Beruflich Dokumente
Kultur Dokumente
S. C. Ricke1
Department of Poultry Science, Texas A&M University, College Station, Texas 77843-2472
ABSTRACT Organic acids have a long history of being Although this situation has implications regarding the
utilized as food additives and preservatives for pre- use of organic acids, it may only apply to circumstances
venting food deterioration and extending the shelf life of in which reduced acid levels have induced resistance and
perishable food ingredients. Specific organic acids have virulence mechanisms in exposed organisms. Evaluating
also been used to control microbial contamination and effectiveness of organic acids for specific applications re-
dissemination of foodborne pathogens in preharvest and quires more understanding general and specific stress
postharvest food production and processing. The antibac-
response capabilities of foodborne pathogens. Develop-
terial mechanism(s) for organic acids are not fully under-
632
SYMPOSIUM: USE OF ANTIMICROBIALS IN PRODUCTION 633
weak or carboxylic acids Cherrington et al., 1991). Several acids serve as uncouplers that generally dissipate pH
of these organic acid compounds are used as direct addi- and electrical gradients across cell membranes (Sheu and
tives incorporated into human foods or can accumulate Freese, 1972; Sheu et al., 1972, 1975; Freese et al., 1973;
over time as a consequence of the fermentation activity Salmond et al., 1984; Russell, 1992; Axe and Bailey, 1995;
of indigenous or starter cultures added to certain dairy, Davidson, 2001).
vegetable, and meat products. In addition, acid sprays Russell (1992) has hypothesized that anion accumula-
have been incorporated as sanitizers during meat pro- tion is the primary toxic effect of organic acids and that
cessing (Acuff et al., 1987; Cherrington et al., 1991; Dick- some organisms are more resistant to organic acids be-
son, 1992; Hardin et al., 1995; Dorsa, 1997). Some organic cause they are capable of allowing their internal pH to
acids, particularly the short-chain fatty acids (SCFA), ace- decline. Less direct antibacterial activities have also been
tate, propionate, and butyrate, are produced in millimolar attributed to organic acids and include interference with
quantities in the gastrointestinal tracts of food animals nutrient transport, cytoplasmic membrane damage re-
and humans and characteristically occur in high concen- sulting in leakage, disruption of outer membrane perme-
trations in regions where strictly anaerobic microflora are ability, and influencing macromolecular synthesis (Cher-
predominant. In the food animal industry, organic acids rington et al., 1991; Denyer and Stewart, 1998; Alakomi
were originally added to animal feeds to serve as fungi- et al., 2000; Davidson, 2001).
stats (Paster, 1979; Dixon and Hamilton, 1981), but in The mechanisms associated with these activities have
In general, potential bacterial targets of biocidal com- Factors that Influence Toxicity
pounds include the cell wall, cytoplasmic membrane, and Efficacy of Organic Acids
specific metabolic functions in the cytoplasm associated
with replication, protein synthesis, and function (Denyer The significant affects and the toxicity of organic acids
and Stewart, 1998; Davidson, 2001). Although the antibac- (either directly or indirectly) for foodborne pathogens
terial mechanism(s) for organic acids are not fully under- have not been clearly elucidated. This is in part due to
stood, they are capable of exhibiting bacteriostatic and complexities involved in designing and conducting the
bactericidal properties depending on the physiological experiments that precisely delineate all of the contribut-
status of the organism and the physicochemical character- ing factors. Direct assessment and comparison of antibac-
istics of the external environment. Given the weak acid terial potency of individual acids can be elusive because
nature of most of these compounds, pH is considered a of the influence of the physical chemistry of respective
primary determinant of effectiveness because it affects the acids, the bacterial species in question, growth conditions
concentration of undissociated acid formed (Davidson, or media composition, and the growth phase (Cherring-
2001). It has been traditionally assumed that undissoci- ton et al., 1991; Lasko et al., 2000). In addition, specific
ated forms of organic acids can easily penetrate the lipid quantitative in vitro responses do not necessarily translate
membrane of the bacterial cell and once internalized into to all in vivo possibilities for a particular organism. This
the neutral pH of the cell cytoplasm dissociate into anions is partially due to the fact that many of the common
and protons (Eklund, 1983, 1985; Salmond et al., 1984; foodborne pathogens such as Salmonella spp. can grow
Cherrington et al., 1990, 1991; Davidson, 2001). Genera- in a multitude of ecosystems and, thus, in vivo growth
tion of both of these species potentially presents problems conditions when exposure to organic acids occurs can
for bacteria that must maintain a near neutral pH cyto- vary widely. It is entirely possible that during a life cycle,
plasm to sustain functional macromolecules. Export of Salmonella can grow aerobically and within a short time
excess protons requires consumption of cellular adeno- frame be forced to switch to an anaerobic metabolism to
sine triphosphate (ATP) and may result in depletion of survive and potentially colonize a highly fermentative
cellular energy (Davidson, 2001). environment such as the gastrointestinal tract. Under
Other toxicity mechanisms have been proposed that these conditions not only would Salmonella be required to
attribute membrane uncoupling capabilities for organic survive high concentrations of SCFA produced by other
acids. It has been speculated that organic acids interfere organisms, but it would also be generating and exporting
with cytoplasmic membrane structure and membrane fermentation organic acids of its own. Distinguishing spe-
proteins such that electron transport is uncoupled and cific organic acid toxic mechanisms in foodborne patho-
subsequent ATP production is reduced or that organic gens will continue to be difficult to achieve until genetic
634 RICKE
techniques can be applied to screen for differential physi- acids simply disappear in the gastrointestinal tract before
ological responses in selected mutants exposed to the reaching locations inhabited by pathogens. Using radio-
multitude of potential environmental backgrounds. actively labeled propionate, Hume et al. (1993b) demon-
Efficacy of organic acids can also be highly influenced strated that most of the propionic acid originating from
by extrinsic factors associated with the environment that the treated feed is metabolized and absorbed in the fore-
they are being added to. An example of this complexity gut of the chicken (crop, gizzard, and proventriculus) and
is the use of propionic acid and its salt forms in animal does not reach the small and intestine or the cecum in
and poultry feeds as an anti-Salmonella and antifungal sufficient quantities to be effective.
compound. It has been suggested that the presence of
propionate in feeds limits Salmonella and fungal contami- Bacterial Mechanisms of Resistance to
nation in the ingredients added to feed and mixed feeds Antibacterial Activities of Organic Acids
during storage. However, several factors can alter the
effective concentration in the feed. Inconsistent antimicro- In addition to the environmental factors that can influ-
bial effects of propionic acid on fungal populations in ence the efficacy of organic acids as antimicrobial chemi-
feed has been attributed to possible buffering and conver- cals, inherent resistance of the target microorganism to
sion to its less active form by protein ingredients such as these compounds is also a factor (Davidson, 2001). Micro-
soybean meal as well as batch differences in primary feed bial sensitivity to antimicrobial agents determines relative
organism and is essentially the degree to which organism enhance identification of signals for stimulation of viru-
can cause harm to its host. Microbial virulence phenotype lence in the pathogen of interest and provide specific
is defined as the ability of the respective pathogen to targets for development of more optimal strategies to
successfully infect the host and includes bacterial cell control this foodborne pathogen.
functions such as adherence to host tissue and invasion
into host cells (Mekalanos, 1992). It was originally sug- Conclusions
gested that because ingested foodborne pathogens come
in contact with low stomach pH, enhanced acid tolerance An obvious prerequisite for successful efforts to mini-
could increase the survivability after entry in the stomach mize the impact of antibiotic resistance in the animal
as well in vesicles of phagosomes after undergoing acidi- industry is development and implementation of alterna-
fication (Foster, 1992). In support of this concept, studies tive antimicrobials. Organic acids have a long history of
in which acid-sensitive mutants of pathogens have been use in the food industry as food preservatives and have
examined indicate that these mutants are also avirulent been demonstrated to be effective under a wide variety
(Lee et al., 1995; Wilmes-Riesenberg et al., 1997). Likewise, of food processing conditions. Although there is indica-
S. enteritidis isolates with enhanced acid tolerance were tion that some tolerance by foodborne pathogens is possi-
demonstrated to be more virulent in mice and more inva- ble, this tolerance may only be for particular circum-
sive in chickens (Humphrey et al., 1996). stances in which exposure to the organic acid is less than
maximum and provides the organism an opportunity to