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A Review of Temperature, pH, and Other Factors that Influence the Survival of Salmonella in Mayonnaise and Other Raw Egg Products

School of the Environment, Health and the Environment, Flinders University, GPO BOX 2100, Adelaide 5001, Australia
Author to whom correspondence should be addressed.
Pathogens 2016, 5(4), 63;
Received: 11 August 2016 / Revised: 26 October 2016 / Accepted: 15 November 2016 / Published: 18 November 2016


Salmonellosis is one of the main causes of foodborne illnesses worldwide, with outbreaks predominately linked to contamination of eggs and raw egg products, such as mayonnaise. This review explores previous studies that have investigated Salmonella control mechanisms utilized in the production of raw egg mayonnaise and other food products. Apart from the use of pasteurized eggs, the main control mechanism identified is the pH of the raw egg products, which plays an important role in the consistency and stability while affecting the survival of Salmonella spp. However, currently there is no consensus regarding the critical pH limit for the control of Salmonella. The effectiveness of pH as a control mechanism is influenced by the type of acid used, with the effectiveness of lemon juice compared with vinegar highly debated. Additionally, Salmonella susceptibility to pH stresses may also be influenced by storage temperature (in some studies refrigeration temperatures protected Salmonella spp. from acidulants) and is further complicated by the development of Salmonella cross-tolerance-induced responses, pH homeostasis achieved by the cellular antiport and symport systems, and acid tolerance response (ATR). These mechanisms all provide Salmonella with an added advantage to ensure survival under various pH conditions. Other confounding factors include the fat content, and the addition of NaCl, garlic and plant essential oils (PEOs) from mint, cinnamon, cardamom and clove.

1. Introduction

Worldwide, foodborne illness is one of the most serious health problems affecting public health and development [1]. In the USA, it was estimated that the annual incidence of foodborne illness was 48 million cases and the economic burden estimate ranges from US $51.0–77.7 billion [2]. In Canada, annual estimates of foodborne illness range from 3.1–5.0 million cases [3] and in Australia the incidence is estimated at 5.4 million cases costing AUD$1.2 billion annually [4]. Worldwide, it is estimated that Salmonella is responsible for 80.3 million cases of food borne illness [5].
Salmonella spp. are members of the family Enterobacteriaceae [6] and are facultative anaerobic rods [7]. There are more than 2600 known serovars [8], and within a serovar the strains could be different in virulence [9]. The serovars of Salmonella are broadly classified into typhoidal and nontyphoidal Salmonella (NTS). Nontyphoidal Salmonella (NTS) serovars include Typhimurium and Enteritidis, which are pathogens with a wide-range of host specificity, but S. enterica serovars, Typhi, Sendai, and Paratyphi A, B, and C are highly adapted to the human as a host and are the causative agents of enteric fever [8]. While there are over 2600 identified serotypes of Salmonella, the majority of clinical Salmonella cases can be attributed to 20 serotypes [10], but there are instances where infection occurs due to uncommon serotypes of Salmonella [11].
One of the main sources of foodborne salmonellosis is eggs and raw egg products [12]. Outbreaks of Salmonella serotype Enteritidis have been repeatedly associated with the consumption of raw and undercooked eggs [13,14]. The eggs can be contaminated during different stages of their formation, processing, and packaging. Vertical or transovarian contamination of eggs can happen during the formation of the egg when the ovaries of the hen are infected. Horizontal transmission can take place if the eggs are contaminated by means of a contaminated environment [15]. According to previous studies, there is an increased probability of whole eggs with low shell quality being able to be penetrated by Salmonella spp. [16], and egg weight and flock age also influence the ability of Salmonella spp. to penetrate the shell and the membranes of the eggs [17]. Moreover, it is found that there is an increased incidence of eggshell penetration from the beginning to the end of lay by S. Enteritidis [18], and there is an increased risk of Salmonella contamination when the flock becomes older [19].
Even though several food items like peanuts, beef, pork, and chicken have been connected with the outbreaks of salmonellosis, eggs and food products prepared using eggs seem to be the most frequent foods that are involved with the disease [20]. Raw eggs are used in many food products like pastries, homemade ice cream, and mayonnaise. Contaminated eggs that have not undergone heat treatment pose a significant risk to public health, and outbreaks of S. Enteritidis have been repeatedly associated with raw or undercooked eggs [21].
In 2008, the OzFoodNet conveyed that 5.4 million cases of foodborne disease, occur in Australia annually, costing an estimated amount of $1.2 billion dollars per year, among which 8310 cases were found to be Salmonella infections at a rate of 39 cases per 100,000 population [4]. While improved sanitation and water supplies have made a significant contribution towards the decrease in incidence of enteric diseases, Salmonella spp. and Campylobacter spp. are commonly reported pathogens of community gastroenteritis [22].
Within raw egg products, homemade mayonnaise prepared with raw eggs is one of the most common foods linked to salmonellosis outbreaks [23]. Mayonnaise is a methodically prepared, semisolid (stabilized oil–water emulsion) dressing, which is a combination of raw eggs, vinegar, oil, and spices, and is perhaps one of the oldest and most widely used in the world [24,25]. Currently, in many countries it is not feasible to produce eggs guaranteed to be free from Salmonella contamination, and hence the control mechanisms utilized post-collections and during food handling are essential for protecting public health [12].
In the USA, it is estimated that there are around 1.4 million illnesses and 600 deaths caused by salmonellosis annually, with the most common serotypes identified as S. typhimurium and S. Enteritidis [26]. In fact, from 1998 to 2008 there were a total of 403 outbreaks of foodborne salmonellosis, and 112 were linked to eggs and raw egg products [27]. In 2009, it was estimated that there were a total of 6.2 million cases of salmonellosis in the European Union, and the incidence rate correlated with the prevalence of S. Enteritidis in laying hens [28]. In Australia in 2011, 45% of all salmonellosis outbreaks were linked to eggs or egg-related products [29]. Globally, there have been numerous published outbreaks of salmonellosis that have been caused by raw-egg mayonnaise [30]. In the U.K., a large outbreak of Salmonella typhimurium definitive type 49 was linked to eggs with raw-egg mayonnaise identified as the likely cause of infection [30]. Another outbreak of salmonellosis was also reported form the U.K. in December 2000, which identified egg mayonnaise sandwiches as the vehicle of infection [31]. Moreover, in Brazil, potato salad made with homemade mayonnaise and stored at unsuitable temperatures was associated with foodborne infection, and S. Enteritidis was identified as the infecting organism [32]. Additionally, in 2010, buffet dishes, which contained mayonnaise, was associated with a salmonellosis outbreak in Germany [33].
This review explores studies investigating different mechanisms for controlling Salmonella in raw-egg mayonnaise. The Salmonella serovar, country of study, and control mechanism investigated are presented in Table A1.

2. pH/Acid Tolerance and Temperature

The pH of mayonnaise plays an important role in its structure and stability [24]. Mayonnaise is an emulsion (Figure A1) stabilized by denatured proteins forming a network that can be impacted by the isoelectric pH of the egg yolk protein. When the charge on the proteins is minimized, the viscoelasticity and stability of the mayonnaise is at its highest [24].
Food safety guidelines published online by the Government of New South Wales (NSW), Australia, suggest that a pH at or below 4.2 has shown to be effective in controlling Salmonella in raw-egg products, however, there are numerous factors that influence the bactericidal efficiency such as the type of acid used [34,35], temperature [36], water activity [37], garlic, ginger, and pepper [38].
Many bacterial species induce responses to environmental stress [39]. When Salmonella spp. are exposed to a stress this can produce cross-tolerance to many or various stresses [40]. Gruzdev et al. reported that following carbon starvation, Salmonella spp. demonstrated greater tolerance to low pH, hyperosmolarity, heat, polymyxin B, and peroxides [41]. Another study conducted by Leyer and Johnson [42] demonstrated that exposure of Salmonella to mild acids (pH 5.8) could induce adaptation to lower pH, heat, NaCl (2.5 M), crystal violet, and polymyxin B. Additionally, subjecting S. enterica cells to an initial acid shock or pH 5.8 or 4.5 before inoculating mayonnaise (pH 4.2–4.5) increased the survival rate and persistence of the organism at 4 °C [43].
Salmonella can also achieve pH homeostasis, which is when the intracellular pH is maintained compared with the environmental pH [44]. Homeostasis is facilitated by cellular proton pumps and potassium/proton and sodium/proton antiport systems [45]. The ability of Salmonella to decrease proton extrusion and membrane proton conductance enables the cell to be protected against acid stress [46]. Additionally, S. typhimurium has a regulated response to further protect from acid stress, which is called the acid tolerance response (ATR) [47]. The ATR protects Salmonella spp. at pH levels of 3.0–4.0, but is activated when environmental pH values are between 6.0 and 5.5 and when pH homeostasis fails [47]. These pH conditions are referred to as the postshock stage and the preshock stage, respectively [47]. During the postshock stage, stimulation of 43 acid shock proteins takes place in order to prevent and repair the damage done to macromolecules by the acids [46].
In contrast, studies conducted by Álvarez-Ordóñez et al. [48] and Samelis et al. [49] suggest that S. typhimurium vulnerability to acid stress is dependent on growth temperature. S. typhimurium growth was observed in the temperature range of 25–37 °C at pH 4.5 [48,49]. Alali et al. [50] proposed that lowering the pH of the mayonnaise-based homemade salads decreased the rate of survival of Salmonella regardless of the temperature. According to a study conducted by Koutsoumanis et al. [51], the minimum pH value that permitted the growth of S. typhimurium was 3.94 within the temperature range 25–35 °C.

3. Vinegar vs. Lemon Juice

Jung and Beuchat [34] found that citric acid (lemon juice) was more effective at controlling S. typhimurium compared with acetic acid (vinegar/8.3 M), lactic acid (2 M), and malic acid (2 M) at an equivalent acid concentration of pH 5.4, 4.4, and 3.7. This is supported by work done by Zhu et al. (2012) which demonstrated that lemon juice was more effective than commercial wine vinegar at controlling Salmonella in mayonnaise spiked with either a mixture of S. Enteritidis (phage 4, 8, and 13) or a mixture of S. typhimurium, S. heidelberg and S. Enteritidis (untypeable phage type). It was also shown that both mixtures of Salmonella survived longer at 4 °C compared to 25 °C. The different bactericidal effects observed at different temperatures could be explained by more efficient cross-membrane migration of the organic acids at higher temperatures [36].
However, these findings differ from a study done by Perales and Garcia [52] that demonstrated that homemade mayonnaise made with vinegar had a greater bactericidal effect on S. Enteritidis compared with homemade mayonnaise made using lemon juice at the same pH (pH ranging from 3.6 to 5 [52]). This study was supported by Lock and Board [53], who also demonstrated that the number of S. Enteritidis PT4 organisms spiked into mayonnaise made with vinegar declined within six days of storage at 20 °C, but the same result was not observed when the mayonnaise was made to the same pH using lemon juice. Roller et al. (2000) concluded that chitosan added to mayonnaise containing acetic acid or lemon juice could be used as a preservative against the normal flora [54].

4. Addition of NaCl and Reduction of Water Activity

Several cellular mechanisms of bacterial cells are involved in osmoregulation, which regulates the osmolality of the cell, protecting physical and chemical properties of the intracellular environment in response to environmental stress [36]. It is achieved by accumulation of electrically neutral, low molecular weight compounds such as osmoprotectants (e.g., proline, glycine-betaine, or ectoine) inside the cell [55]. It is clear that Salmonella is adapted to endure prolonged starvation and desiccation periods [56]. It has been demonstrated that during the early stages of starvation, Salmonella can upregulate the osmoprotectant transporters (proP, proU, and osmU), ensuring the survival of this bacteria under low and intermediate moisture conditions [57].
Salt is a common preservative used in food products [58]. The sodium ions associate with water molecules to reduce the amount of unbound water in foods, making it difficult for the microorganisms to grow [59]. Salt can stimulate osmotic shock in microbial cells, affecting the growth and promoting cell death [60].
It has been shown that the permeability of the S. typhimurium cells is altered by heat, and this allows the sodium ions to penetrate the cell into the cytoplasm and interfere with the cell metabolism [61]. Although there are limited studies investigating the effect of salt concentration on Salmonella contamination of mayonnaise, there have been studies demonstrating that Salmonella spp. are capable of enduring extended starvation and desiccation stresses [62]. Even though reducing the amount of available water in food is a long-established method for controlling bacterial growth [37], there have been outbreaks of salmonellosis linked to foods with low water activity (aw), such as peanut butter [56]. Water activity is defined as the ratio of water vapor pressure (Pwv) in a food system to the saturation water vapor pressure (Pswv) at the temperature of the food system (Figure A2). Optimal growth of Salmonella spp. occurs when the aw is 0.99, but there is evidence that Salmonella may develop increased tolerance that allows for survival under low aw conditions for longer periods time (i.e., 43 days) [37]. According to Mattick et al. [37], Salmonella spp. are found to have an increased heat tolerance at low aw.

5. Garlic (Allium sativum)

According to the scripts found on ancient Egyptian pyramids, garlic has been used for medicinal purposes as well as a spice since ancient times [63]. In 1822, the antibacterial properties of onion and garlic were observed and recorded [64]. According to the literature, garlic contains strong antibacterial compounds that are effective against Salmonella and is often used as a spice for fermented fish [65]. Use of garlic in food products could increase the shelf life as well as decrease the potential for food poisoning [63]. Garlic, ginger, and pepper are known to contain bactericidal agents against Salmonella [38]. Traditional medicine uses the extract of these plants in order to treat infections caused by enteric bacteria like S. typhi [66]. It has been demonstrated that addition of 1% garlic to the mayonnaise inoculated with acid tolerance-induced S. Enteritidis reduced counts of the organism by 10-fold after 2 days compared with the control mayonnaise batch incubated without garlic [67].

6. Oils

Plant essential oils (PEOs) are well-known as antibacterial agents that could be used to control foodborne diseases [68]. These plant secondary metabolites are hydrophobic in nature and can be added to mayonnaise, which is advantageous because they can interact with the cell membranes of the bacteria, subsequently causing the cell components to flow out from the cell [69]. According to Wendakoon et al. [70], some PEOs can hinder the enzymatic reactions through the inhibition of the proteins of bacteria [70]. PEOs from mint, cinnamon, cardamom, and clove were found to reduce the bacterial count of S. Enteritidis in milk products, yogurt, and cucumber [71]. In a study conducted by Dabbah et al. [72], PEOs from orange, lemon, and grapefruit reduced the Salmonella count in milk. According to Valverde et al. [73], cinnamon bark oil at the concentration of 7000 ppm can be used to decrease Salmonella spp. in liquid whole eggs. Additionally, it has also been found that the antimicrobial activity of oregano essential oils (OEO) is improved when combined with ethylenediaminetetraacetic acid (EDTA) or nisin [74]. The inhibitory activity of nisin can be increased when combined with EDTA, which alters the bacterial outer membrane, enabling nisin to access the cytoplasmic membrane [75].

7. Fat Content

Juneja and Eblen (2000) reported that increased fat content in food decreased the water activity, which could lead to poor heat conductivity, increasing the survival rate of the pathogen S. typhimurium in beef. This is supported by a study that showed the fastest decrease in S. typhimurium was detected in fat-free mayonnaise (at pH 2.6) compared with full-fat mayonnaise at the same pH [76].

8. Conclusions

Salmonella contamination of raw egg products, such as mayonnaise, is a major issue of public health concern as a causative agent of salmonellosis outbreaks. This review paper explores studies that have that have investigated Salmonella control mechanisms within raw-egg mayonnaise. One of the main factors influencing the survival of Salmonella in mayonnaise, whilst also affecting the appearance and stability, is pH. Some studies indicate that Salmonella susceptibility to pH stresses may be dependent on the growth temperatures; however, this is still debated. Additionally, the effectiveness of pH as a control mechanism is influenced by the type of acid used. The effectiveness of lemon juice compared with vinegar as a control mechanism is also still debated, with current studies producing contradicting results. Additionally, evaluating the effectiveness of pH as a control mechanism is further complicated by the development of Salmonella cross-tolerance-induced responses, pH homeostasis achieved by the cellular antiport and symport systems, and ATR, which provides Salmonella with an added advantage to ensure survival under various pH environments. There have also been a few studies investigating the effectiveness of additive such as salt, garlic, and PEOs from mint, cinnamon, cardamom, and clove to inhibit the growth of Salmonella spp.
Currently, it is not possible to guarantee that raw-egg mayonnaise will not be contaminated with Salmonella. Therefore, there is an urgent need for further research to continue to explore the potential control mechanisms discussed in this paper. This will inform protocols for food handling and mayonnaise preparation to reduce the risk of foodborne salmonellosis.

Author Contributions

Thilini Keerthirathne drafted and edited the manuscript. Harriet Whiley concept, designed, supervised, coordinated, corrected and contributed to the manuscript. Kirstin Ross supervised, coordinated, corrected and contributed to the manuscript. Howard Fallowfield supervised, coordinated, corrected and contributed to the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Table A1. Salmonella serovar, country of study, and control mechanism investigated.
Table A1. Salmonella serovar, country of study, and control mechanism investigated.
CountrySalmonella spp.FoodControl MechanismsCommentsReference
U.K.S. EnteritidisMayonnaisepH20 mL vinegar (6% w/v acetic acid) per fresh egg yolk, 40 mL per fresh egg white or 60 mL per fresh whole egg was used. Should be held at 20 °C or above for at least 48 h before refrigeration or consumption.[77]
U.K.S. EnteritidisMayonnaise-based shrimp saladpH/preservatives chitosan and acetic acidChitosan could be useful as a preservative combined with acetic acid.[54]
China/U.S.S. typhimurium S. heidelberg S. EnteritidisHome-Style MayonnaisepH commercial wine vinegar, lemon juice, and acetic or citric acidSalmonella counts in acid solutions at 4 °C were reported as significantly higher than those in samples at 25 °C. Viability of Salmonella decreased as the amounts of vinegar and lemon juice in mayonnaise increased.[35]
FranceS. typhimuriumReduced-calorie mayonnaisepH/TemperatureHigher temperature with a low pH, greater the inactivation of the organism.[78]
U.S.SalmonellaMayonnaise-based potato salad, macaroni salad, and coleslawpH, NaCl, and temperatureDecreased pH and increased the bactericidal activity irrespective of sodium concentration or storage temperature Sodium concentrations had little or no effect on the behavior of Salmonella when stored at 4 or 10 °C for up to 27 days.[50]
U.K.S. EnteritidisMayonnaisepH acetic acid (vinegar)Mayonnaise made with vinegar to a pH of 4.1 or less controlled S. Enteritidis. Storage of mayonnaise at refrigeration temperatures protected Salmonella spp. from acidulants and therefore a holding time of 24 h at 18–22 °C was advised before refrigeration.[79]
SpainS. EnteritidisHome-made MayonnaisepH/temperatureVinegar was used as an acidulant to achieve a pH of 3.6–4 and storage in a warm place is recommended.[52]
U.S.S. senftenbergEgg saladspH/temperatureSignificant decrease in Salmonella numbers, particularly during storage at room temperature (22 °C) at the acidity ranging from pH 4.25–4.30 was recorded.[80]
BrazilS. EnteritidisMayonnaiseoil oregano essential oilNatural antimicrobial to reduce the S. Enteritidis growth[81]
SpainS. EnteritidisEgg mayonnaiseoil (virgin olive oil)Egg mayonnaise made with virgin olive oil required more than 48 h to reduce the number of microorganisms to an undetectable level.[54]
U.K.S. EnteritidisHomemade MayonnaiseTemperature, pH, oils (olive oil with garlic, basil, soya, grapeseed, rapeseed, groundnut, sunflower, hazelnut)The death rate of the S. Enteritidis differed with the various oils.[82]
BrazilS. EnteritidisMayonnaiseoil oregano essential oils (OEO1/OEO2) Nisin EDTAAntimicrobial activity of OEO against S. Enteritidis was improved when combined with nisin or EDTA.[74]
U.K,S. EnteritidisMayonnaisegarlicGarlic (1%) reduced the viable cells of S. Enteritidis in mayonnaise by a factor of 10.[67]
GreeceS. EnteritidisMayonnais- based Aubergine saladsorbic/benzoic acidsAddition of preservatives decreased the pathogen survival.[83]
U.K.S. EnteritidisMayonnaisepHWithin the pH 4.2–4.5 S. Enteritidis remained stable for 4 weeks at 4 °C.[43]
Figure A1. Preparation of mayonnaise [74,81,82,84,85].
Figure A1. Preparation of mayonnaise [74,81,82,84,85].
Pathogens 05 00063 g001
Figure A2. Definition of water activity.
Figure A2. Definition of water activity.
Pathogens 05 00063 g002


  1. Newman, K.L.; Leon, J.S.; Rebolledo, P.A.; Scallan, E. The impact of socioeconomic status on foodborne illness in high-income countries: A systematic review. Epidemiol. Infect. 2015, 143, 2473–2485. [Google Scholar] [CrossRef] [PubMed]
  2. Scharff, R.L. Economic burden from health losses due to foodborne illness in the united states. J. Food Prot. 2012, 75, 123–131. [Google Scholar] [CrossRef] [PubMed]
  3. Thomas, M.K.; Murray, R.; Flockhart, L.; Pintar, K.; Pollari, F.; Fazil, A.; Nesbitt, A.; Marshall, B. Estimates of the burden of foodborne illness in canada for 30 specified pathogens and unspecified agents, circa 2006. Foodborne Pathog. Dis. 2013, 10, 639–648. [Google Scholar] [CrossRef] [PubMed]
  4. Hall, G.; Kirk, M.D.; Becker, N.; Gregory, J.E.; Unicomb, L.; Millard, G.; Stafford, R.; Lalor, K.; Group, O.W. Estimating foodborne gastroenteritis, australia. Emerg. Infect. Dis. 2005, 11, 1257–1264. [Google Scholar] [CrossRef] [PubMed]
  5. Majowicz, S.E.; Musto, J.; Scallan, E.; Angulo, F.J.; Kirk, M.; O’Brien, S.J.; Jones, T.F.; Fazil, A.; Hoekstra, R.M.; International Collaboration on Enteric Disease Burden of Illness Studies. The global burden of nontyphoidal salmonella gastroenteritis. Clin. Infect. Dis. 2010, 50, 882–889. [Google Scholar] [CrossRef] [PubMed]
  6. Janda, J.M.; Abbott, S.L. The family enterobacteriaceae. In Practical Handbook of Microbiology, 3rd ed.; CRC Press: Boca Raton, FL, USA, 2015; p. 307. [Google Scholar]
  7. Batista, D.F.A.; Freitas Neto, O.C.; Barrow, P.A.; de Oliveira, M.T.; Almeida, A.M.; Ferraudo, A.S.; Berchieri, A., Jr. Identification and characterization of regions of difference between the salmonella gallinarum biovar gallinarum and the salmonella gallinarum biovar pullorum genomes. Infect. Genet. Evol. 2015, 30, 74–81. [Google Scholar] [CrossRef] [PubMed]
  8. Gal-Mor, O.; Boyle, E.C.; Grassl, G.A. Same species, different diseases: How and why typhoidal and non-typhoidal salmonella enterica serovars differ. Front. Microbiol. 2014, 5, 391. [Google Scholar] [CrossRef] [PubMed]
  9. Rabsch, W.; Andrews, H.L.; Kingsley, R.A.; Prager, R.; Tschäpe, H.; Adams, L.G.; Bäumler, A.J. Salmonella enterica serotype typhimurium and its host-adapted variants. Infect. Immun. 2002, 70, 2249–2255. [Google Scholar] [CrossRef] [PubMed]
  10. Centers for Disease Control Prevention. Multistate outbreak of salmonella serotype tennessee infections associated with peanut butter—United states, 2006–2007. Morb. Mortal. Wkly. Rep. 2007, 56, 521–524. [Google Scholar]
  11. Wilson, M.R.; Brown, E.; Keys, C.; Strain, E.; Luo, Y.; Muruvanda, T.; Grim, C.; Beaubrun, J.J.-G.; Jarvis, K.; Ewing, L. Whole genome DNA sequence analysis of salmonella subspecies enterica serotype tennessee obtained from related peanut butter foodborne outbreaks. PLoS ONE 2016, 11, e0146929. [Google Scholar] [CrossRef] [PubMed]
  12. Whiley, H.; Ross, K. Salmonella and eggs: From production to plate. Int. J. Environ. Res. Public Health 2015, 12, 2543–2556. [Google Scholar] [CrossRef] [PubMed]
  13. Mishu, B.; Koehler, J.; Lee, L.A.; Rodrigue, D.; Brenner, F.H.; Blake, P.; Tauxe, R.V. Outbreaks of salmonella enteritidis infections in the united states, 1985–1991. J. Infect. Dis. 1994, 169, 547–552. [Google Scholar] [CrossRef] [PubMed]
  14. Delarocque-Astagneau, E.; Desenclos, J.-C.; Bouvet, P.; Grimont, P. Risk factors for the occurrence of sporadic salmonella enterica serotype enteritidis infections in children in france: A national case-control study. Epidemiol. Infect. 1998, 121, 561–567. [Google Scholar] [CrossRef] [PubMed]
  15. De Reu, K.; Grijspeerdt, K.; Messens, W.; Heyndrickx, M.; Uyttendaele, M.; Debevere, J.; Herman, L. Eggshell factors influencing eggshell penetration and whole egg contamination by different bacteria, including salmonella enteritidis. Int. J. Food Microbiol. 2006, 112, 253–260. [Google Scholar] [CrossRef] [PubMed]
  16. Sauter, E.; Petersen, C. The effect of egg shell quality on penetration by various salmonellae. Poult. Sci. 1974, 53, 2159–2162. [Google Scholar] [CrossRef] [PubMed]
  17. Berrang, M.; Frank, J.; Buhr, R.; Bailey, J.; Cox, N.; Mauldin, J. Eggshell characteristics and penetration by salmonella through the productive life of a broiler breeder flock. Poult. Sci. 1998, 77, 1446–1450. [Google Scholar] [CrossRef] [PubMed]
  18. Nascimento, V.; Cranstoun, S.; Solomon, S. Relationship between shell structure and movement of salmonella enteritidis across the eggshell wall. Br. Poult. Sci. 1992, 33, 37–48. [Google Scholar] [CrossRef] [PubMed]
  19. Bruce, J.; Johnson, A. The bacterial flora of unhatched eggs. Br. Poult. Sci. 1978, 19, 681–689. [Google Scholar] [CrossRef]
  20. De Oliveira Elias, S.; Tomasco, P.V.; Alvarenga, V.O.; de Souza Sant’Ana, A.; Tondo, E.C. Contributor factors for the occurrence of salmonellosis during preparation, storage and consumption of homemade mayonnaise salad. Food Res. Int. 2015, 78, 266–273. [Google Scholar] [CrossRef]
  21. Centers for Disease Control Prevention. Outbreaks of salmonella serotype enteritidis infection associated with consumption of raw shell eggs—United states, 1994–1995. Morb. Mortal. Wkly. Rep. 1996, 45, 737–742. [Google Scholar]
  22. Sinclair, M.; Hellard, M.; Wolfe, R.; Fairley, C. Pathogens Causing Community Gastroenteritis in Australia [Poster Abstract]. In Proceedings of the Australian Society for Infectious Disease Conference, Barossa Valley, South Australia, 13–17 April 2002.
  23. Scallan, E.; Hoekstra, R.M.; Angulo, F.J.; Tauxe, R.V.; Widdowson, M.-A.; Roy, S.L.; Jones, J.L.; Griffin, P.M. Foodborne illness acquired in the united states—Major pathogens. Emerg. Infect. Dis. 2011, 17, 7–15. [Google Scholar] [CrossRef] [PubMed]
  24. Depree, J.; Savage, G. Physical and flavour stability of mayonnaise. Trends Food Sci. Technol. 2001, 12, 157–163. [Google Scholar] [CrossRef]
  25. Di Mattia, C.; Balestra, F.; Sacchetti, G.; Neri, L.; Mastrocola, D.; Pittia, P. Physical and structural properties of extra-virgin olive oil based mayonnaise. LWT-Food Scie. Technol. 2015, 62, 764–770. [Google Scholar] [CrossRef]
  26. Mead, P.S.; Slutsker, L.; Dietz, V.; McCaig, L.F.; Bresee, J.S.; Shapiro, C.; Griffin, P.M.; Tauxe, R.V. Food-related illness and death in the united states. Emerg. Infect. Dis. 1999, 5, 607–625. [Google Scholar] [CrossRef] [PubMed]
  27. Jackson, B.R.; Griffin, P.M.; Cole, D.; Walsh, K.A.; Chai, S.J. Outbreak-associated salmonella enterica serotypes and food commodities, united states, 1998–2008. Emerg. Infect. Dis. 2013, 19, 1239–1244. [Google Scholar] [CrossRef] [PubMed]
  28. Havelaar, A.H.; Ivarsson, S.; Lofdahl, M.; Nauta, M.J. Estimating the true incidence of campylobacteriosis and salmonellosis in the european union, 2009. Epidemiol. Infect. 2013, 141, 293–302. [Google Scholar] [CrossRef] [PubMed]
  29. OzFoodNet Working Group. Monitoring the incidence and causes of diseases potentially transmitted by food in australia: Annual report of the ozfoodnet network, 2011. Commun. Dis. Intell. Q. Rep. 2015, 39, E236–E264. [Google Scholar]
  30. Mitchell, E.; O’Mahony, M.; Lynch, D.; Ward, L.; Rowe, B.; Uttley, A.; Rogers, T.; Cunningham, D.; Watson, R. Large outbreak of food poisoning caused by salmonella typhimurium definitive type 49 in mayonnaise. Br. Med. J. 1989, 298, 99–101. [Google Scholar] [CrossRef]
  31. Mason, B.; Williams, N.; Salmon, R.; Lewis, A.; Price, J.; Johnston, K.; Trott, R. Outbreak of salmonella indiana associated with egg mayonnaise sandwiches at an acute nhs hospital. Commun. Dis. Public Health/PHLS 2001, 4, 300–304. [Google Scholar]
  32. Carneiro, M.R.P.; Cabello, P.H.; Albuquerque-Junior, R.L.C.; Jain, S.; Candido, A.L. Characterization of a foodborne outbreak caused by salmonella enteritidis in aracaju, state of sergipe, brazil. Rev. Soc. Bras. Med. Trop. 2015, 48, 334–337. [Google Scholar] [CrossRef] [PubMed]
  33. Von Wissmann, B.; Klinc, C.; Schulze, R.; Wolf, A.; Schreiner, H.; Rabsch, W.; Prager, R.; Hautmann, W. Outbreak of salmonellosis after a wedding party, bavaria, germany, summer 2010: The importance of implementing food safety concepts. Eurosurveillance 2012, 17, 20076. [Google Scholar] [PubMed]
  34. Jung, Y.; Beuchat, L. Sensitivity of multidrug-resistant salmonella typhimurium dt104 to organic acids and thermal inactivation in liquid egg products. Food Microbiol. 2000, 17, 63–71. [Google Scholar] [CrossRef]
  35. Zhu, J.; Li, J.; Chen, J. Survival of salmonella in home-style mayonnaise and acid solutions as affected by acidulant type and preservatives. J. Food Prot. 2012, 75, 465–471. [Google Scholar] [CrossRef] [PubMed]
  36. Yang, Y.; Khoo, W.J.; Zheng, Q.; Chung, H.-J.; Yuk, H.-G. Growth temperature alters salmonella enteritidis heat/acid resistance, membrane lipid composition and stress/virulence related gene expression. Int. J. Food Microbiol. 2014, 172, 102–109. [Google Scholar] [CrossRef] [PubMed]
  37. Mattick, K.; Jørgensen, F.; Legan, J.; Cole, M.; Porter, J.; Lappin-Scott, H.; Humphrey, T. Survival and filamentation of salmonella entericaserovar enteritidis pt4 and salmonella enterica serovar typhimurium dt104 at low water activity. Appl. Environ. Microbiol. 2000, 66, 1274–1279. [Google Scholar] [CrossRef] [PubMed]
  38. Indu, M.; Hatha, A.; Abirosh, C.; Harsha, U.; Vivekanandan, G. Antimicrobial activity of some of the south-indian spices against serotypes of escherichia coli, salmonella, listeria monocytogenes and aeromonas hydrophila. Braz. J. Microbiol. 2006, 37, 153–158. [Google Scholar] [CrossRef]
  39. Alvarez-Ordóñez, A.; Broussolle, V.; Colin, P.; Nguyen-The, C.; Prieto, M. The adaptive response of bacterial food-borne pathogens in the environment, host and food: Implications for food safety. Int. J. Food Microbiol. 2015, 213, 99–109. [Google Scholar] [CrossRef] [PubMed]
  40. Hiramatsu, R.; Matsumoto, M.; Sakae, K.; Miyazaki, Y. Ability of shiga toxin-producing escherichia coli and salmonella spp. To survive in a desiccation model system and in dry foods. Appl. Environ. Microbiol. 2005, 71, 6657–6663. [Google Scholar] [CrossRef] [PubMed]
  41. Gruzdev, N.; Pinto, R.; Sela, S. Effect of desiccation on tolerance of salmonella enterica to multiple stresses. Appl. Environ. Microbiol. 2011, 77, 1667–1673. [Google Scholar] [CrossRef] [PubMed]
  42. Leyer, G.; Johnson, E. Acid adaptation induces cross-protection against environmental stresses in salmonella typhimurium. Appl. Environ. Microbiol. 1993, 59, 1842–1847. [Google Scholar] [PubMed]
  43. Leuschner, R.G.; Boughtflower, M.P. Standardized laboratory-scale preparation of mayonnaise containing low levels of salmonella enterica serovar enteritidis. J. Food Prot. 2001, 64, 623–629. [Google Scholar] [PubMed]
  44. Krulwich, T.A.; Sachs, G.; Padan, E. Molecular aspects of bacterial ph sensing and homeostasis. Nat. Rev. Microbiol. 2011, 9, 330–343. [Google Scholar] [CrossRef] [PubMed]
  45. Booth, I.R. Regulation of cytoplasmic ph in bacteria. Microbiol. Rev. 1985, 49, 359–378. [Google Scholar] [PubMed]
  46. Foster, J.W.; Hall, H.K. Inducible ph homeostasis and the acid tolerance response of salmonella typhimurium. J. Bacteriol. 1991, 173, 5129–5135. [Google Scholar] [CrossRef] [PubMed]
  47. Foster, J.W.; Hall, H.K. Adaptive acidification tolerance response of salmonella typhimurium. J. Bacteriol. 1990, 172, 771–778. [Google Scholar] [CrossRef] [PubMed]
  48. Álvarez-Ordóñez, A.; Fernández, A.; Bernardo, A.; López, M. Acid tolerance in salmonella typhimurium induced by culturing in the presence of organic acids at different growth temperatures. Food Microbiol. 2010, 27, 44–49. [Google Scholar] [CrossRef] [PubMed]
  49. Samelis, J.; Ikeda, J.; Sofos, J. Evaluation of the ph-dependent, stationary-phase acid tolerance in listeria monocytogenes and salmonella typhimurium dt104 induced by culturing in media with 1% glucose: A comparative study with Escherichia coli o157: H7. J. Appl. Microbiol. 2003, 95, 563–575. [Google Scholar] [CrossRef] [PubMed]
  50. Alali, W.Q.; Mann, D.A.; Beuchat, L.R. Viability of salmonella and listeria monocytogenes in delicatessen salads and hummus as affected by sodium content and storage temperature. J. Food Prot. 2012, 75, 1043–1056. [Google Scholar] [CrossRef] [PubMed]
  51. Koutsoumanis, K.P.; Kendall, P.A.; Sofos, J.N. Modeling the boundaries of growth of salmonella typhimurium in broth as a function of temperature, water activity, and ph. J. Food Prot. 2004, 67, 53–59. [Google Scholar] [PubMed]
  52. Perales, I.; Garcia, M. The influence of ph and temperature on the behaviour of salmonella enteritidis phage type 4 in home-made mayonnaise. Lett. Appl. Microbiol. 1990, 10, 19–22. [Google Scholar] [CrossRef]
  53. Lock, J.; Board, R. The fate of salmonella enteritidis pt4 in home-made mayonnaise prepared from artificially inoculated eggs. Food Microbiol. 1995, 12, 181–186. [Google Scholar] [CrossRef]
  54. Roller, S.; Covill, N. The antimicrobial properties of chitosan in mayonnaise and mayonnaise-based shrimp salads. J. Food Prot. 2000, 63, 202–209. [Google Scholar] [PubMed]
  55. Csonka, L.N.; Hanson, A.D. Prokaryotic osmoregulation: Genetics and physiology. Annu. Rev. Microbiol. 1991, 45, 569–606. [Google Scholar] [CrossRef] [PubMed]
  56. Podolak, R.; Enache, E.; Stone, W.; Black, D.G.; Elliott, P.H. Sources and risk factors for contamination, survival, persistence, and heat resistance of salmonella in low-moisture foods. J. Food Prot. 2010, 73, 1919–1936. [Google Scholar] [PubMed]
  57. Finn, S.; Händler, K.; Condell, O.; Colgan, A.; Cooney, S.; McClure, P.; Amézquita, A.; Hinton, J.C.; Fanning, S. Prop is required for the survival of desiccated salmonella enterica serovar typhimurium cells on a stainless steel surface. Appl. Environ. Microbiol. 2013, 79, 4376–4384. [Google Scholar] [CrossRef] [PubMed]
  58. Rahman, M.S. Hurdle Technology in Food Preservation. In Minimally Processed Foods; Springer: Cham, Switzerland, 2015; pp. 17–33. [Google Scholar]
  59. Henry, J.E.; Taylor, C.L. Strategies to Reduce Sodium Intake in the United States; National Academies Press: Washington, DC, USA, 2010. [Google Scholar]
  60. Davidson, P.M.; Taylor, T.M.; Schmidt, S.E. Chemical Preservatives and Natural Antimicrobial Compounds. In Food Microbiology; American Society of Microbiology: Washington, DC, USA, 2013; pp. 765–801. [Google Scholar]
  61. Manas, P.; Pagan, R.; Leguérinel, I.; Condon, S.; Mafart, P.; Sala, F. Effect of sodium chloride concentration on the heat resistance and recovery of salmonella typhimurium. Int. J. Food Microbiol. 2001, 63, 209–216. [Google Scholar] [CrossRef]
  62. Finn, S.; Condell, O.; McClure, P.; Amézquita, A.; Fanning, S. Mechanisms of survival, responses and sources of salmonella in low-moisture environments. Front. Microbiol. 2013, 4, 331. [Google Scholar] [CrossRef] [PubMed]
  63. Kumar, M.; Berwal, J. Sensitivity of food pathogens to garlic (allium sativum). J. Appl. Microbiol. 1998, 84, 213–215. [Google Scholar] [CrossRef] [PubMed]
  64. Johnson, M.G.; Vaughn, R.H. Death of salmonella typhimurium and escherichia coli in the presence of freshly reconstituted dehydrated garlic and onion. Appl. Microbiol. 1969, 17, 903–905. [Google Scholar] [PubMed]
  65. Bernbom, N.; Ng, Y.Y.; Paludan-Müller, C.; Gram, L. Survival and growth of salmonella and vibrio in som-fak, a thai low-salt garlic containing fermented fish product. Int. J. Food Microbiol. 2009, 134, 223–229. [Google Scholar] [CrossRef] [PubMed]
  66. Ekwenye, U.; Elegalam, N. Antibacterial activity of ginger (zingiber officinale roscoe and garlic (allium sativum l.) extracts on escherichia coli and salmonella typhi. Int. J. Mol. Adv. Sci. 2005, 1, 411–416. [Google Scholar]
  67. Leuschner, R.G.; Zamparini, J. Effects of spices on growth and survival of escherichia coli 0157 and salmonella enterica serovar enteritidis in broth model systems and mayonnaise. Food Control 2002, 13, 399–404. [Google Scholar] [CrossRef]
  68. Bajpai, V.; Rahman, A.; Dung, N.; Huh, M.; Kang, S. In vitro inhibition of food spoilage and foodborne pathogenic bacteria by essential oil and leaf extracts of magnolia liliflora desr. J. Food Sci. 2008, 73, M314–M320. [Google Scholar] [CrossRef] [PubMed]
  69. Lambert, R.; Skandamis, P.N.; Coote, P.J.; Nychas, G.J. A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J. Appl. Microbiol. 2001, 91, 453–462. [Google Scholar] [CrossRef] [PubMed]
  70. Wendakoon, C.N.; Sakaguchi, M. Inhibition of amino acid decarboxylase activity of enterobacter aerogenes by active components in spices. J. Food Prot. 1995, 58, 280–283. [Google Scholar]
  71. Tassou, C.; Drosinos, E.; Nychas, G. Effects of essential oil from mint (mentha piperita) on salmonella enteritidis and listeria monocytogenes in model food systems at 4 and 10 c. J. Appl. Bacteriol. 1995, 78, 593–600. [Google Scholar] [CrossRef] [PubMed]
  72. Dabbah, R.; Edwards, V.; Moats, W. Antimicrobial action of some citrus fruit oils on selected food-borne bacteria. Appl. Microbiol. 1970, 19, 27–31. [Google Scholar] [PubMed]
  73. Valverde, M.; Iniesta, F.; Garrido, L.; Rodríguez, A.; García-García, I.; Macanas, H.; Roda, R. Inactivation of Salmonella spp. in Refrigerated Liquid Egg Products Using Essential Oils and Their Active Compounds. In Proceedings of the International Conference on Food Innovation “Food Innova”, Universitydad Politecnica De Valencia, Valencia, Spain, 25–26 October 2010.
  74. Da Silva, J.P.L.; de Souza, E.F.; Della Modesta, R.C.; Gomes, I.A.; Freitas-Silva, O.; de Melo Franco, B.D.G. Antibacterial activity of nisin, oregano essential oil, edta, and their combination against salmonella enteritidis for application in mayonnaise. Vigil. Sanit. Debate Soc. Ciênc. Tecnol. 2016, 4, 83–91. [Google Scholar] [CrossRef]
  75. Stevens, K.; Klapes, N.; Sheldon, B.; Klaenhammer, T. Antimicrobial action of nisin against salmonella typhimurium lipopolysaccharide mutants. Appl. Environ. Microbiol. 1992, 58, 1786–1788. [Google Scholar] [PubMed]
  76. Lock, J.; Board, R. The fate of salmonella enteritidis pt4 in deliberately infected commercial mayonnaise. Food Microbiol. 1994, 11, 499–504. [Google Scholar] [CrossRef]
  77. Xiong, R.; Xie, G.; Edmondson, A. Modelling the ph of mayonnaise by the ratio of egg to vinegar. Food Control 2000, 11, 49–56. [Google Scholar] [CrossRef]
  78. Membre, J.-M.; Majchrzak, V.; Jolly, I. Effects of temperature, ph, glucose, and citric acid on the inactivation of salmonella typhimurium in reduced calorie mayonnaise. J. Food Prot. 1997, 60, 1497–1501. [Google Scholar]
  79. Radford, S.; Board, R. Review: Fate of pathogens in home-made mayonnaise and related products. Food Microbiol. 1993, 10, 269–278. [Google Scholar] [CrossRef]
  80. Simmons, S.E.; Bartolucci, D.P.; Stadelman, W. Formulation and evaluation of a low ph egg salad. J. Food Sci. 1979, 44, 1501–1504. [Google Scholar] [CrossRef]
  81. Da Silva, J.P.L.; de Melo, B.D.G. Application of oregano essential oil against salmonella enteritidis in mayonnaise salad. Int. J. Food Sci. Nutr. Eng. 2012, 2, 70–75. [Google Scholar] [CrossRef]
  82. Lock, J.; Board, R. The influence of acidulants and oils on autosterilization of home-made mayonnaise. Food Res. Int. 1995, 28, 569–572. [Google Scholar] [CrossRef]
  83. Tassou, C.C.; Samaras, F.J.; Arkoudelos, J.S.; Mallidis, C.G. Survival of acid-adapted or non-adapted salmonella enteritidis, listeria monocytogenes and escherichia coli o157: H7, in traditional greek salads. Int. J. Food Sci. Technol. 2009, 44, 279–287. [Google Scholar] [CrossRef]
  84. Giacintucci, V.; Di Mattia, C.; Sacchetti, G.; Neri, L.; Pittia, P. Role of olive oil phenolics in physical properties and stability of mayonnaise-like emulsions. Food Chem. 2016, 213, 369–377. [Google Scholar] [CrossRef] [PubMed]
  85. Medina, E.; Romero, C.; Brenes, M.; de Castro, A. Antimicrobial activity of olive oil, vinegar, and various beverages against foodborne pathogens. J. Food Prot. 2007, 70, 1194–1199. [Google Scholar] [PubMed]

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Keerthirathne, T.P.; Ross, K.; Fallowfield, H.; Whiley, H. A Review of Temperature, pH, and Other Factors that Influence the Survival of Salmonella in Mayonnaise and Other Raw Egg Products. Pathogens 2016, 5, 63.

AMA Style

Keerthirathne TP, Ross K, Fallowfield H, Whiley H. A Review of Temperature, pH, and Other Factors that Influence the Survival of Salmonella in Mayonnaise and Other Raw Egg Products. Pathogens. 2016; 5(4):63.

Chicago/Turabian Style

Keerthirathne, Thilini Piushani, Kirstin Ross, Howard Fallowfield, and Harriet Whiley. 2016. "A Review of Temperature, pH, and Other Factors that Influence the Survival of Salmonella in Mayonnaise and Other Raw Egg Products" Pathogens 5, no. 4: 63.

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