Antimicrobial Effects of Lactates: a Review

Antimicrobial Effects of Lactates: A Review

LEORA A. SHELEF

Department of Nutrition and Food Science, Wayne State University, Detroit Michigan 48202

(Received October 13, 1993/Accepted January 10, 1994) Downloaded from http://meridian.allenpress.com/jfp/article-pdf/57/5/445/1664955/0362-028x-57_5_445.pdf by guest on 24 September 2021 ABSTRACT TABLE 1. Properties of lactic acid.

Sodium lactate is used as humectant and flavor enhancer in A derivative of fatty acid (propionic). M.W. 90.08. meat and poultry products, and there is growing evidence of antimicrobial properties of the salt. Potassium and calcium lactate Colorless, nonvolatile, viscous liquid (7 cp for 65% solution at are equally effective in controlling growth of aerobes and anaer- 25°C), with acrid taste. GRAS additive for general purposes. obes in meats, and antibotulinal and antilisterial activities of the lactate anion have been established. The specific action of lactate Dissociation constant, pKa = 3.86. on the microbial cell is not well understood. No intracellular pH lowering effect could be demonstrated, and the reported small Very soluble in water. Density (60% solution) = 1.14. decreases in water activity appear insufficient to explain the effect. Other explanations have been proposed but not yet con- The acid undergoes self-esterification and lactoyllactic acid, CH CH(OH)COOCH(CH )COOH, forms: 4.2% in a 6.3% solu- firmed. Although lactates appear to be bacteriostatic, their ability 3 3 to control spoilage and pathogenic bacteria in fresh and processed tion; 12.3% in 55% solution and 33.8% in 88.6% solution. meat favors their use, particularly in refrigerated meat products in pH of aqueous solutions at 25°C: 1% - 2.28; 10% - 1.75. combination with other microbial inhibitors. Corrosive; one of the most difficult acids to handle. )' Key Words: Antimicrobial, lactates, water activity (aw meat

TABLE 2. Major uses of lactic acid. Lactic acid is one of the most widely distributed acids in nature, and together with acetic acid is the most widely Cheese curd - adjusting to pH 4.8-5.2 before processing improves employed as preservative. The food-grade acid is produced flavor, texture and stability. by controlled fermentation of refined sucrose or other carbohydrate sources. The compound is purified by conver- Unsalted butter - improves shelf stability. sion to crystalline calcium lactate, which is then treated with sulfuric acid to give solutions of the pure acid (24). Egg whites - adjusting the pH before drying improves protein dispersion, powder stability and whipping properties. The acid is also manufactured synthetically by hydrolysis of lactonitrile. Major properties of lactic acid, which is a Egg yolks - improves the shelf stability of mayonnaise. GRAS additive (3), are summarized in Table 1, and its major uses in foods are summarized in Table 2. Beer - prevents butyric acid bacteria during fermentation. Most applications of lactic acid, used for improving the quality of a variety of foods and for controlling microbial Bread dough - prevents "ropiness" without affecting yeast fermen- growth, are associated with the pH lowering effect. For tation. example, the pH of a 1% aqueous solution of the acid is Hard candy - prevents crystallization (in combination with the 2.28, and sprays of 1 to 3% solutions are most often used sodium salt for buffering effect). to sanitize meat surfaces. The treatment results in reduction in viable counts during storage of the carcasses, and is Infant foods containing dried milk - precipitates the proteins and especially effective if done early, before bacteria are frrmly renders them more digestible. The acid (0.3%) or its salts act as attached to the meat surfaces, since attached organisms antibacterials and regulators of intestinal flora. tend to be more acid resistant. The decontaminating prop- Olives - maintains clarity of the brine. erties of the acid in meat have been reviewed extensively (10,15,53,60). The psychrotrophic gram-negative bacteria Pickles and relishes - improves taste. that cause meat spoilage are generally sensitive to the treatment, and a shift towards a predominantly gram-posi- Cattle, sheep and poultry carcasses - lowers the viable counts tive flora is favored, For example, decontamination of veal during storage by dipping in solution or spraying (1-3% acid) before bacteria become attached to the surface. tongues with 2% lactic acid, followed by vacuum-packing,

JOURNAL OF FOOD PROTECTION, VOL. 57, MAY 1994 increased the shelf-life and decreased the bacterial counts LACTATES AS ANTIMICROBIAL ADDITIVES by almost 3 loglo cycles (58). Lowering of the pH by the acid may adversely affect taste and other properties of the Until recently, there have been scant reports on antimi- food. For example, addition of the acid to fresh meat causes crobial activities of salts of lactic acid. Growth suppression oxidation of myoglobin and darkening of the tissue (10). of Bacillus cereus, B. subtilis and B. circulans was observed in broth containing 0.3% sodium lactate and com- SALTS OF LACTIC ACID plete inhibition required 12% of the salt (2). In 1972 Krol (34) reported decreased growth of lactobacilli, micrococci The sodium, potassium and calcium salts of lactic acid and "Achromobacter" species in dry-cured, country-style are approved for use in foods as direct food ingredients (3). ham formulated with sodium lactate. L-lactate at a concen- Major properties and uses of these salts are summarized in tration found in muscle of low pH (ca. 100 mM) prevented Table 3. Sodium and potassium lactate (CH)CHOHCOONa, anaerobic growth of gram-negative fermentative bacteria mol wt 112.07, and CH)CHOHCOOK, mol wt 128.18, (Serratia liquefaciens, Yersinia enterocolitica, Enterobacter respectively) are generally available as 60% aqueous solu- cloacae and Aeromonas hydrophila) in buffered broth at tions with a neutral pH. They are used as humectants and pH 5.55 and also prevented aerobic growth of the aeromonad, Downloaded from http://meridian.allenpress.com/jfp/article-pdf/57/5/445/1664955/0362-028x-57_5_445.pdf by guest on 24 September 2021 flavor enhancers in meat and poultry products and contrib- but no inhibition was seen at pH 6.1 (26). ute to increased cooking yields and water holding capacity Since 1989, the potential benefits of sodium lactate as (16,45). Levels of 2% (3.3% of the 60% solutions) are used an antimicrobial agent spurred interest in research on its in hot dogs, frankfurters and similar products. Injection of effects in meat products. Studies focused on changes in beef roasts with 4% solution of sodium lactate before total aerobes and anaerobes in fresh or cooked meats and cooking was reported to increase the cooking yield up to poultry under various packaging conditions, and specific 15%, improve palatability and lower the aerobic plate effects on Clostridium botulinum and Listeria monocyto- counts during refrigerated storage (20). genes were also reported. A summary of the reports outlin- Calcium lactate (Ca[CH)CHOHCOO]2' mol wt 218.22) ing the tested products and lactate levels, storage conditions is a hygroscopic powder available in the monohydrate or and the antimicrobial effects is shown in Table 4. Although the more stable pentahydrate form. In addition to its use for the sodium salt has been used most often, potassium lactate dietary calcium supplementation, major applications are in demonstrated similar antimicrobial effects. The effects at gel formation with low methylated pectin and prevention of the recommended levels of 2% based on the final weight of "ropiness" in bread dough, as well as a firming agent the product or even twice that amount were generally (Table 3). bacteriostatic and concentration-dependent. Since in most studies the meats were formulated to simulate commercial TABLE 3. Properties of salts of lactic acid. products, the effect of lactate was not differentiated from that of its combination with sodium chloride (NaCl), and in Sodium and potassium lactate some tests also with nitrites. Combinations with NaCl were reported to reduce the effective dose of the lactate salt Available primarily as 60% solutions with neutral pH. (1,9,38,50). In addition, pumping brine containing 10% NaCl and 20% sodium lactate into beef roasts showed Used as emulsifiers, humectants and pH control agents. (2-3% protection against survival and growth of C. sporogenes recommended. ) and L. monocytogenes in temperature-abused cooked-in- Flavor enhancers (adjuvants) in meat and poultry products; in- the-bag products (56). crease water holding capacity and cooking yields. MECHANISM OF INHIBITION 2% lactate, based on final weight of the product, is recommended in meat and poultry products. Studies on the specific action of lactate on the microbial cell are limited (32), but at least two possible mecha- Calcium lactate nisms have been proposed: (i) ability of weak lipophilic acids (e.g., lactic acid) to pass across the cell membrane in Available as dry powder, mono- or pentahydrate. their undissociated form, dissociate within the cell and acidify the cell interior (22,29,47); and (ii) specific ability Used for calcium supplementation. ) of sodium lactate to lower the water activity (aw (13,36). Firming agent and coloration inhibitor in apple slices. Lowering of intracellular pH Prevents ropiness (0.2%) and coliform (0.3%) in bread dough and In regard to entry of the acid into the cell membrane, other baked products. the lipophilic acid molecules are able to diffuse freely across the cell membrane in their protonated form (25). Cattle feed additive to regulate the microflora (I % in silage liquor). Energy-linked carriers and the membrane potential may also be involved in the uptake (33). If the extracellular pH Used in gel production from demethylated pectins. is lower than the intracellular pH, the acid dissociates and releases protons that acidify the cytoplasm. The cell reacts Improves quality of dried milk powder. generally to maintain a constant internal pH by removing

JOURNAL OF FOOD PROTECTION, VOL. 57, MAY 1994 TABLE 4. Recent reported antimicrobial effects of lactates in meat products.

Product Storage Sodium Effect d, °C lactate, %

Vacuum packed pork liver pate 42,6 2 Inhibition of aerobes and anaerobes (13) Comminuted cooked turkey, vacuum packed 10,27 3-3.5 Delayed toxigenesis in proteolytic C. botulinum (7-8 d) (37) Fresh pork sausage 45, 5 3 Reduced aerobes; 2 wk extended shelf-life (35) Frankfurters 56,4 2-4 Inhibition of L. monocytogenes and aerobes (4%) (4) Cooked chicken roll (uncured) 49,4 2-4 Inhibition of L. monocytogenes and aerobes (4%) (4) Cooked, vacuum packed beef roasts 80,0 1-4 Reduced aerobes by 3-4% lactate (44) Fresh pork sausage 28,4 2-3 Delayed growth of aerobes (8) Low fat beef patties 12, 5-7 2-3" Reduced aerobes (17) Communited cooked beef, 55% m.c. 7,20 4 Inhibition of L. monocytogenes (9) Pork liver sausage, 2% NaCl 50,5 3b Inhibition of L. monocytogenes (59) Fresh pork sausage (40 and 8% fat) 12, 5-7 2" Reduced aerobes, psychrotrophs and colifonns (7) Cooked turkey and chicken roll (uncured) 80, 8-30 1.2-3 Delayed toxigenesis in non-proteolytic C. botulinum (38) Downloaded from http://meridian.allenpress.com/jfp/article-pdf/57/5/445/1664955/0362-028x-57_5_445.pdf by guest on 24 September 2021

" Potassium lactate. b Sodium, potassium or calcium lactate. the protons, and since much of the cell energy is expended Effect on water activity to maintain internal pH constant, growth rate is reduced There is some evidence that bacterial inhibition by (25). Interference with the proton gradient across the mem- salts of lactic acid may be associated with effects on water

)' brane further disrupts cell functions, such as amino acid activity (aw When we first investigated antilisterial effects transport (18,22). This mechanism is supported by observa- of sodium lactate, initial tests were conducted in broth (50). tions of increased antimicrobial activity at reduced pH than Results in the liquid medium showed that only at high at near-neutral values and of organic acids (considered concentrations of sodium lactate, exceeding 5%, was growth nonelectrolytes because of their relatively low ionization suppressed. Although on an equal concentration basis anti- constants) being more effective inhibitors than inorganic microbial agents have been generally less effective in food acids (12,21,30,54). than in broth, we found that lower listeriostatic lactate There are indications that lactic acid does not act on concentrations were required in cooked meat and poultry the microbial cell in the same manner as do other fermen- than in broth, and they decreased as moisture, aw values, tation acids such as acetic and propionic, and does not and temperature were reduced (9,50). Other studies using behave as predicted on the basis of dissociation constants broth as the growth medium also confirmed limited or no (40). Although L. monocytogenes is sensitive to lactic acid microbial inhibition by lactate (e.g., 41), whereas addition and its salts, studies on changes in intracellular pH of the to meat products generally demonstrated antimicrobial ef- organism in the presence of lactic and other weak organic fects, as evident from data in Table 4. acids showed that the cells maintained a pH gradient of The effects of lactates on water activity were studied in about 1.0 to 1.5 pH unit over a medium pH of 3.5 to 6.5. aqueous solutions and in meat products. Chirife and Ferro In response to extracellular lactic acid, the intracellular pH Fontan (11) studied the effect of sodium lactate in aqueous remained near 5.0 even when the external pH was reduced solutions and observed no exceptional aw lowering proper- to 3.5 (30). These observations and those of Young and ties. Indeed, they found that at equal concentrations lactate

' Foegeding (61) suggest that inhibition of L. monocytogenes was inferior to NaCI in lowering the aw in contrast to is not associated with decrease in intracellular pH. Salts of previous reports (36). De Wit and Rombouts (14) compared organic acids, such as sodium and potassium lactate, are growth of several spoilage and pathogenic organisms in fully dissociated in aqueous solutions, and at the pH of an broth in the presence of sodium lactate or NaCI at an equal unfermented meat product, which is typically 6.0-6.5, the water activity of 0.958. The sodium concentration in the concentration of the undissociated form of the added lactate media was also the same. With the exception· of a strain of is low (5,59) Escherichia coli, all test organisms displayed sensitivity to Growth inhibition of bacteria has been attributed to lactate but not to chloride. The authors concluded that the both the proton and the anion (19). Regarding lactate salts, antibacterial effect of sodium lactate could not be ascribed antibotulinal and antilisterial activities of the lactate anion to the water activity lowering effect (14). have been established in studies that compared activities of As to measurements in meat products, Hammer and the sodium and potassium salts (9,37). Studies with calcium Wirth (27) reported aw values in liver sausage mixes after lactate further supported the antimicrobial activity of the additions of I% of various sodium salts including: acetate, anion (59). Russell (46) suggested that anion accumulation ascorbate, chloride, citrate, diphosphate, glutamate and lac-

' is responsible for the toxic effect of fermentation acids at tate. Sodium chloride was most effective in reducing the aw low pH, but the relationship between ApH across the cell followed by lactate, which produced 66% of the reduction membrane, anion accumulation and acid toxicity has re- by the chloride. Measurements of changes in both bacterial ceived little attention. No studies appear to have been done growth and aw in meat products by the addition of sodium on the effect of the lactate anion at near neutral pH. lactate have been reported by a number of researchers. A

JOURNAL OF FOOD PROTECTION, VOL. 57, MAY 1994 summary of these data is presented in Table 5. Either containing lactate (mean aw = 0.954). If a critical aw is sodium lactate or a combination of sodium lactate and assumed to be the same in broth and in food, then the chloride were employed in these studies. The aw of the inhibition of listerial growth observed in lactate-treated lactate-free products ranged from 0.959 to 0.986 (mean aw meats at a higher aw can be attributed to an action of lactate

= 0.970). Although different products, microorganisms, that is unrelated to aw . The observations of listerial control levels of lactate and chloride, and methods for aw determi- at a higher aw than predicted support the efficacy of a nation were used, in each of the studies the level of lactate barrier system, whereby bacteriostatic effects in foods can

' that inhibited bacterial growth in meat also lowered the aw be attained at a higher aw by a combination of additives. even though the change was small. The critical range was Water activity has become a universally accepted,

0.945 to 0.965 (mean aw = 0.970) and the mean difference practical measurement to predict shelf-stability and micro- was 0.016 (Table 5). In our studies on effects of lactates on biological safety of foods, but questions and debates on its growth of L. monocytogenes in a meat model system value have been raised in recent years. Slade and Levine consisting of an additive-free comminuted beef, the addi- (52) proposed that polymeric solutes may produce more tion of 4% sodium lactate to meat with 55% moisture stable systems with greater microbiological stability than completely inhibited growth of strain Scott A when held at non polymeric small compounds such as sugars. Since lactic Downloaded from http://meridian.allenpress.com/jfp/article-pdf/57/5/445/1664955/0362-028x-57_5_445.pdf by guest on 24 September 2021

20°C for 7 days (9). Measurements of aw showed that NaCl acid undergoes self-esterification and polymerization in was more effective than sodium lactate in lowering the aw aqueous solutions (28; see also Table 1), such changes may of the meat (Table 6), in agreement with findings of Chirife have an effect on the availability of water for microbial and Ferro Fontan (11), but 4% NaCl alone did not inhibit growth. growth whereas 4% sodium lactate did. Resistance of L. monocytogenes to NaCl is well documented despite its Other effects aw lowering effect. It may be concluded from the data Other explanations have been proposed for the antimi- summarized in Tables 5 and 6 that although sodium lactate crobial effect of lactate. It was suggested that in the inhibi- lowers the aw in meat, the effect is small and insufficient to tion of C. botulinum high levels of lactate ions may shift fully explain the antimicrobial effects. the reduction of pyruvate to lactate closer to its thermody- The specific data on inhibition of L. monocytogenes by namic equilibrium and thereby inhibit a major anaerobic (37). lactate and the corresponding measured aw can be compared energy metabolism pathway essential for growth Still further to other published studies on effect of aw on growth another plausible explanation proposed by these authors for of the organism. Several factors affect the ability of the C. botulinum was that lactate efflux from the bacterial cell

' organism to survive at low aw including temperature, salt may be coupled to adenosine triphosphate (ATP) genera- combinations, and pH, as seen from the summary of the tion from proton transfer across cell membranes. This may studies (Table 7). For example, Miller (39) studied growth be inhibited by a high level of extracellular lactate, as and survival of L. monocytogenes Scott A in brain heart demonstrated in membrane vesicles from Streptococcus infusion (BHI) broth at various aw levels using either NaCl, faecalis (51). glycerol or propylene glycol as humectants. The corre- Hydroxycarboxylic acids (citric, lactic, malic and tar- sponding minimal aw levels for growth at 28°C were 0.92, taric) are known for their chelating properties. Together 0.90 and 0.97, respectively. Nolan et al. (43) used either with citrates, pyrophosphates and ethylenediaminetetraacetic NaCl, sucrose or glycerol in tryptic soy broth-yeast extract acid (EDT A), lactates are the most commonly used chela-

(TSB- YE) to determine minimal aw levels for growth dur- tors in foods (31). For example, the stability constant of Fe ing incubation at 21°C for up to 21 d. Minimal aw levels (III) for lactic acid is 6.4 (23). This value can not predict were 0.92, 0.92 and 0.90, respectively, and the presence of the formation efficiency of an iron-lactate complex in a 0.6% of yeast extract in TSB increased the tolerance of food system such as meat, which contains numerous inter- L. monocytogenes to all three humectants when compared fering constituents, and is lower than the value for citrate to TSB alone. Despite the variations in testing conditions (11.85). However, chelation of iron in meat may contribute

and humectants, the values for the minimum aw for growth to the antilisterial activity of lactate. This is supported by of listeriae with NaCl as humectant range from 0.90 to observation that lactate stabilizes fats and oils, probably by 0.94, with a mean (n = 5) of 0.922 (Table 7). Overall, these chelating trace amounts of iron (42). Moreover, we have values are lower than those reported in meat products observed enhanced antilisterial activity of lactates in meats

TABLE 5. Effects of sodium lactate on water activity and microbial growth in meat products.

Product Storage NaUNaCl Product Critical Organisms Reference dloC % aw aw (no lactate)

Pork liver pate 42/6 2/2 0.959 0.940 Total aero anaer. (13) Cooked ham 60/5 1/2.2 0.970 0.965 Total aerobes (57) Comminuted, cooked beef 7/20 4/0 0.986 0.964 L. monocytogenes (9) Pork liver sausage 50/5 4/2 0.965 0.955 L. monocytogenes (59) 2/4 0.945 3/3 0.951

JOURNAL OF FOOD PROTECTION, VOL. 57, MAY 1994 There is now sufficient evidence for antibacterial ef- Water acti vity (a )" w fects of the sodium, potassium and calcium salts of lactic Salt Salt concentration, % 2 3 4 acid in fresh and processed meat products. In addition to growth of aerobes and anaerobes that is controlled in the Sodium chloride 0.962 0.954 0.943 presence of lactates, at least two pathogens, C. botulinum Sodium lactate 0.972 0.968 0.964 (both proteolytic and non-proteolytic strains) and L monocytogenes, are also affected. Hence, there are benefits of " Adapted from (9). added safety for meat products containing lactates, particu- "a of control was 0.986. w larly during extended shelf-life at refrigeration tempera- tures. A number of explanations have been considered for the antimicrobial effect of the salts at neutral or near neutral pH, including acidification of the cell cytoplasm and low- TABLE 7. Minimal water activity levels for growth and survival ering of a . No one single reason appears satisfactory at this of L. monocytogenes in humectant-broth systems. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/57/5/445/1664955/0362-028x-57_5_445.pdf by guest on 24 September 2021 time in e~plaining the effects. Observation of more pro- Humectant Testing Minimum Reference nounced antibacterial effects in meats than in broth empha- conditions aw sizes the need for further studies of the activity of lactates in food systems. 16% NaCI I yr -0.90 (48) 10% NaCl -0.93 (6) REFERENCES 10.5% NaCI 15 d, 37°C <0.80 (49) 20-30% NaCI (49) 5 d, 37°C 1. Anders, R. J., J. G. Cervany and A. L. Milkowski. 1989. Method for 30.5% NaCI 100 d, 4°C (49) delaying Clostridium botulinum growth in fish and poultry. U.S. Pat. NaCI 20 d, 4°C 0.93 & 0.94" (55) 4,798,729 Jan. 17 and 4,888,191 Dec. 19. Sucrose 0.92 & 0.94" (55) 2. Angersbach, H. 1971. 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