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Two perspectives of Listeria monocytogenes hazards in dairy products: the prevalence and the antibiotic resistance

Two perspectives of Listeria monocytogenes hazards in dairy products: the prevalence and the... Listeria monocytogenes is among the most food-borne pathogens. It has the ability to grow over a range of temperature, including refrigeration temperature. Foods kept in refrigerator more than the prescribed period of time create an opportunity for the occurrence of Listeria monocytogenes. As this review shows, the prevalence of L. monocytogenes has more likely evident in pasteurized milk than other dairy products, such as raw milk. Inadequate temperature and faults in technology during pasteurization can be the disposing factors for the presence of the organism in dairy products. The organism, on the other hand, has been found to be resistant to those commonly known antibiotics that have human and veterinary importance, namely, ampicillin, Tetracycline, and chloramphenicol, streptomycin, erytromycin, penicillin G., and others. Resistance ability of the organism can be mediated by different natural and acquired resistance mechanisms, such as self-transferrable plasmids, mobilizable plasmids, and conjugative transposons. The emergence and spread of antibiotic resistance of L. monocytogenes has serious public health and economic impacts at large. This paper has reviewed the prevalence and the antibiotic resistance of L.  monocytogenes isolates of dairy products and the strategic mechanisms of the organism develop resistance against the antibiotics. Key words: Listeria monocytogenes; prevalence; antibiotic resistance; dairy products. risk to the consumers when they are contaminated by pathogens Introduction (Ndieyira et al., 2017). Food-borne diseases are mostly associated with microbial con- Listeriosis is one of the most serious and severe food-borne dis- tamination due to improper food handling during production, eases and it is caused by Listeria monocytogenes (WHO, 2003). processing, storage, and transportation (Martinović et  al., 2016). The organism contaminates food items at any production stages Mostly the diseases are evident in developing countries where pov- before consumption. Following consumption, the pathogen passes erty, illiteracy, poor hygienic conditions, and environmental sanita- the intestinal barrier and spreads to the blood and lymphatic system tion and lack of infrastructure can be the disposing factors for the to reach the liver and spleen, where it can multiply (Andersson outbreaks of the diseases. On the other hand, modern lifestyle has et al., 2015). Listeria monoctogenes is considered as an opportun- significantly changed food-eating habits globally, particularly in istic human pathogen causing meningitis or septicaemia, especially developed countries, with a consequent increased need for ready- infections among pregnant women, elderly, or individuals with to-eat foods and take away foods which are frequently consumed weakened immune system. Immuno-compromised individuals are (Lopez-Valladares et  al., 2018) and subsequently pose a potential © The Author 2019. Published by Oxford University Press on behalf of Zhejiang University Press. This Open Access article contains public sector information licensed under the Open Government Licence v2.0 (http://www.nationalarchives.gov.uk/doc/open- government-licence/version/2/). Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 234 B. H. Ulusoy and K. Chirkena, 2019, Vol. 3, No. 4 particularly vulnerable to this intracellular pathogen (Ramaswamy Therefore, the objective of this paper is to review on the prevalence et  al., 2007). It can seriously infect the foetus in the pregnant and antibiotic resistance of L.  monocytogenes isolates of dairy women as it vertically transmits from mother to foetus through products. placenta (Cossart, 2011). The report of WHO (2018b) shows that pregnant women are about 20 times more likely to get infection by Sources of Dairy Milk Contamination With listeriosis than healthy adults as the disease can result in miscar- L. monocytogenes riage or stillbirth and people with HIV/AIDS are at least 300 times more likely to get sick than those with normal immune system. Silage, inadequate hygiene, sanitation, and housing conditions are Some studies have revealed food products such as cheese, the source of L.  monocytogenes contamination in raw milk and raw milk, and other dairy products as the main sources of the dairy environment. Besides to this, bulk tank milk, milk filter, L.  monocytogenes and also consider as risk for food of humans milking machine, milk handler, faecal contamination, poor on-farm (Lungu et al., 2011; Seyoum et al., 2015). Additionally, food prod- hygiene during milking, storage, and transportation are also con- ucts stored in vacuum or in modified atmospheres and extended sidered as the source of contamination (Pantoja et  al., 2012). On refrigerator provide an opportunity for the bacterium to multiply the environment of dairy farm, once contamination occurs, it can to large numbers toward the end of the shelf life (Lopez-Valladares easily be disseminated to the animals and from animals to animals et al., 2018). The source of L. monocytogenes in raw milk is mainly (Hunt et  al., 2012). Food products are mostly contaminated by the gastrointestinal tract of animals and the environment. A study L.  monocytogenes at any stage of production and processing lines. conducted on the prevalence of L. monocytogenes isolates of milk The organism can enter the food chain from ‘farm to fork’ through samples and other dairy products indicated that the organism can carrier animals that shed the organism directly to foods, which most be found even in the balance tank of the pasteurizer and corres- likely increase the risk associated with contamination of raw milk ponding sample of pasteurized milk collected after pasteurization and other food items (Hunt et  al., 2012). Most animals may be (72.6°C for 15 s) under high-temperature short-time (Navratilova asymptomatic carriers shedding L. monocytogenes in dairy products et  al., 2004). Contamination of milk after pasteurization or due for months (Bangieva and Rusev, 2017). to defects in technology during pasteurization (inadequate tem- The most common route of infection to humans is through con- perature, technical errors) is responsible for the presence of sumption of contaminated milk and milk products. It is a fact that L.  monocytogenes in pasteurized milk. Therefore, the occurrence one of the hygienic requirements for foods of animal origin is the of L.  monocytogenes in dairy milk because of failure in the pas- absence of pathogenic microorganisms such as bacteria, protozoa, teurization process or post-pasteurization contamination is still a fungi, and viruses; however, at the time of the absence of hygienic concern (Lee et al., 2019). conditions, foods become easily exposed to those pathogens to cause Listeria monocytogenes is the major concern for the food infection to humans after consumption. Therefore, human listeriosis quality and safety in food industries, because it has the ability to is the disease associated with the consumption of foods of animals’ form biofilms which can resist the standard cleaning and disinfec- origin such as dairy products contaminated by L.  monocytogenes, tion procedures (Centorame et  al., 2017). Antibiotics have been particularly (Pitt et  al., 2000). Additionally, humans can acquire commercially available for long time for the treatment of infec- L. monocytogenes through foods kept in the refrigerators more than tious diseases, including those of food-borne infections. However, the prescribed time (greater than 5 days) (CFS, 2014), particularly the resistance of microorganisms against these antibiotics has been ready-to-eat foods with long shelf-life under refrigerator. also developing over this same period of time (Lungu et al., 2011), and thus, it has become worldwide. The emergence and develop- ment of antibiotic-resistant microorganisms, which of mostly food- The Prevalence of L. monocytogenes in Dairy borne pathogenic bacteria, such as Salmonella, Staphylococcus Products aureus, Escherichia coli, L. monocytogenes, and other pathogens in food products, like dairy products, has been the challenge for The occurrence of L. monocytogenes is worldwide and it is distrib- food-processing industries as these microorganisms can easily able uted widely in the environment. It has been considered as a poten- to contaminate food products, leading to reduce their shelf life tial contaminant of raw milk and other dairy products, including during storage of foods in extended time (Leong et al., 2014).The various types of foods. It is obvious that pasteurization of milk can resistance of such pathogens to antibiotics may be arisen from kill L. monocytogenes, but it is appeared in the milk after pasteur- misuse of antibiotics, for instance, in the treatment of diseases in ization contamination and may be due to inadequate temperature animals and humans and as growth promoter for animals, and this and technical errors. Some literatures indicate that cleanliness of the in turn poses some serious health problems to the public (Rahimi animals’ udder, milking equipment, milking man (handlers), health et al., 2012). of the animals, and sanitation of dairy unit and shed can be the The emergence of L. monocytogenes in food products like dairy determinant factors in the microbial contamination of unpasteur- products and others is due to the antibiotic resistance of the or- ized milk (Mary and Shrinithivihahshini, 2017). Additionally, since ganism. Olaimat et  al. (2018) reviewed on the emergence of anti- L. monocytogenes has the ability to multiply and grow at low and biotic resistance among L.  monocytogenes strains isolated from even freezing temperatures, foods kept in a refrigerator for a long food products and possible ways the resistance has developed. time are the factors for the presence of the pathogen (Kasalica et al., Due to this emergence of antibiotic resistance of the pathogen, fu- 2011). ture outbreaks and spread of the diseases may be hard to manage. Research-based evidence indicates that the prevalence of Extensive monitoring and assessment on the prevalence and anti- L.  monocytogenes has been evident in contaminated raw and pas- biotic resistance of this pathogenic microorganism in foods pro- teurized milk (Mansouri-Najand et  al., 2015). However, the in- cessed in different industries is more important to control and vestigation of Owusu-Kwarteng et  al. (2018) showed that the manage the dissemination of disease caused by L. monocytogenes. prevalence of L. monocytogenes obtained in raw cow milk from the Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 Prevalence and antibiotic resistance of L. monocytogenes, 2019, Vol. 3, No. 4 235 Table 1 ·The prevalence of L. monocytogenes isolates of dairy milk and milk products from different countries Dairy products Country Area Prevalence (%) References Raw milk Czech republic – 2.1 Navratilova et al., 2004 Ethiopia central high land 2.04 Seyoum et al., 2015 India Tiruchengode 16.6 Sreeja et al., 2016 Turkey Samsun 5 Kevenk and Terzi Gulel (2016) Ghana Northern Region 8.8 Owusu-Kwarteng et al., 2018 Iran Central 7.8 Akrami-Mohajeri et al., 2018 Ethiopia Addis Ababa 13 Gebretsadik et al., 2011 Central Iran Yazd 7.8 Akrami-Mohajeri et al., 2018 Iran Isfahan 4.39 Shamloo et al., 2015 Market milk India Kolkata 6.25 Saha et al., 2015 Pasteurized milk Czech republic – 5 Navratilova et al., 2004 Ethiopia Central high land 20 Seyoum et al., 2015 India Tiruchengode 25 Sreeja et al., 2016 Yoghurt Ethiopia Central high land 5 Seyoum et al., 2015 Cheese Ethiopia Central high land 26.7 Seyoum et al., 2015 Brazil Paraná 54.5 Abrahão et al., 2008 Traditional cheese Central Iran Yazd 7.5 Akrami-Mohajeri et al., 2018 White cheese Turkey Samsun 5 Kevenk and Terzi Gulel (2016) Farm pooled milk India Kolkata 5 Saha et al., 2015 Traditional butter Central Iran Yazd 1 Akrami-Mohajeri et al., 2018 Traditional curd Central Iran Yazd 1 Akrami-Mohajeri et al., 2018 Dairy product Turkey Ankara 10 Şanlıbaba et al., 2018 Traditional ice cream Central Iran Yazd – Akrami-Mohajeri et al., 2018 Farm cheese Turkey Samsun 20 Kevenk and Terzi Gulel (2016) Northern region of Ghana was 8.8%, whereas no L. monocytogenes challenge with an emergence of antibiotic-resistant bacterial strains, was detected in boiled cow milk. On the other hand, Navratilova including pathogens of public health importance such as Salmonella, et al. (2004) and Sreeja et al. (2016) reported higher prevalence of Staphylococcus aureus, Escherichia coli, and L.  monocytogenes as L. monocytogenes in pasteurized milk than raw milk as indicated in they potentially cause deterioration of foods. American food supply Table 1. The investigation of Seyoum et al. (2015) on different sam- is among the safest in the world, but people can still get sick from ples of dairy milk collected from the central high land of Ethiopia food-borne infections due to antibiotic-resistant bacteria (Centre showed that the prevalence of L.  monocytogenes varies based on for Disease Control and Prevention [CDC], NCEZID, 2018).Thus, the geographical location (urban areas, 3.4% and peri-urban areas, in USA alone, each year at least 2 million people are infected with 1.03%) and the type of samples taken (raw milk, pasteurized milk, antibiotic-resistant bacteria and at least 23,000 people die (Li and yoghurt, and cheese). However, similar to Navratilova et al. (2004) Webster, 2018). On similar cases, CDC reported 25,000 annual and Sreeja et  al. (2016), this study also obtained higher preva- deaths in the European Union (Sandoiu, 2018) in relation to the lence of L. monocytogenes and pasteurized milk and even in cheese effect of antibiotic resistance. It has been the major threats to food when compared with raw milk and yoghurt (Table 1). The other security and food development that antibiotic resistance makes the research work carried out in a total of 415 samples of milk and diseases harder to treat as the antibiotics become ineffective, which milk products from Tiruchirappalli city, Tamil Nadu, India con- may increase the mortality rate, the recovery time in hospitals (pro- firmed that 219 (52.7%) samples were found L.  monocytogenes longed hospital stay), as well as medical costs (WHO, 2018a). positive. Among these, raw milk and flavoured milk were 100% Some studies have shown that an extensive use of antibiotics contaminated by L.  monocytogenes followed by branded milk in livestock and poultry feed leads to the formation of antibiotic- (65.9%), cheese (62.5%), ice-cream (49.2%), milk powder (26.6%), resistant bacterial strains, which if they are transmitted to humans milk sweets (20%), ghee and paneer (13.3%), and yoghurt (6.6%), through animal products, might cause health problems to consumers whereas curd and butter were free from L.  monocytogenes (Mary (Akrami-Mohajeri et  al., 2018). Therefore, antibiotic resistance is and Shrinithivihahshini, 2017) also recognized as a challenge to dairy processing industries be- cause of the rapid emergence and spread of resistant bacteria and genes among humans, animals, and environment on a global scale Antibiotic Resistance of Bacteria Isolates of (Rousham et  al., 2018). Microorganisms, particularly bacteria, re- Food Products spond differently to antibiotics and other antimicrobial compounds, either due to intrinsic differences or to the development of resistance Antibiotic resistance is the ability of microorganism to combat the by adaptation or genetic exchange. action of one or more antibiotics that are used in clinical practice where the organism changes its response to the antibiotics as reviewed by Olaimat et al. (2018). It is a global public health issue, threatens Occurrence and Spread and of Antibiotic for the effectiveness of antibiotic therapy, and also challenges the Resistance efforts for developing new antibiotics. A variety of bacterial patho- gens isolated globally have now become multidrug resistance (Li and The use and misuse of antibiotics in farm animal settings as growth Nikaido, 2009). In recent years, the food industries have faced a promoters or as means of disease treatment has increased antibiotic Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 236 B. H. Ulusoy and K. Chirkena, 2019, Vol. 3, No. 4 resistance among bacteria in habitat. This reservoir of resistance of resistant bacteria develops in humans, animals, and environ- may be transferred directly or indirectly to humans through food ments (Badore, 2013). Poor hygiene and sanitation and poor in- consumption. The resistant bacteria can cause serious health ef- fection control are interconnected key factors contributing to the fects directly or through transmission of antibiotic-resistance traits spread of resistant bacteria in health care facilities and animal to pathogens, causing diseases that are difficult to treat (Economou production. and Gousia, 2015). However, in the review of Phillips et al. (2004), it was stated that although antibiotics are used in both animals and Antibiotic Resistance of L. monocytogenes in humans, most of the resistance problem in humans has arisen from Dairy Products human use. In natural environment, for example, fresh water, the overuse of antibiotics has enhanced the antibiotic resistance, making The challenge of the pathogenic L. monocytogenes, including other a potential risk for public health worldwide. In this regard, the food-borne microorganisms, is not limited to only contamination antibiotic resistance investigated by Yin et  al. (2013) in Lake Tailu of food items and environment, but also able to resist most com- obtained high percentage of resistance to streptomycin and ampi- monly known antibiotics that are often used for treatment of infec- cillin among bacterial isolates, followed by tetracycline and chlor- tions. Bacterial resistance to antibiotics has been rising dangerously amphenicol. Bacterial isolates selected for further study in this area to high level over the world, causing serious public health (WHO, also indicated that some opportunistic pathogens and 62% of the 2018a). The resistance of L. monocytogenes, isolates from different 78 isolates showed multiple antibiotic resistance. The prevalence dairy products, to some commonly used antibiotics such as peni- of antibiotic resistance and the dissemination of transferable anti- cillin, ampicillin, tetracycline, and gentamicin is evident (Yakubu biotic resistance in bacteria clearly show the urgency of realizing et  al., 2012; Olaimat et  al., 2018).The antibiotic resistance of the health risk to human and animals because it becomes a growing L.  monocytogenes, which was isolated from 164 samples of three global public threat with serious health, political, and economic im- types of dairy-based foods (Baladi cheese, Shankleesh, and Kishk) plications (Devarajan et al., 2016), and as in the review of Olaimat collected from the Bekaa valley from various sources such as mar- et  al. (2018), it is also the issue of food security and development kets, houses, and small family dairy farms in the Northeast regions because it makes the diseases harder to treat as antibiotics become of Lebanon, was investigated by Harakeh et al. (2009) who obtained ineffective. that more isolates were resistant to oxacillin (93.33%), penicillin The antibiotic-resistant bacteria are able to develop the stra- (90%), and ampicillin (60%) than to the rest of the antibiotics, tegic defensive mechanisms to take over the activity of the anti- indicating the emergence of multidrug-resistant L.  monocytogenes biotics, which may be through transfer of antibiotic-resistant in the environment. Similarly, the same pathogen isolated from other genes to each other or one another by horizontal gene transfer foods, such as ready-to-eat foods, was found resistant to oxacillin (Figure 1, no. 4). The spread of antibiotic resistance can be car- (94.1%) and penicillin (100%), including other antibiotics such as ried out through several routes. Person-to-person direct or in- nalidixic acid, ampicillin, linezoid, and lindamycin (Şanlıbaba et al., direct contact, animals to humans or humans to animals, food, 2018). Thus, the resistance of such strains to antibiotic drugs would water, and trade are some of the possible routes in which spread pose a very serious public health problem. Figure 1. ·Ways of bacterial resistance development. Source: CDC, 2018. Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 Prevalence and antibiotic resistance of L. monocytogenes, 2019, Vol. 3, No. 4 237 In a study conducted by Girma and Abebe (2018) in bo- to a broad spectrum of sub lethal environmental stresses during vine raw milk from Debre-Birhan town, Ethiopia, of the total 36 food production and processing; this may include physical stressors L.  monocytogenes species subjected for antimicrobial suscepti- such as heat, high pressure, desiccation, and irradiation; chemical bility test, 11 (30.5%) were resistance to nalidixic acid, followed by stressors such as acids, salts, and oxidants; and biological stressors 9(25%), 8(22.2%), and 4(11.1%) to tetracycline, chloramphenicol, such as microbial antagonism. For pathogenic bacteria, including and streptomicin, respectively. Similarly, according to an investigation L.  monocytogenes, to be resistant to the effect of antibiotics, the done on the antibiotic resistance of L. monocytogenes in samples of following listed in (Table 2) have been found to be the main factors. raw milk and dairy products collected from Samsun, Turkey, among The bacterial response to stress includes changes in cell compos- the collected samples, about 15.3% of the isolates were resistant to ition and physiological state, which enable food-borne pathogens at least one drug and 36.5% were multidrug-resistant, whereas the to maintain their normal functions and survive in foods during most common resistance encountered was to tetracycline (34.6%), processing. followed by chloramphenicol (25%) and penicillin G (23%) (Kevenk and Terzi Gulel, 2016). It is evident that L.  monocytogenes strains Mechanisms and Strategy of Antibiotic Resistance from food products exhibit resistance to other several types of anti- of L. monocytogenes biotics, including those of which are frequently used to treat human Bacteria constantly find new defence strategies, which is also called listeriosis, namely, kanamycin, levofloxacin, amoxicillin, rifampicin, ‘resistance mechanisms’, against the effects of antibiotics (Figure 2). and ciprofloxacin (Şanlıbaba et al., 2018). Antibiotic resistance in L.  monocytogenes is chiefly caused by dif- ferent genetic mechanisms like self-transferrable plasmids, mobiliz- able plasmids, and conjugative transposons. However, efflux pumps Factors Influencing the Antibiotic Resistance have also been reported to be linked with antibiotic resistance in of L. monocytogenes L.  monocytogenes (Navratilova et  al., 2004). Transmission of re- sistance among bacterial species has been demonstrated. The trans- Antibiotics are used for different purposes like growth supplements, mission from L. monocytogenes to S. aureus, and from Escherichia disease control and prevention, protection of public health, animal coli to S. aureus and L. monocytogenes by Enterococci and strepto- production enhancement, and public health associated with anti- cocci, in particular, represent a reservoir of genes of resistance for biotic resistance (Hao et al., 2014). However, when they are misused L.  monocytogenes. The resistance mechanisms are developed by or extensively used in humans and animals, they greatly contribute using instructions provided by their DNA. Resistance genes are often to the development and spread of antibiotic resistance among food- found within plasmids, small pieces of DNA that carry genetic in- borne pathogens including L. monocytogenes. The use of antibiotics structions from one to another. Thus, the transferability of antibiotic in low-dose or incomplete courses is the main reason for the emer- resistance genes among bacteria enables further spread of antibiotic- gence and spread of antibiotic resistance. On the other hand, forma- resistant bacteria (Bertsch et al., 2014). tion of biofilm on foods, instrument, and utensils and lack of new antibiotics being developed can also trigger the ability of the or- ganism to resist the activity of antibiotics. One mechanism of resist- Antibiotic Resistance Mediated by ance of bacteria is biofilm formation, which is also a mechanism of Conjugation virulence (Cepas et al., 2019). Biofilm-based infections are extremely difficult to cure because it enhances the resistance of the bacterial Conjugation is the process of transfer of genetic materials between strains (Hall and Mah, 2017). bacterial cells by direct cell to cell or by bridge like connection be- Some food-borne pathogens are naturally resistant to certain tween two cells. It takes place when the genetic materials transfer antibiotics and this is related to their general physiology, whereas from the donor to the recipient cells like streptomycin-resistant other pathogens develop antibiotic resistance by mutation or other L.  monocytogenes LM35 (donor) and streptomycin-sensitive types of genetic alteration (Olaimat et al., 2018). In addition, during L.  monocytogenes LM65 and LM100 (recipient strains) (Purwati their adaptation to environmental stresses, pathogens can become et  al., 2001). The investigation of Pourshaban et  al., (2002) on more resistant to antibiotics. Listeria monocytogenes may expose transferrable tetracycline resistance in L.  monocytogenes isolates Table 2 Antibiotic resistance of L. monocytogenes (isolates of dairy milk and milk products) to some selected antibiotics in different coun- tries Antibiotics Countries Central Iran Nigeria Ethiopia India Turkey (Yazd) (Sokoto) (Debre Birhan) (Kolkata) (Samsun) Tetracycline 86.3% 0% 25% 0% 34.6% Chloramphenicol 77.2% 0% 22.2% 40% 25% Ampicillin – 100% – 0% 9.6% Penicillin G 77.2% – – 0% 23% Gentamicin 18.1% 10% – 0% – Erythromycin 36.3% – – – 9.6% Streptomycin 45.5% 20% 11.1% – – Ciprofloxacin – 0% – 100% – References Akrami-Mohajeri et al., 2018 Yakubu et al., 2012 Girma and Abebe, 2018 Saha et al., 2015 Kevenk and Terzi Gulel (2016) Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 238 B. H. Ulusoy and K. Chirkena, 2019, Vol. 3, No. 4 Antibiotic Resistance Environmental Extensive Horizontal genec Biofilm Customers transfer formaon stress anbioc use Foods Disease Food Use of sub instruments treatment & Physical stress; microflora; inhibitory and utensils; prevenon; contaminang chemical concentra Growth preservaves; bacteria; Plant Persisted on of promoters; & animal disinfectants bacteria cells anbioc Pescides on Pathogen fruits Figure 2. ·Factors influencing antibiotic resistance of Listeria monocytogenes. Source: Malekmohammadi et al., 2017; Olaimat et al., 2018. of foods indicated that L.  monocytogenes stains 266 and 286 and investigate potential mechanisms underlying resistance and sensitive L.  innocua 52P transferred tetracycline resistance to L.  ivanovii to benzalkonium chloride in L. monocytogenes. In this study, reser- through conjugation, whereas only L.  monocytogenes and pine, an efflux pump inhibitor, was added to the strains to investi- L. innocua 52P transferred resistance to Enterococcus faecalis. The gate the role of efflux pumps in sensitivity/adaptation or resistance, genome of bacteria is composed of the chromosome and accessory resulting in a decrease in minimum inhibition concentration for movable genetic elements such as transposons and plasmids. In this benzalkonium chloride, whereas no decrease was observed for re- process of transfer, the genetic materials can be transferred from sistant strains, indicating that efflux pumps played no role in innate one cell to another; for example, Streptococcus agalactiae, which resistance of certain strains of L. monocytogenes to this compound. its plasmid is resistant to antibiotics such as chloramphenicol and The pumps may be specific for one substrate or may transport a macrolides, and Enterococcus, which is resistant to erythromycin, range of structurally dissimilar compounds, including antibiotics of both can be transferred to Listeria monocytogenes. multiple classes; such pumps can be associated with multiple drug In gastrointestinal tract of animals and in food processing plants, resistance, as reviewed by Webber and Piddock (2003). Bacterial ef- L. monocytogenes can be exposed to conjugation with Entrococcus flux pumps have evolved as a protective mechanism in both Gram species and Staphylococcus species carrying plasmids coding for negative and Gram positive, and particularly Gram-negative bac- antibiotic resistance. On the other hand, the gut of some insects, teria to maintain cell homeostasis and communication by actively like cockroaches, thought as an effective in vivo model for the nat- pumping out solutes, metabolites, quorum sensing molecules, and ural transfer of antimicrobial resistance plasmids among bacteria, toxins, especially antimicrobial compounds. They can be specific playing a crucial role in conjugation-mediated genetic exchanges. to antibiotics. However, most of them are multidrug transporters Regarding this, a study evaluated a conjugation-mediated horizontal that are capable of pumping a wide range of unrelated antibiotics transfer of resistance genes between Escherichia coli and other or- like macrolides and tetracycline and thus significantly contribute to ganisms of the same family within the intestine of Blaberus craniifer multidrug-resistant organisms and Sun et al. (2014) also reviewed on Burmeister revealed that the insects allow for the exchange of anti- the mechanism, physiology, and pharmacological exploitation of ef- microbial resistance plasmids among bacteria and may signify a po- flux pump inhibitors as promising antidrug resistance interventions. tential reservoir for the dissemination of antibiotic-resistant bacteria in different environments (Anacarso et al., 2016). Modification or Change of the Target Molecule Natural variations or acquired changes in the target sites of anti- Antibiotic Resistance Mediated by biotics that prevent drug binding are a common mechanism of re- Efflux Pumps sistance. Target site changes often result from spontaneous mutation Efflux pumps are membrane proteins found in both Gram-positive of a bacterial gene on the chromosome. Bacterial resistance is al- and Gram-negative bacteria that are involved in detoxifying cells, ways caused by molecular changes at the bacterial surfaces, which including antibiotics, from within cells to the external environment alter the nature of specific drug-target interactions (Ndieyira et al., (Lungu et al., 2011). They export antibiotics from the cell and main- 2017). Since antibiotic interaction with target molecule is gener- tain their low-intracellular concentrations and also determine the in- ally quite specific, minor alteration of the target molecule can have trinsic and/or acquired resistance (Poole, 2005).They have also been an important effect on the antibiotic binding. When antibiotics are considered as one of the mechanisms responsible for the antimicro- designed to single out and destroy specific part of the bacterium, bial resistance in biofilm-forming microorganisms such as Listeria the resistant bacterium can change the look of their targets so that monocytogenes, Pseudomonas aeruginosa, Escherichia coli, and the antibiotics cannot recognize and destroy them, allowing the Candida albicans (Soto, 2013). bacteria to survive. Therefore, modifying the target on which anti- Two groups of L.  monocytogenes strains, strains naturally sen- biotics bind and act is another mechanism of developing bacterial sitive to benzalkonium chloride and strains naturally resistant to resistance against antibiotics (Kapoor et  al., 2017). For example, benzalkonium chloride, were studied by Romanova et al. (2006) to when the structure of penicillin binding protein (PBP) in bacteria is Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 Prevalence and antibiotic resistance of L. monocytogenes, 2019, Vol. 3, No. 4 239 altered, penicillin can no longer bind to that protein and it becomes presence of the pathogen in dairy products has imposed a serious ineffective. public health globally. Foods kept in the refrigeration more than the prescribed time create an opportunity for the occurrence of Listeria monocytogenes. The prevalence of L.  monocytogenes isolates of Membrane Fluidity dairy products has been commonly challenging the dairy processing industry; since the organism has the ability to develop biofilm, the Membrane fluidity can play an important role in antimicrobial re- standard cleaning and disinfections, routinely applied, may not be sistance of L.  monocytogenes. The sensitivity of L.  monocytogenes fully effective in eliminating it. The pathogen has also the ability to to antimicrobial compounds was altered when bacterial membrane resist the activity of most commonly used antibiotics. The antibiotic lipid composition was modified by growth in the presence of added resistance of L. monocytogenes isolates of dairy products is another fatty acids. The cells of L. monocytogenes grown in the presence of concern of health issue because the antibiotic resistance of the micro- carbon chain (C14:0 or C18:0) of fatty acids have higher phase tran- organism has been developed against the activity of the antibiotics. sition and increased resistance to antibiotics than cells grown in the Based on the review, preventive measures, including good hygienic presence of carbon chain (C18:1) of fatty acyl (Juneja and Davidson, and sanitation practice in dairy products, good dairy management, 1993). Listeria monocytogenes has high levels of branched-chain and quality feed supply, are more practical for keeping food safety fatty acids. This leads to maintenance of constant membrane flu- and quality. idity at low temperatures by including fatty acids with lower Conflict of interest statement. The authors certify that there are no conflicts phase-transition temperatures (Kapoor et al., 2017). The fluidity of of interest with any organization, financial, or other regarding the material membrane lipid bilayer is altered mainly through the adjustment of discussed in the manuscript. membrane fatty acid composition. Listeria monocytogenes strains typically alter their membrane fluidity with changes in fatty acid chain length or by forming branched-chain fatty acids (Yoon et al., References 2015). Branched-chain fatty acids represent the dominant group of Abrahão, W. M., da Silva Abrahão, P. R., Monteiro, C. L. B., Pontarolo, R. membrane fatty acids and have been established as crucial deter- (2008). Ocorrência de Listeria monocytogenes em queijos e sorvetes minants in L.  monocytogenes resistance ability. This mechanism is produzidos no Estado do Paraná, Brasil. Revista Brasileira de Ciências mediated by membrane fluidity by modulating membrane fatty acid Farmacêuticas, 44(2): 289–296. composition. 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Two perspectives of Listeria monocytogenes hazards in dairy products: the prevalence and the antibiotic resistance

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Oxford University Press
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© The Author(s) 2019. Published by Oxford University Press on behalf of Zhejiang University Press.
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2399-1399
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2399-1402
DOI
10.1093/fqsafe/fyz035
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Abstract

Listeria monocytogenes is among the most food-borne pathogens. It has the ability to grow over a range of temperature, including refrigeration temperature. Foods kept in refrigerator more than the prescribed period of time create an opportunity for the occurrence of Listeria monocytogenes. As this review shows, the prevalence of L. monocytogenes has more likely evident in pasteurized milk than other dairy products, such as raw milk. Inadequate temperature and faults in technology during pasteurization can be the disposing factors for the presence of the organism in dairy products. The organism, on the other hand, has been found to be resistant to those commonly known antibiotics that have human and veterinary importance, namely, ampicillin, Tetracycline, and chloramphenicol, streptomycin, erytromycin, penicillin G., and others. Resistance ability of the organism can be mediated by different natural and acquired resistance mechanisms, such as self-transferrable plasmids, mobilizable plasmids, and conjugative transposons. The emergence and spread of antibiotic resistance of L. monocytogenes has serious public health and economic impacts at large. This paper has reviewed the prevalence and the antibiotic resistance of L.  monocytogenes isolates of dairy products and the strategic mechanisms of the organism develop resistance against the antibiotics. Key words: Listeria monocytogenes; prevalence; antibiotic resistance; dairy products. risk to the consumers when they are contaminated by pathogens Introduction (Ndieyira et al., 2017). Food-borne diseases are mostly associated with microbial con- Listeriosis is one of the most serious and severe food-borne dis- tamination due to improper food handling during production, eases and it is caused by Listeria monocytogenes (WHO, 2003). processing, storage, and transportation (Martinović et  al., 2016). The organism contaminates food items at any production stages Mostly the diseases are evident in developing countries where pov- before consumption. Following consumption, the pathogen passes erty, illiteracy, poor hygienic conditions, and environmental sanita- the intestinal barrier and spreads to the blood and lymphatic system tion and lack of infrastructure can be the disposing factors for the to reach the liver and spleen, where it can multiply (Andersson outbreaks of the diseases. On the other hand, modern lifestyle has et al., 2015). Listeria monoctogenes is considered as an opportun- significantly changed food-eating habits globally, particularly in istic human pathogen causing meningitis or septicaemia, especially developed countries, with a consequent increased need for ready- infections among pregnant women, elderly, or individuals with to-eat foods and take away foods which are frequently consumed weakened immune system. Immuno-compromised individuals are (Lopez-Valladares et  al., 2018) and subsequently pose a potential © The Author 2019. Published by Oxford University Press on behalf of Zhejiang University Press. This Open Access article contains public sector information licensed under the Open Government Licence v2.0 (http://www.nationalarchives.gov.uk/doc/open- government-licence/version/2/). Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 234 B. H. Ulusoy and K. Chirkena, 2019, Vol. 3, No. 4 particularly vulnerable to this intracellular pathogen (Ramaswamy Therefore, the objective of this paper is to review on the prevalence et  al., 2007). It can seriously infect the foetus in the pregnant and antibiotic resistance of L.  monocytogenes isolates of dairy women as it vertically transmits from mother to foetus through products. placenta (Cossart, 2011). The report of WHO (2018b) shows that pregnant women are about 20 times more likely to get infection by Sources of Dairy Milk Contamination With listeriosis than healthy adults as the disease can result in miscar- L. monocytogenes riage or stillbirth and people with HIV/AIDS are at least 300 times more likely to get sick than those with normal immune system. Silage, inadequate hygiene, sanitation, and housing conditions are Some studies have revealed food products such as cheese, the source of L.  monocytogenes contamination in raw milk and raw milk, and other dairy products as the main sources of the dairy environment. Besides to this, bulk tank milk, milk filter, L.  monocytogenes and also consider as risk for food of humans milking machine, milk handler, faecal contamination, poor on-farm (Lungu et al., 2011; Seyoum et al., 2015). Additionally, food prod- hygiene during milking, storage, and transportation are also con- ucts stored in vacuum or in modified atmospheres and extended sidered as the source of contamination (Pantoja et  al., 2012). On refrigerator provide an opportunity for the bacterium to multiply the environment of dairy farm, once contamination occurs, it can to large numbers toward the end of the shelf life (Lopez-Valladares easily be disseminated to the animals and from animals to animals et al., 2018). The source of L. monocytogenes in raw milk is mainly (Hunt et  al., 2012). Food products are mostly contaminated by the gastrointestinal tract of animals and the environment. A study L.  monocytogenes at any stage of production and processing lines. conducted on the prevalence of L. monocytogenes isolates of milk The organism can enter the food chain from ‘farm to fork’ through samples and other dairy products indicated that the organism can carrier animals that shed the organism directly to foods, which most be found even in the balance tank of the pasteurizer and corres- likely increase the risk associated with contamination of raw milk ponding sample of pasteurized milk collected after pasteurization and other food items (Hunt et  al., 2012). Most animals may be (72.6°C for 15 s) under high-temperature short-time (Navratilova asymptomatic carriers shedding L. monocytogenes in dairy products et  al., 2004). Contamination of milk after pasteurization or due for months (Bangieva and Rusev, 2017). to defects in technology during pasteurization (inadequate tem- The most common route of infection to humans is through con- perature, technical errors) is responsible for the presence of sumption of contaminated milk and milk products. It is a fact that L.  monocytogenes in pasteurized milk. Therefore, the occurrence one of the hygienic requirements for foods of animal origin is the of L.  monocytogenes in dairy milk because of failure in the pas- absence of pathogenic microorganisms such as bacteria, protozoa, teurization process or post-pasteurization contamination is still a fungi, and viruses; however, at the time of the absence of hygienic concern (Lee et al., 2019). conditions, foods become easily exposed to those pathogens to cause Listeria monocytogenes is the major concern for the food infection to humans after consumption. Therefore, human listeriosis quality and safety in food industries, because it has the ability to is the disease associated with the consumption of foods of animals’ form biofilms which can resist the standard cleaning and disinfec- origin such as dairy products contaminated by L.  monocytogenes, tion procedures (Centorame et  al., 2017). Antibiotics have been particularly (Pitt et  al., 2000). Additionally, humans can acquire commercially available for long time for the treatment of infec- L. monocytogenes through foods kept in the refrigerators more than tious diseases, including those of food-borne infections. However, the prescribed time (greater than 5 days) (CFS, 2014), particularly the resistance of microorganisms against these antibiotics has been ready-to-eat foods with long shelf-life under refrigerator. also developing over this same period of time (Lungu et al., 2011), and thus, it has become worldwide. The emergence and develop- ment of antibiotic-resistant microorganisms, which of mostly food- The Prevalence of L. monocytogenes in Dairy borne pathogenic bacteria, such as Salmonella, Staphylococcus Products aureus, Escherichia coli, L. monocytogenes, and other pathogens in food products, like dairy products, has been the challenge for The occurrence of L. monocytogenes is worldwide and it is distrib- food-processing industries as these microorganisms can easily able uted widely in the environment. It has been considered as a poten- to contaminate food products, leading to reduce their shelf life tial contaminant of raw milk and other dairy products, including during storage of foods in extended time (Leong et al., 2014).The various types of foods. It is obvious that pasteurization of milk can resistance of such pathogens to antibiotics may be arisen from kill L. monocytogenes, but it is appeared in the milk after pasteur- misuse of antibiotics, for instance, in the treatment of diseases in ization contamination and may be due to inadequate temperature animals and humans and as growth promoter for animals, and this and technical errors. Some literatures indicate that cleanliness of the in turn poses some serious health problems to the public (Rahimi animals’ udder, milking equipment, milking man (handlers), health et al., 2012). of the animals, and sanitation of dairy unit and shed can be the The emergence of L. monocytogenes in food products like dairy determinant factors in the microbial contamination of unpasteur- products and others is due to the antibiotic resistance of the or- ized milk (Mary and Shrinithivihahshini, 2017). Additionally, since ganism. Olaimat et  al. (2018) reviewed on the emergence of anti- L. monocytogenes has the ability to multiply and grow at low and biotic resistance among L.  monocytogenes strains isolated from even freezing temperatures, foods kept in a refrigerator for a long food products and possible ways the resistance has developed. time are the factors for the presence of the pathogen (Kasalica et al., Due to this emergence of antibiotic resistance of the pathogen, fu- 2011). ture outbreaks and spread of the diseases may be hard to manage. Research-based evidence indicates that the prevalence of Extensive monitoring and assessment on the prevalence and anti- L.  monocytogenes has been evident in contaminated raw and pas- biotic resistance of this pathogenic microorganism in foods pro- teurized milk (Mansouri-Najand et  al., 2015). However, the in- cessed in different industries is more important to control and vestigation of Owusu-Kwarteng et  al. (2018) showed that the manage the dissemination of disease caused by L. monocytogenes. prevalence of L. monocytogenes obtained in raw cow milk from the Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 Prevalence and antibiotic resistance of L. monocytogenes, 2019, Vol. 3, No. 4 235 Table 1 ·The prevalence of L. monocytogenes isolates of dairy milk and milk products from different countries Dairy products Country Area Prevalence (%) References Raw milk Czech republic – 2.1 Navratilova et al., 2004 Ethiopia central high land 2.04 Seyoum et al., 2015 India Tiruchengode 16.6 Sreeja et al., 2016 Turkey Samsun 5 Kevenk and Terzi Gulel (2016) Ghana Northern Region 8.8 Owusu-Kwarteng et al., 2018 Iran Central 7.8 Akrami-Mohajeri et al., 2018 Ethiopia Addis Ababa 13 Gebretsadik et al., 2011 Central Iran Yazd 7.8 Akrami-Mohajeri et al., 2018 Iran Isfahan 4.39 Shamloo et al., 2015 Market milk India Kolkata 6.25 Saha et al., 2015 Pasteurized milk Czech republic – 5 Navratilova et al., 2004 Ethiopia Central high land 20 Seyoum et al., 2015 India Tiruchengode 25 Sreeja et al., 2016 Yoghurt Ethiopia Central high land 5 Seyoum et al., 2015 Cheese Ethiopia Central high land 26.7 Seyoum et al., 2015 Brazil Paraná 54.5 Abrahão et al., 2008 Traditional cheese Central Iran Yazd 7.5 Akrami-Mohajeri et al., 2018 White cheese Turkey Samsun 5 Kevenk and Terzi Gulel (2016) Farm pooled milk India Kolkata 5 Saha et al., 2015 Traditional butter Central Iran Yazd 1 Akrami-Mohajeri et al., 2018 Traditional curd Central Iran Yazd 1 Akrami-Mohajeri et al., 2018 Dairy product Turkey Ankara 10 Şanlıbaba et al., 2018 Traditional ice cream Central Iran Yazd – Akrami-Mohajeri et al., 2018 Farm cheese Turkey Samsun 20 Kevenk and Terzi Gulel (2016) Northern region of Ghana was 8.8%, whereas no L. monocytogenes challenge with an emergence of antibiotic-resistant bacterial strains, was detected in boiled cow milk. On the other hand, Navratilova including pathogens of public health importance such as Salmonella, et al. (2004) and Sreeja et al. (2016) reported higher prevalence of Staphylococcus aureus, Escherichia coli, and L.  monocytogenes as L. monocytogenes in pasteurized milk than raw milk as indicated in they potentially cause deterioration of foods. American food supply Table 1. The investigation of Seyoum et al. (2015) on different sam- is among the safest in the world, but people can still get sick from ples of dairy milk collected from the central high land of Ethiopia food-borne infections due to antibiotic-resistant bacteria (Centre showed that the prevalence of L.  monocytogenes varies based on for Disease Control and Prevention [CDC], NCEZID, 2018).Thus, the geographical location (urban areas, 3.4% and peri-urban areas, in USA alone, each year at least 2 million people are infected with 1.03%) and the type of samples taken (raw milk, pasteurized milk, antibiotic-resistant bacteria and at least 23,000 people die (Li and yoghurt, and cheese). However, similar to Navratilova et al. (2004) Webster, 2018). On similar cases, CDC reported 25,000 annual and Sreeja et  al. (2016), this study also obtained higher preva- deaths in the European Union (Sandoiu, 2018) in relation to the lence of L. monocytogenes and pasteurized milk and even in cheese effect of antibiotic resistance. It has been the major threats to food when compared with raw milk and yoghurt (Table 1). The other security and food development that antibiotic resistance makes the research work carried out in a total of 415 samples of milk and diseases harder to treat as the antibiotics become ineffective, which milk products from Tiruchirappalli city, Tamil Nadu, India con- may increase the mortality rate, the recovery time in hospitals (pro- firmed that 219 (52.7%) samples were found L.  monocytogenes longed hospital stay), as well as medical costs (WHO, 2018a). positive. Among these, raw milk and flavoured milk were 100% Some studies have shown that an extensive use of antibiotics contaminated by L.  monocytogenes followed by branded milk in livestock and poultry feed leads to the formation of antibiotic- (65.9%), cheese (62.5%), ice-cream (49.2%), milk powder (26.6%), resistant bacterial strains, which if they are transmitted to humans milk sweets (20%), ghee and paneer (13.3%), and yoghurt (6.6%), through animal products, might cause health problems to consumers whereas curd and butter were free from L.  monocytogenes (Mary (Akrami-Mohajeri et  al., 2018). Therefore, antibiotic resistance is and Shrinithivihahshini, 2017) also recognized as a challenge to dairy processing industries be- cause of the rapid emergence and spread of resistant bacteria and genes among humans, animals, and environment on a global scale Antibiotic Resistance of Bacteria Isolates of (Rousham et  al., 2018). Microorganisms, particularly bacteria, re- Food Products spond differently to antibiotics and other antimicrobial compounds, either due to intrinsic differences or to the development of resistance Antibiotic resistance is the ability of microorganism to combat the by adaptation or genetic exchange. action of one or more antibiotics that are used in clinical practice where the organism changes its response to the antibiotics as reviewed by Olaimat et al. (2018). It is a global public health issue, threatens Occurrence and Spread and of Antibiotic for the effectiveness of antibiotic therapy, and also challenges the Resistance efforts for developing new antibiotics. A variety of bacterial patho- gens isolated globally have now become multidrug resistance (Li and The use and misuse of antibiotics in farm animal settings as growth Nikaido, 2009). In recent years, the food industries have faced a promoters or as means of disease treatment has increased antibiotic Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 236 B. H. Ulusoy and K. Chirkena, 2019, Vol. 3, No. 4 resistance among bacteria in habitat. This reservoir of resistance of resistant bacteria develops in humans, animals, and environ- may be transferred directly or indirectly to humans through food ments (Badore, 2013). Poor hygiene and sanitation and poor in- consumption. The resistant bacteria can cause serious health ef- fection control are interconnected key factors contributing to the fects directly or through transmission of antibiotic-resistance traits spread of resistant bacteria in health care facilities and animal to pathogens, causing diseases that are difficult to treat (Economou production. and Gousia, 2015). However, in the review of Phillips et al. (2004), it was stated that although antibiotics are used in both animals and Antibiotic Resistance of L. monocytogenes in humans, most of the resistance problem in humans has arisen from Dairy Products human use. In natural environment, for example, fresh water, the overuse of antibiotics has enhanced the antibiotic resistance, making The challenge of the pathogenic L. monocytogenes, including other a potential risk for public health worldwide. In this regard, the food-borne microorganisms, is not limited to only contamination antibiotic resistance investigated by Yin et  al. (2013) in Lake Tailu of food items and environment, but also able to resist most com- obtained high percentage of resistance to streptomycin and ampi- monly known antibiotics that are often used for treatment of infec- cillin among bacterial isolates, followed by tetracycline and chlor- tions. Bacterial resistance to antibiotics has been rising dangerously amphenicol. Bacterial isolates selected for further study in this area to high level over the world, causing serious public health (WHO, also indicated that some opportunistic pathogens and 62% of the 2018a). The resistance of L. monocytogenes, isolates from different 78 isolates showed multiple antibiotic resistance. The prevalence dairy products, to some commonly used antibiotics such as peni- of antibiotic resistance and the dissemination of transferable anti- cillin, ampicillin, tetracycline, and gentamicin is evident (Yakubu biotic resistance in bacteria clearly show the urgency of realizing et  al., 2012; Olaimat et  al., 2018).The antibiotic resistance of the health risk to human and animals because it becomes a growing L.  monocytogenes, which was isolated from 164 samples of three global public threat with serious health, political, and economic im- types of dairy-based foods (Baladi cheese, Shankleesh, and Kishk) plications (Devarajan et al., 2016), and as in the review of Olaimat collected from the Bekaa valley from various sources such as mar- et  al. (2018), it is also the issue of food security and development kets, houses, and small family dairy farms in the Northeast regions because it makes the diseases harder to treat as antibiotics become of Lebanon, was investigated by Harakeh et al. (2009) who obtained ineffective. that more isolates were resistant to oxacillin (93.33%), penicillin The antibiotic-resistant bacteria are able to develop the stra- (90%), and ampicillin (60%) than to the rest of the antibiotics, tegic defensive mechanisms to take over the activity of the anti- indicating the emergence of multidrug-resistant L.  monocytogenes biotics, which may be through transfer of antibiotic-resistant in the environment. Similarly, the same pathogen isolated from other genes to each other or one another by horizontal gene transfer foods, such as ready-to-eat foods, was found resistant to oxacillin (Figure 1, no. 4). The spread of antibiotic resistance can be car- (94.1%) and penicillin (100%), including other antibiotics such as ried out through several routes. Person-to-person direct or in- nalidixic acid, ampicillin, linezoid, and lindamycin (Şanlıbaba et al., direct contact, animals to humans or humans to animals, food, 2018). Thus, the resistance of such strains to antibiotic drugs would water, and trade are some of the possible routes in which spread pose a very serious public health problem. Figure 1. ·Ways of bacterial resistance development. Source: CDC, 2018. Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 Prevalence and antibiotic resistance of L. monocytogenes, 2019, Vol. 3, No. 4 237 In a study conducted by Girma and Abebe (2018) in bo- to a broad spectrum of sub lethal environmental stresses during vine raw milk from Debre-Birhan town, Ethiopia, of the total 36 food production and processing; this may include physical stressors L.  monocytogenes species subjected for antimicrobial suscepti- such as heat, high pressure, desiccation, and irradiation; chemical bility test, 11 (30.5%) were resistance to nalidixic acid, followed by stressors such as acids, salts, and oxidants; and biological stressors 9(25%), 8(22.2%), and 4(11.1%) to tetracycline, chloramphenicol, such as microbial antagonism. For pathogenic bacteria, including and streptomicin, respectively. Similarly, according to an investigation L.  monocytogenes, to be resistant to the effect of antibiotics, the done on the antibiotic resistance of L. monocytogenes in samples of following listed in (Table 2) have been found to be the main factors. raw milk and dairy products collected from Samsun, Turkey, among The bacterial response to stress includes changes in cell compos- the collected samples, about 15.3% of the isolates were resistant to ition and physiological state, which enable food-borne pathogens at least one drug and 36.5% were multidrug-resistant, whereas the to maintain their normal functions and survive in foods during most common resistance encountered was to tetracycline (34.6%), processing. followed by chloramphenicol (25%) and penicillin G (23%) (Kevenk and Terzi Gulel, 2016). It is evident that L.  monocytogenes strains Mechanisms and Strategy of Antibiotic Resistance from food products exhibit resistance to other several types of anti- of L. monocytogenes biotics, including those of which are frequently used to treat human Bacteria constantly find new defence strategies, which is also called listeriosis, namely, kanamycin, levofloxacin, amoxicillin, rifampicin, ‘resistance mechanisms’, against the effects of antibiotics (Figure 2). and ciprofloxacin (Şanlıbaba et al., 2018). Antibiotic resistance in L.  monocytogenes is chiefly caused by dif- ferent genetic mechanisms like self-transferrable plasmids, mobiliz- able plasmids, and conjugative transposons. However, efflux pumps Factors Influencing the Antibiotic Resistance have also been reported to be linked with antibiotic resistance in of L. monocytogenes L.  monocytogenes (Navratilova et  al., 2004). Transmission of re- sistance among bacterial species has been demonstrated. The trans- Antibiotics are used for different purposes like growth supplements, mission from L. monocytogenes to S. aureus, and from Escherichia disease control and prevention, protection of public health, animal coli to S. aureus and L. monocytogenes by Enterococci and strepto- production enhancement, and public health associated with anti- cocci, in particular, represent a reservoir of genes of resistance for biotic resistance (Hao et al., 2014). However, when they are misused L.  monocytogenes. The resistance mechanisms are developed by or extensively used in humans and animals, they greatly contribute using instructions provided by their DNA. Resistance genes are often to the development and spread of antibiotic resistance among food- found within plasmids, small pieces of DNA that carry genetic in- borne pathogens including L. monocytogenes. The use of antibiotics structions from one to another. Thus, the transferability of antibiotic in low-dose or incomplete courses is the main reason for the emer- resistance genes among bacteria enables further spread of antibiotic- gence and spread of antibiotic resistance. On the other hand, forma- resistant bacteria (Bertsch et al., 2014). tion of biofilm on foods, instrument, and utensils and lack of new antibiotics being developed can also trigger the ability of the or- ganism to resist the activity of antibiotics. One mechanism of resist- Antibiotic Resistance Mediated by ance of bacteria is biofilm formation, which is also a mechanism of Conjugation virulence (Cepas et al., 2019). Biofilm-based infections are extremely difficult to cure because it enhances the resistance of the bacterial Conjugation is the process of transfer of genetic materials between strains (Hall and Mah, 2017). bacterial cells by direct cell to cell or by bridge like connection be- Some food-borne pathogens are naturally resistant to certain tween two cells. It takes place when the genetic materials transfer antibiotics and this is related to their general physiology, whereas from the donor to the recipient cells like streptomycin-resistant other pathogens develop antibiotic resistance by mutation or other L.  monocytogenes LM35 (donor) and streptomycin-sensitive types of genetic alteration (Olaimat et al., 2018). In addition, during L.  monocytogenes LM65 and LM100 (recipient strains) (Purwati their adaptation to environmental stresses, pathogens can become et  al., 2001). The investigation of Pourshaban et  al., (2002) on more resistant to antibiotics. Listeria monocytogenes may expose transferrable tetracycline resistance in L.  monocytogenes isolates Table 2 Antibiotic resistance of L. monocytogenes (isolates of dairy milk and milk products) to some selected antibiotics in different coun- tries Antibiotics Countries Central Iran Nigeria Ethiopia India Turkey (Yazd) (Sokoto) (Debre Birhan) (Kolkata) (Samsun) Tetracycline 86.3% 0% 25% 0% 34.6% Chloramphenicol 77.2% 0% 22.2% 40% 25% Ampicillin – 100% – 0% 9.6% Penicillin G 77.2% – – 0% 23% Gentamicin 18.1% 10% – 0% – Erythromycin 36.3% – – – 9.6% Streptomycin 45.5% 20% 11.1% – – Ciprofloxacin – 0% – 100% – References Akrami-Mohajeri et al., 2018 Yakubu et al., 2012 Girma and Abebe, 2018 Saha et al., 2015 Kevenk and Terzi Gulel (2016) Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 238 B. H. Ulusoy and K. Chirkena, 2019, Vol. 3, No. 4 Antibiotic Resistance Environmental Extensive Horizontal genec Biofilm Customers transfer formaon stress anbioc use Foods Disease Food Use of sub instruments treatment & Physical stress; microflora; inhibitory and utensils; prevenon; contaminang chemical concentra Growth preservaves; bacteria; Plant Persisted on of promoters; & animal disinfectants bacteria cells anbioc Pescides on Pathogen fruits Figure 2. ·Factors influencing antibiotic resistance of Listeria monocytogenes. Source: Malekmohammadi et al., 2017; Olaimat et al., 2018. of foods indicated that L.  monocytogenes stains 266 and 286 and investigate potential mechanisms underlying resistance and sensitive L.  innocua 52P transferred tetracycline resistance to L.  ivanovii to benzalkonium chloride in L. monocytogenes. In this study, reser- through conjugation, whereas only L.  monocytogenes and pine, an efflux pump inhibitor, was added to the strains to investi- L. innocua 52P transferred resistance to Enterococcus faecalis. The gate the role of efflux pumps in sensitivity/adaptation or resistance, genome of bacteria is composed of the chromosome and accessory resulting in a decrease in minimum inhibition concentration for movable genetic elements such as transposons and plasmids. In this benzalkonium chloride, whereas no decrease was observed for re- process of transfer, the genetic materials can be transferred from sistant strains, indicating that efflux pumps played no role in innate one cell to another; for example, Streptococcus agalactiae, which resistance of certain strains of L. monocytogenes to this compound. its plasmid is resistant to antibiotics such as chloramphenicol and The pumps may be specific for one substrate or may transport a macrolides, and Enterococcus, which is resistant to erythromycin, range of structurally dissimilar compounds, including antibiotics of both can be transferred to Listeria monocytogenes. multiple classes; such pumps can be associated with multiple drug In gastrointestinal tract of animals and in food processing plants, resistance, as reviewed by Webber and Piddock (2003). Bacterial ef- L. monocytogenes can be exposed to conjugation with Entrococcus flux pumps have evolved as a protective mechanism in both Gram species and Staphylococcus species carrying plasmids coding for negative and Gram positive, and particularly Gram-negative bac- antibiotic resistance. On the other hand, the gut of some insects, teria to maintain cell homeostasis and communication by actively like cockroaches, thought as an effective in vivo model for the nat- pumping out solutes, metabolites, quorum sensing molecules, and ural transfer of antimicrobial resistance plasmids among bacteria, toxins, especially antimicrobial compounds. They can be specific playing a crucial role in conjugation-mediated genetic exchanges. to antibiotics. However, most of them are multidrug transporters Regarding this, a study evaluated a conjugation-mediated horizontal that are capable of pumping a wide range of unrelated antibiotics transfer of resistance genes between Escherichia coli and other or- like macrolides and tetracycline and thus significantly contribute to ganisms of the same family within the intestine of Blaberus craniifer multidrug-resistant organisms and Sun et al. (2014) also reviewed on Burmeister revealed that the insects allow for the exchange of anti- the mechanism, physiology, and pharmacological exploitation of ef- microbial resistance plasmids among bacteria and may signify a po- flux pump inhibitors as promising antidrug resistance interventions. tential reservoir for the dissemination of antibiotic-resistant bacteria in different environments (Anacarso et al., 2016). Modification or Change of the Target Molecule Natural variations or acquired changes in the target sites of anti- Antibiotic Resistance Mediated by biotics that prevent drug binding are a common mechanism of re- Efflux Pumps sistance. Target site changes often result from spontaneous mutation Efflux pumps are membrane proteins found in both Gram-positive of a bacterial gene on the chromosome. Bacterial resistance is al- and Gram-negative bacteria that are involved in detoxifying cells, ways caused by molecular changes at the bacterial surfaces, which including antibiotics, from within cells to the external environment alter the nature of specific drug-target interactions (Ndieyira et al., (Lungu et al., 2011). They export antibiotics from the cell and main- 2017). Since antibiotic interaction with target molecule is gener- tain their low-intracellular concentrations and also determine the in- ally quite specific, minor alteration of the target molecule can have trinsic and/or acquired resistance (Poole, 2005).They have also been an important effect on the antibiotic binding. When antibiotics are considered as one of the mechanisms responsible for the antimicro- designed to single out and destroy specific part of the bacterium, bial resistance in biofilm-forming microorganisms such as Listeria the resistant bacterium can change the look of their targets so that monocytogenes, Pseudomonas aeruginosa, Escherichia coli, and the antibiotics cannot recognize and destroy them, allowing the Candida albicans (Soto, 2013). bacteria to survive. Therefore, modifying the target on which anti- Two groups of L.  monocytogenes strains, strains naturally sen- biotics bind and act is another mechanism of developing bacterial sitive to benzalkonium chloride and strains naturally resistant to resistance against antibiotics (Kapoor et  al., 2017). For example, benzalkonium chloride, were studied by Romanova et al. (2006) to when the structure of penicillin binding protein (PBP) in bacteria is Downloaded from https://academic.oup.com/fqs/article-abstract/3/4/233/5613233 by guest on 19 February 2020 Prevalence and antibiotic resistance of L. monocytogenes, 2019, Vol. 3, No. 4 239 altered, penicillin can no longer bind to that protein and it becomes presence of the pathogen in dairy products has imposed a serious ineffective. public health globally. Foods kept in the refrigeration more than the prescribed time create an opportunity for the occurrence of Listeria monocytogenes. The prevalence of L.  monocytogenes isolates of Membrane Fluidity dairy products has been commonly challenging the dairy processing industry; since the organism has the ability to develop biofilm, the Membrane fluidity can play an important role in antimicrobial re- standard cleaning and disinfections, routinely applied, may not be sistance of L.  monocytogenes. The sensitivity of L.  monocytogenes fully effective in eliminating it. The pathogen has also the ability to to antimicrobial compounds was altered when bacterial membrane resist the activity of most commonly used antibiotics. The antibiotic lipid composition was modified by growth in the presence of added resistance of L. monocytogenes isolates of dairy products is another fatty acids. The cells of L. monocytogenes grown in the presence of concern of health issue because the antibiotic resistance of the micro- carbon chain (C14:0 or C18:0) of fatty acids have higher phase tran- organism has been developed against the activity of the antibiotics. sition and increased resistance to antibiotics than cells grown in the Based on the review, preventive measures, including good hygienic presence of carbon chain (C18:1) of fatty acyl (Juneja and Davidson, and sanitation practice in dairy products, good dairy management, 1993). Listeria monocytogenes has high levels of branched-chain and quality feed supply, are more practical for keeping food safety fatty acids. This leads to maintenance of constant membrane flu- and quality. idity at low temperatures by including fatty acids with lower Conflict of interest statement. The authors certify that there are no conflicts phase-transition temperatures (Kapoor et al., 2017). The fluidity of of interest with any organization, financial, or other regarding the material membrane lipid bilayer is altered mainly through the adjustment of discussed in the manuscript. membrane fatty acid composition. Listeria monocytogenes strains typically alter their membrane fluidity with changes in fatty acid chain length or by forming branched-chain fatty acids (Yoon et al., References 2015). Branched-chain fatty acids represent the dominant group of Abrahão, W. M., da Silva Abrahão, P. R., Monteiro, C. L. B., Pontarolo, R. membrane fatty acids and have been established as crucial deter- (2008). Ocorrência de Listeria monocytogenes em queijos e sorvetes minants in L.  monocytogenes resistance ability. This mechanism is produzidos no Estado do Paraná, Brasil. Revista Brasileira de Ciências mediated by membrane fluidity by modulating membrane fatty acid Farmacêuticas, 44(2): 289–296. composition. 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