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ISSN : 1229-1153(Print)
ISSN : 2465-9223(Online)
Journal of Food Hygiene and Safety Vol.35 No.2 pp.103-108

Correlation Between food Processing-Associated Stress Tolerance and Antimicrobial Resistance in Food Pathogens

Benjamin Kojo Woode1, Frank Daliri2, Eric Banan-Mwine Daliri3*
1Institute of Food Science, University of Debrecen, Hajdu Bihar County, Hungary
2Department of Agriculture Biotechnology, Kwame Nkrumah University of Science and Technology, Private Mail Bag, University Post Office, Kumasi, Ghana
3Department of Food Science and Biotechnology, Kangwon National University, Chuncheon, Korea
*Correspondence to: Eric Banan-Mwine Daliri, Department of Food science and Biotechnology, Kangwon National University, Chuncheon, Gangwon 24341, Korea Tel: +82-33-250-6457 Email:
February 7, 2020 February 19, 2020 February 19, 2020


Recently, consumer demand for safe but minimally processed food has rapidly increased. For this reason, many food processing industries are applying hurdle technology to enhance food safety, extend shelf life, and make foods appear minimally processed. Meanwhile, studies have shown that a treatment (stress) meant to inactivate foodborne pathogens may trigger adaptation mechanisms and could even offer cross protection against subsequent treatments. Also, certain routine farm practices such as antibiotic and herbicide use could result in the development of antibiotic-resistant pathogens. Such bacteria may be tolerant to food processing-associated stress and be more likely to remain viable in processed foods. In this review, we discuss the correlation between food processing-associated stress and antibiotic resistance. We also discuss molecular mechanisms such as the use of sigma factors, SOS response pathways and efflux pumps as means of cross protection against antimicrobial compounds and other food processing associated stresses.


    In recent years, the demand for fresh or minimally processed foods has increased since such foods preserve the quality and physicochemical properties of the food. For this reason, many food companies combine several processing methods (hurdle technology) so as to exert minimal effects on the overall quality of the food while improving the safety and extending the shelf life of the food product. However, some food processing methods occasionally render some pathogenic bacteria resistant to subsequent treatments and even antimicrobial compounds1). Also, routine agricultural practices such as herbicide2) and antibiotic use tend to have significant impact on the susceptibility or resistance of pathogenic bacteria to food processing methods. Throughout the history of modern medicine, the use of antibiotics has been one of the best chemotherapeutic strategies for controlling infectious diseases in humans and farm animals3). However, the continuous and indiscriminate use of antibiotics for disease treatment and agriculture has contributed to the development of antibioticresistant bacteria as well as increased bacterial resistance in the gut, excreta and the environment4). For this reason, antibiotic resistant bacterial infections are rapidly becoming a global health threat and a huge economic burden that require critical measures to combat them5). Zoonotic antibiotic-resistant bacteria can be transmitted from livestock (and their products) to humans through food or skin contact6). Many studies have suggested that antibiotic resistant gene transfer could occur in the gut between normal commensals and antibiotic-resistant bacteria when foods containing antibiotic-resistant bacteria are consumed (Fig. 1)7,8). Since food is usually processed by drying, boiling, heating, frying, freezing, marinating and several other methods, the bacteria in food encounter many physical and chemical stresses (e.g., acids, oxidants, etc)9). Although all these processes inactivate pathogens in and on food surfaces, the stresses associated with the processing methods occasionally trigger adaptation responses10). This happens as a result of genetic and physiological adjustments in the bacteria could eventually render the cells significantly resistant to other stresses. Moreover, such adaptive responses to food-associated stresses have been reported to have a tendency of conferring cross protection against antibiotics leading to the cells becoming antibiotic resistant11).

    In this review, we discuss the relationship between bacterial stress resistance during food processing and their relationship with antibiotic resistance. We also discuss the molecular mechanisms for the cross protection between food stress and antibiotic resistance.

    The interplay between food-associated stress and antibiotic resistance

    Bacteria in processed foods usually experience stress resulting from the processing methods and these stresses are intended to inactivate microbial cells.

    Osmosis and antibiotic resistance

    Salt is a common food preservative for inactivating bacteria, yeast and mold. The addition of salt to foods creates an osmotic gradient between the intracellular and extracellular environments of bacteria cells and this can result in cell death12). Although salting is a good method of ensuring microbiological safety, the presence of antibiotic resistant genes in certain bacteria reduce their susceptibility to cell death by high salt concentration. A study by Komora et al.13) reported that antibiotic resistant L. monocytogenes showed high osmotic stress tolerance than their antibiotic susceptible counterparts when they were treated with 37% NaCl for 7 days. Also, they observed that multidrug resistant (MDR) L. monocytogenes showed higher resistance to osmotic stress than strains that were resistant to only one antibiotic. Similarly, antibiotic resistant S. aureus display better resistance to osmotic stress relative to their susceptible9). On the other hand, there are reports that some bacteria develop antibiotic resistance after they become resistant to high salt concentrations. For instance, Al- Nabulsi et al.14) showed that L. monocytogenes displaced resistance to ampicillin, tetracycline, doxycycline and vancomycin after they adapted to high salt concentration. Another study also showed that high salt concentrations could provide cross adaptation for E. coli against chloramphenicol and tetracycline15). Several bacteria isolated from high salt containing foods16) and other materials17) have been reported to be resistant to antibiotics and this demonstrates a possible link between osmotic stress and antibiotic resistance.

    Heat tolerance and antibiotic resistance

    Thermal pasteurization is a common sterilization method used in food industry as it leads to cell damage. However since high temperatures affect food quality, mild heat (45- 60°C) is preferable in food industry18). Yet, when microbes are incompletely inactivated, bacteria heat response is triggered and this can affect the efficiency of other treatments. Several reports have shown the impact of thermal adaptation on antibiotic resistance. Ebinesh et al.19) showed that Acinetobacter baumannii developed resistance against norfloxacin, amikacin, tazobactam, piperacillin, imipenem and meropenem after the bacteria were exposed to 45°C. In an earlier study, Rodríguez-Verdugo et al.20) adapted E. coli strains for about 2000 generations at 42.2°C and demonstrated that the heat-adapted strains had become resistance to rifampicin. It however seems that antibiotic resistance does not enhance heat tolerance in bacteria as shown in many studies. For instance Mcmahon et al.21) have shown that the survival of MDR E. coli (resistant to ceftriaxone, amikacin and nalidixic acid), MDR Salmonella enterica serovar Typhimurium (resistant to ceftriaxone, amikacin and trimethoprim) and MDR Staphylococcus aureus (ceftriaxone, amikacin and trimethoprim) decreased significantly when stored under 45°C. Other studies found no difference in the D-values of wild type Listeria monocytogenes and streptomycin-resistant counterparts when they were exposed to 55°C22) and 58°C (for 60 min)13). Interestingly, some studies even propose that antimicrobial resistance tends to decrease thermal resistance. For example, Doherty et al.23) showed that wild type Yersinia enterocolitica exhibited better resistance to 50-60°C than their nalidixic acid resistant counterparts. Similarly, MDR Escherichia coli O157:H7 displayed a lower D value at 55°C compared to wild types24).

    Cold tolerance and antibiotic resistance

    Cooling and freezing exert low temperature stress on microorganisms during food processing and preservation. Freezing cause water in cell membranes to expand, crystalize and destroy the cell membrane and its contents leading to cell death. Meanwhile, bacteria may adapt to cold temperature treatments and this could eventually influence their sensitivity to antibacterial compounds25). Exposing Cronobacter sakazakii to 5°C for 24 hours drastically improved its resistance to norfloxacin, amikacin, tazobactam, piperacillin, imipenem and meropenem relative to their unstressed counterparts26). Similarly, cold treatment of L. monocytogenes at 10°C for 24 hours improved their resistance to enrofloxacin, streptomycin, penicillin, gentamycin, tetracycline, doxycycline, ciprofloxacin, vancomycin, and ampicillin14). The antibiotic resistance did not disappear after the cold stress was removed.

    Acid tolerance and antibiotic resistance

    Bacteria may encounter acidic conditions in foods containing organic acids or when the foods are treated with acids. Just as other stresses, bacteria gradually adapt to acidic conditions when they exposed to milder concentrations for some time and this may influence the cell’s response to other stress conditions. In a study to ascertain the effect of acid stress tolerance on antibiotic resistance, Al-Nabulsi et al.14) low pH adapted L. monocytogenes (lactic acid, pH 5.5-6.0, 30 minutes) displayed stronger resistance to antibiotics than their acid sensitive counterparts. Another study also reported the possibility of acid tolerance in Salmonella species to promote the resistance to ciprofloxacin, ceftriaxone and sulfamethoxazole-trimethoprim27). Similarly, acid stressed A. baumannii developed resistance against amikacin, norfloxacin, piperacillin-tazobactam, imipenem, and meropenem19). Acid adapted C. sakazakii also showed strong resistance against tetracycline, tilmicosin, florfenicol, amoxicillin, ampicillin, vancomycin and neomycin, ciprofloxacin, and enrofloxacin better than wild strains26). The correlation between antibiotic resistance and acid tolerance has been studied over the years28). In an earlier study, wild type L. monocytogenes were found to be more susceptible to low pH inactivation when compare to antibiotic resistant strains when they were subjected to 1% lactic acid for 60 min13). Similarly, there was an improvement in the acid tolerance of antibiotic resistant S. aureus relative to wild type strains after they were exposed to a pH of 1.5 for 40 minutes9). Other studies have suggested that pretreatment of some bacteria with antimicrobial compounds could even protect them from subsequent acid stress29). Results from studies about the link between antibiotic resistance and acid resistance have yielded contradictory results. For instance, Duffy et al.24) reported that antibiotic resistant E. coli O157:H7 were more easily inactivated in yogurt and low pH juices than wild type E. coli O157:H7 strains. Meanwhile, Al-Nabulsi et al.26) found no difference in acid tolerance between antibiotic resistant and wild type Salmonella strains when exposed to 2% acetic acid and 2% lactic acid. A similar observation was made by Hughes et al.30) when they treated wild and antibiotic resistant Salmonella species with 3% lactic acid and 100 ppm of acidified NaCl. It is very possible that the impact of antibiotic resistance on acid tolerance as well as the influence of acid tolerance on antibiotic resistance is strain or specie dependent28).

    Mechanisms for cross protection between antibiotic resistance and food-associated stress tolerance

    Cross protection of bacteria by food associated stresses could pose danger to consumers. During hurdle technology however, it would be desirable if initial treatments could improve pathogen susceptibility subsequent treatments. For this reason, several studies have been carried out to unveil the mechanisms underlying cross protection between antibiotic resistance and other stress tolerance. Some of the mechanisms include the use of sigma factors, SOS response, and efflux pumps.

    Sigma factors

    Sigma factors important regulators of stress in bacteria. They play critical roles during cold conditions, heat, acid, salt, oxidative stress and many others31). The sigma factors in Gram-positive are known as σS (RpoS) while those in Gram-negative bacteria are called σB (SigB)32).

    Sigma factors bind to RNA polymerase core enzymes and directed to DNA promoter sequences to initiate transcription33). Deletion of σB in S. aureus reduced their resistance to teicoplanin, methicillin, and vancomycin34) while the presence of sigma factor RpoH heat tolerance and antibiotic resistance in P. aeruginosa35). Heat shocking of P. aeruginosa at 42°C induced overexpression of RpoH which resulted in the overexpression of the asrA gene. asrA genes encode aminoglycoside-induced stress response ATPdependent protease and is responsible for the observed aminoglycoside resistance. It has been shown that pretreating E. coli with trimethoprim could deplete adenine nucleotides leading to a drop in intracellular pH. The drop in intracellular pH induces the production of sigma factorrpoS which also upregulate the production of acid resistant proteins such as GadB and GadC29). The rpoS-dependent regulation is critical for increasing intracellular pH and maintaining a constant intracellular pH during acid stress36). Since sigma factors are generally triggered into action during stress, the presence of these factors could protect the cell against subsequent stress conditions.

    SOS response

    The SOS pathway plays a critical role in detecting and repairing DNA damage by expression of genes required for the process37,38). LexA (a SOS transcriptional repressor) binds to operator sites of SOS regulated genes to initiate SOS response39). In the presence of DNA lesions, RecA (another SOS transcriptional protein) binds to singlestranded DNA causing auto-catalytic cleavage of LexA proteins leading to derepression of SOS genes for DNA repair40). The SOS pathway has been shown to be important in bacteria response to ultraviolet radiation, toxic biomolecules, and antibiotics41). It has been shown that exposure of S. aureus to UV induces DNA damage which evokes the SOS-mediated DNA repair mechanism38. The SOS-mediated antibiotic resistance has also been observed in many bacteria including staphylococci37), E. coli42) and Pseudomonas aeruginosa38). Since the SOS response is meant to detect and repair DNA damage, it is possible that triggering the SOS response could offer cross protection for the bacterium against subsequent stresses.

    Efflux pumps

    Efflux pumps are transport proteins critical for transporting toxic compounds out of the cell membrane. Examples of this proton pump families include Multidrug and Toxic-compound Extrusion family, the major facilitator superfamily, the Resistance Nodulation Division family, the ATP-binding cassette superfamily, and the Small Multidrug Resistance family43). These transport proteins are stimulated in the presence of stress to actively extrude antimicrobial compounds from microbial cells to resist their lethal effects. For instance, it has been shown that pretreatment of Salmonella Enteritidis with chlorine, sodium nitrite, acetic acid or sodium benzoate can induce the overexpression of marRAB operon which plays a key role in the production of AcrAB efflux pumps44). In another study where E. coli was exposed to high salt concentration, the cells overexpressed AcrAB-TolC multidrug efflux pumps15) and this shows how the response to one stress could offer protection against subsequent stresses. Inhibition of efflux pumps has been studied as means of bacteria inactivation. Komora et al.13) showed that inhibiting efflux pumps with thioriodazine and reserpine in antibiotic resistant L. monocytogenes could significantly increase their susceptibility to hydrogen peroxide and benzalkonium chloride. Several studies have shown that deletion of mdrL from L. monocytogenes could render the cells more susceptible to benzalkonium chloride1) macrolides and cefotaxime9).

    Conclusion and perspectives

    The steps involved in food processing are key means of antibiotic resistant bacteria dissemination. We have shown that the different stresses applied during food processing are potential drivers of antibiotic resistance as well as cross protection promoters. It is therefore important to consider the possibility of cross protection when designing strategies for hurdle technology or other food processing methods. Although the impact of different food-associated stresses on microbes is strain dependent, extensive studies concerning how stress could induce resistance as well as cross protection remains imperative. More so, the possibility of bacteria stresses adaptation and cross protection against subsequent inactivation strategies calls for the development of antimicrobial compounds with multiple mechanisms.

    국문 요약

    최근 최소한으로 가공된 안전한 식품에 대한 소비자의 수요가 기하급수적으로 증가하고 있다. 이러한 이유로 많 은 식품가공 업체에서는 식품안전을 강화하고 유통기한 을 연장하기 위한 최소한의 가공공정 중 허들기술(hurdle technology)을 적용하고 있다. 한편, 연구에 따르면 식품 에 함유된 병원균을 비활성화하기 위한 공정 및 방법들 은 식중독세균들의 스트레스 적응 메커니즘을 촉발시켜 심지어 후속 치료로 부터 교차 보호를 준다. 또한, 항생 제와 제초제 사용과 같은 일상적인 농장 관행은 항생제 내성을 가진 병원균의 생성을 초래할 수 있다.

    이러한 항생제 내성 박테리아는 식품 처리과정과 관련 된 스트레스에 내성을 가질 수 있고 가공 식품에서 생존 할 수 있는 가능성을 높일 수 있다. 이 리뷰에서는 식품 가공과 관련된 스트레스와 항생제 내성의 상관관계에 대 해 논의한다. 또한, 항균성 화합물 및 기타 식품 처리 관 련 스트레스에 대한 교차 보호 수단으로서 시그마 인자 (sigma factors), SOS 반응 경로(SOS response pathways) 및 유출 펌프(efflux pumps)의 사용과 같은 분자유전학적 기작에 대해서도 논의한다.



    Examples of how bacteria become antibiotic resistant and how resistant genes are spread.



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