Potential Benefits

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Most of the potential benefits to be discussed will focus on those applicable to human health or nutrition. A separate section addresses the issue of probiotics for livestock use.

  1. Control of Growth of Undesirable Organisms in the Intestinal Tract
  2. acidophilus, Lb. casei, and species of Bifidobacterium can inhibit growth of undesirable microorganisms that might be encountered in the gastrointestinal tract. Most of the older reports dealing with this type of control focused on a therapeutic approach; in that cultured products made with these organisms were used to treat infections of various types (Gordon et al., 1957; Winkelstein, 1955). Some studies involving these organisms were poorly done and improper controls were used, so it is difficult to draw definite conclusions concerning the benefit of probiotic organisms. The newer approach is to provide consumers with products containing the probiotic organisms for use as preventive treatment in controlling intestinal infections. Studies using chickens as animal models and in which the birds were dosed with specific intestinal pathogens following consumption of cells of Lb. acidophilus have shown that the lactobacilli do exert control over Salmonella infections (Watkins and Miller, 1983). Feeding lactobacilli to birds before challenge with pathogens followed by continued consumption of Lb. aci-dophilus after the challenge dose resulted in best control of pathogens, sug gesting that continuous consumption of the probiotic organism is desirable. Researchers conducting this study also showed that Lb. acidophilus was effective in controlling Escherichia coli in the intestinal tract of chickens (Watkins et al., 1982).

In recent years, several other studies have shown the efficacy of certain probiotic organisms in controlling growth of undesirable microorganisms in the intestinal tract. A product containing a selected culture of lactobacilli and developed and marketed in Argentina has been useful in controlling intestinal infections (Oliver et al., 1999). Consumption of milk fermented with Lb. casei significantly decreased the severity of diarrhea in children in day care centers in France (Pedone et al., 1999). Consumption of cells of Lb. acidophilus controlled small bowel overgrowth in patients with kidney failure (Simenhoff et al., 1996). Ingestion of cells of Bi. bifidum reduced shedding of rotavirus (Duffy et al., 1994). Selected strains of Lb. acidophilus excreted an antimicrobial substance active against Helicobacter pylori both in vivo and in vitro (Coconnier et al., 1998).

Just how the probiotic bacteria function in inhibiting growth of undesirable microorganisms in the intestinal tract is not clear. Many of the probiotic organisms produce substances that are inhibitory in vitro; however, it is difficult to confirm the activity of these compounds in vivo. The probiotic bacteria in question all produce large amounts of acid during their growth, because they rely on fermentation to obtain energy for growth. However, the antagonistic action that they produce toward undesirable microorganisms apparently is not caused just by acid produced during their growth. Several of these organisms produce antibiotic-like substances, some of which have been classified as bacteriocins, which may be involved in the antagonistic action toward these pathogens. Bacteriocins, according to the classic definition, are bacterial proteins active against organisms closely related to the producer organism (Tagg et al., 1976). This may limit the breadth of action of these inhibitory substances produced by probiotic bacteria. They would not be expected to have any effect on gram-negative intestinal pathogens. Furthermore, because of their sensitivity to proteolytic enzymes, bacterio-cins may not survive the digestive function of the intestines.

Antimicrobial substances, other than bacteriocins, produced by probiotic bacteria have been implicated in recent publications as having a possible role in controlling intestinal pathogens. A low molecular weight nonproteinaeous material produced by a Lactobacillus culture was active against a broad range of gram-negative and gram-positive bacteria (Silva et al, 1987). These researchers suggested the inhibitory agent to be a short-chain fatty acid other than lactic or acetic. Reuterin, an antimicrobial agent produced by Lb. reuterii, has a broad spectrum of activity. It has been characterized as a mixture of various forms of P-hydroxypropionaldehyde (Talarico and Dobrogosz, 1989). It also could be active in the control of pathogens.

Competitive exclusion by probiotic bacteria is another mechanism that has been suggested as being important in controlling intestinal infections (Watkins and Miller, 1983). Competitive exclusion involves the ability of lactobacilli or bifidobacteria to occupy binding sites on the intestinal wall, thereby preventing attachment and growth of enteric pathogens.

Definitive scientific data showing the mechanism of action whereby these probiotic bacteria may exert inhibitory actions toward pathogens in the intestinal tract would make it easier to select the most effective strains of probiotic bacteria for use in dairy products to help control intestinal infections in humans. Most likely the antagonistic actions produced by probiotic bacteria toward intestinal pathogens result from a combination of factors.

B. Improvement of Immune Response

Enhancement of the body's immune response by consuming cells of certain lactobacilli increases resistance of the host to intestinal infections (Lessard and Brisson, 1987; Perdigon et al., 1990a; Sato et al., 1988; Romond et al., 1997). Of the lactobacilli, Lb. casei seems to be the primary one involved (Perdigon et al., 1990B). Bi. longum also can stimulate the immune system to control E. coli in the gastrointestinal tract (Romond et al., 1997). As with other characteristics of the lactic acid bacteria, the relative ability of probiotic bacteria to cause such an effect probably varies tremendously among strains of individual species. Researchers in this area have suggested that this action involves activation of macrophages which in turn destroy pathogenic organisms in the body. It also has been suggested that consumption of these organisms is followed by secretion of components into the intestinal tract which are inhibitory toward certain of the foodborne pathogens. This enhancement of the immune system increases the host defense mechanisms and could be very important for control of foodborne illnesses. This may be a key explanation as to how certain probiotic microorganisms used as dietary adjuncts can exert control over intestinal infections.

C. Improvement of Lactose Digestion

People who lack the ability to digest lactose adequately are classified as lactose maldigestors. (In the past, terms such as ''lactose intolerance'' or ''lactose malabsorption'' have been used to describe this condition). The problem results from inadequate levels of P-galactosidase in the small intestine to hydrolyze ingested lactose adequately. Once a lactose maldigestor consumes sufficient lactose, it passes into the large intestine where it undergoes an uncontrolled fermentation that results in symptoms of cramps, flatulence, and diarrhea. These symptoms often follow consumption of milk by such individuals. Because lactose maldiges-

tion results from inadequate levels of an enzyme to hydrolyze lactose in the small intestine, the possibility exists for providing such an enzyme via the diet. Inclusion of a purified enzyme such as P-galactosidase in the diet is rather expensive and survival of the enzyme during passage through the stomach likely would be minimal. Research has shown that the presence of viable starter cultures in yogurt can be beneficial to lactose maldigestors (Gilliland and Kim, 1984; Kolars et al., 1984). This beneficial action results from presence of P-galactosidase in the bacterial cells. Apparently being inside the bacterial cells protects the enzyme during passage through the stomach so that it is present and active when yogurt reaches the small intestine. Once the yogurt culture reaches the small intestine, it interacts with bile, which increases permeability of the cells of these bacteria and enables the substrate to enter and be hydrolyzed (Noh and Gilliland, 1992). The enzyme remains inside the cell upon exposure to bile rather than leaking out into the surrounding medium. As mentioned previously, the starter cultures used for yogurt manufacture (Lb. delbrueckii subsp. bulgaricus and S. thermophilus) are not bile resistant and thus are not expected to survive and grow in the intestinal tract. Despite this limitation, consumption of these bacteria provides a means of transferring P-galactosidase into the small intestine where it can improve lactose utilization in lactose maldigestors.

Nonfermented milk containing cells of Lb. acidophilus also can be beneficial for lactose maldigestors (Kim and Gilliland, 1983). This organism, unlike the yogurt starter cultures, can survive and grow in the intestinal tract. However, a similar mechanism in improving lactose utilization in lactose maldigestors to that observed for yogurt bacteria is probably involved. P-Galactosidase activity of cells of Lb. acidophilus is greatly increased in the presence of bile because of increased cellular permeability (Noh and Gilliland, 1993). As with yogurt cultures, cells of Lb. acidophilus do not lyse in the presence of bile, but their permeability is increased permitting lactose to enter the cells and be hydrolyzed. Because Lb. acidophilus can survive and grow in the intestinal tract, it is reasonable to expect, however, that additional P-galactosidase may be formed after ingestion of milk containing this organism.

There has been some controversy over whether or not acidophilus milk is effective in improving lactose utilization by lactose maldigestors; however, if the cells contain sufficient levels of P-galactosidase before ingestion, it is reasonable to assume they will provide such a benefit. Results of studies that have suggested milk containing Lb. acidophilus is ineffective (Payne et al., 1981; Saviano et al., 1984) in improving lactose digestion might be questioned, because no evidence was provided concerning cultures used or the procedure by which they were produced. In those studies, it is possible, that insufficient P-galactosidase was present in milk containing cells of Lb. acidophilus at the time of consumption. One of the studies (Saviano et al., 1984) indicated that no P-galactosidase activity was detected in milk containing Lb. acidophilus.

Based on the proposed mechanism for improving lactose digestion by yogurt cultures, it seems reasonable that consumption of any product containing bacterial cells having adequate intracellular P-galactosidase activity could provide a benefit such as improving lactose utilization. Because this enzyme usually is inducible in most microorganisms, it is important that before ingestion the organism be grown in a medium containing lactose. This becomes particularly important when cells of probiotic bacteria grown in some medium other than milk are added to nonfermented milk. The level of P-galactosidase activity also varies among strains of Lb. acidophilus as well as among commercial yogurt cultures. Therefore, it is important to consider the level of P-galactosidase activity in probiotic or starter cultures to be used for improving lactose digestion in lactose maldigestors. It also is important for the activity to remain high during transportation and storage of such products so that the consumer receives the product containing enough of the enzyme to provide a benefit.

D. Anticarcinogenic Actions

Anticarcinogenic or antimutagenic activities have been reported for several cultures used to manufacture various fermented milk products (Goldin and Gorbach, 1984; Oda et al., 1983; Reddy et al., 1983; Shahani et al., 1983). Some of these studies have involved products containing probiotic bacteria expected to survive and grow in the intestinal tract, whereas others have involved only bacteria used to manufacture the product and which are not normally expected to survive and grow in the intestinal tract. For instance, consumption of yogurt by mice inhibited development of certain tumors (Reddy et al., 1983). This represents another potential health benefit for a cultured product without necessarily involving one of the traditional probiotic bacteria. In other studies involving human subjects, a culture of lactobacilli exhibited potential in controlling cancer of the colon (Goldin and Gorbach, 1984). The lactobacillus used in this study was later identified as Lb. casei.

  1. acidophilus, Lb. casei, and Lb. delbrueckii subsp. bulgaricus are species most often mentioned as having potential to provide anticarcinogenic actions. For Lb. delbrueckii subsp. bulgaricus, which is not normally considered a probi-otic organism, the anticarcinogenic action apparently is associated with substances produced by the organism during manufacture of yogurt as opposed to being produced in the body following consumption of yogurt. However, for Lb. acidophilus and Lb. casei growth or action in the gastrointestinal tract seems to be important. Part of the benefit may involve direct effects in inhibiting tumor formation. However, the main effect may result indirectly through inhibiting growth of undesirable bacteria that form carcinogens in the large intestine (Goldin and Gorbach, 1984). Thus, this may represent another benefit in being able to control growth of undesirable organisms in the gastrointestinal tract.
  2. Control of Serum Cholesterol

In the 1970s, two studies were published that suggested organisms such as Lb. acidophilus can potentially reduce serum cholesterol levels in humans. One of these studies involved milk fermented with what was described as a ''wild'' strain of lactobacillus and then fed to a group of men on a high-cholesterol diet (Mann and Spoerry, 1974). The study was designed to evaluate the influence of a surfactant (Tween 20) on serum cholesterol levels. The researchers theorized that the surfactant would increase absorption of cholesterol from the intestine and thus increase serum cholesterol levels. However, the serum cholesterol level in both groups of men, that is, those receiving the surfactant and those who did not, decreased! This was one of the first studies that suggested consumption of a fermented dairy product could reduce serum cholesterol levels in humans. However, neither the organism involved in the fermentation nor the mechanism was identified. In another study, cells of Lb. acidophilus added to infant formula reduced serum cholesterol in infants receiving the formula (Harrison and Peat, 1975), whereas infants receiving the formula without cells of Lb. acidophilus exhibited increased serum cholesterol levels. The researchers concluded that Lb. acidophilus, through its growth in the intestine, in some way influenced the serum cholesterol level, although no mechanism was suggested.

Several studies have shown that animals consuming milk containing cells of Lb. acidophilus had lower serum cholesterol levels than did animals that did not receive milk containing the lactobacilli (Danielson et al., 1989; Gilliland et al., 1985; Grunewald, 1982). Some strains of Lb. acidophilus can actively assimilate or take up cholesterol during growth in laboratory media (Gilliland et al., 1985; Gopal et al., 1996). This occurs when the organisms are grown anaerobi-cally in the presence of bile. A portion of the cholesterol is incorporated into the cellular membrane of Lb. acidophilus (Noh et al., 1997). There is variation among strains of this organism in their ability to exert control over serum cholesterol levels (Gilliland et al., 1985). Pigs on a high-cholesterol diet fed a strain of Lb. acidophilus that actively assimilated cholesterol during growth in laboratory media had significantly lower serum cholesterol levels than did pigs receiving a strain of Lb. acidophilus that did not actively assimilate cholesterol in laboratory media (Gilliland et al., 1985). This suggests the ability to assimilate cholesterol in laboratory media provides an indication of the potential of this organism, if consumed, to exert some control over serum cholesterol levels. Similar findings were noted when a mixture of Lb. johnsonii and Lb. reuteri was fed to pigs (du Toit et al., 1998).

Another activity of Lb. acidophilus that may be important is its ability to deconjugate bile acids. This provides yet another mechanism whereby ingested Lb. acidophilus might exert control of serum cholesterol levels. Deconjugation of bile acids by lactobacilli can occur in the small intestine. Lb. acidophilus more actively deconjugates glycocholic acid than it does taurocholic acid (Corzo and Gilliland, 1999). This becomes significant because the dominant conjugated bile acid in the human intestine is glycocholic acid. Free bile acids are less well absorbed in the small intestine than are conjugated bile acids and thus more are excreted through feces (Chickai et al., 1987). Excretion of bile acids through feces represents one of the major mechanisms whereby the body eliminates cholesterol. This is because cholesterol is a precursor for synthesis of bile acids and many bile acids that are excreted from the body are replaced by synthesis of new ones. Thus, there is a potential for reducing the cholesterol pool in the body. Furthermore, free bile acids do not support absorption of cholesterol from the intestinal tract as well as do conjugated ones (Eyssen, 1973). Thus, deconjugation of bile acids in the intestinal tract may reduce the efficiency by which cholesterol is absorbed from the intestinal tract.

Research into the potential of Lb. acidophilus to exert hypocholesterolemic effects in humans has indicated tremendous variation among strains of Lb. acido-philus isolated from the human intestinal tract in their ability to assimilate cholesterol (Buck and Gilliland, 1994). Evaluation of strains of Lb. acidophilus used commercially in cultured or culture-containing dairy products in the United States has revealed that none is particularly active in assimilating cholesterol from laboratory media (Gilliland and Walker, 1990). On the other hand, new strains that are very active in this regard have been isolated from the human intestinal tract, and thus they may provide greater potential for use as dietary adjuncts to assist in controlling serum cholesterol levels (Buck and Gilliland, 1994). Of 122 isolates of Lb. acidophilus obtained from human intestinal sources, several were identified as having great potential for exerting control over serum cholesterol levels, because they were very active in assimilating cholesterol during growth in a laboratory medium. They were far more active in this regard than were the currently commercially available strains of Lb. acidophilus. One of these strains is presently used in the Netherlands to produce a fermented yogurt product named Fysiq which is promoted as being useful in helping maintain a healthy cholesterol level. This strain of Lb. acidophilus has been used in a human feeding trial of hypercho-lesterolemic individuals and caused a significant reduction in serum cholesterol levels (Anderson and Gilliland, 1999).

There may be other probiotic organisms that can help to control serum cholesterol levels. Some of these include Lb. casei (Brashears et al., 1998) and Bifidobacterium species (Gopal et al., 1996). Bi. longum removes cholesterol from laboratory media much the same as does Lb. acidophilus and incorporates part of it into the cellular membrane of this bacterium (Dambekodi and Gilliland, 1998). Lb. casei also can remove cholesterol from laboratory growth media. However, no evidence was found for association of cholesterol with the cellular membrane of this bacterium (Brashears et al., 1998). Both these organisms also can deconjugate bile acids. Currently there is great interest throughout the world in the potential of these bacteria to exert some control over serum cholesterol levels in hypercholesterolemic individuals.

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