prudent use of antibiotics in animal husbandry are therefore essential to control further emergence and transmission of antibiotic resistance.

 ACKNOWLEDGEMENT: The authors wish to thank the technologists in the Department of Microbiology and Biotechnology, National Institute for Pharmaceutical Research and Development, for their support during the course of this study.

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How to cite this article:

Oladosu P, Aboh MI, Amaeze N, Mmaju EC, Anuforom O and Emeje M: Possible Transmission of Drug-Resistant Salmonella Typhimurium and Listeria Monocytogenes within the Beef Industry in Abuja, Nigeria. Int J Pharm Sci Res 2016; 7(9): 3633-42.doi: 10.13040/IJPSR.0975-8232.7(9).3633-42.

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