Clinical Microbiology Newsletter

Vol. 30, No. 4

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February 15, 2008

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Lactobacillus: a Review
Christine M. Slover, Pharm.D., Manager, Medical Information, Critical Care, Infectious Diseases, Astellas Pharma US, Inc., Deerfield, Illinois, and Larry Danziger, Pharm.D., Professor of Pharmacy, Associate Vice Chancellor for Research, University of Illinois at Chicago, Chicago, Illinois

Abstract
Lactobacilli colonize the gastrointestinal and urinary tracts of humans, making them an integral part of the microbial flora. However, in certain circumstances, they can cause disease. Although lactobacilli are often misidentified as streptococci, it is highly likely that these infections will be attributed to them due to current improvements in laboratory techniques. A recent resurgence in interesting natural products has caused an increased focus on the use of probiotics. Many of these probiotic formulations contain Lactobacillus species. Although there have been reports of lactobacilli providing benefit in infectious diarrhea, the use of these probiotic products in immunosuppressed or critically ill patients is not advised, since these populations are at increased risk of developing infections due to lactobacilli.

Introduction
Lactobacilli are non-spore-forming, gram-positive rods that are an important part of the normal human bacterial flora commonly found in the mouth, gastrointestinal (GI) tract and female genitourinary tract (1-3). Microscopically, these bacteria appear as non-motile, thin rods varying in length from long to short. They can also appear as coryneform with a bent morphology or tend to grow in chains. Most species of lactobacilli are facultative anaerobes growing in either the presence or absence of an anaerobic environment. Only about 20% of species isolated from humans are obligate anaerobes. Lactobacilli tend to grow well on blood agar (4). Some, but not all, species will also grow on Lactobacillus selective medium. Lactic acid is the major metabolic end product of lactobacilli during glucose fermentation

(2,3). Acetic and succinic acids are also produced, but only in small amounts. The GI tracts of various mammals are commonly colonized with Lactobacillus spp. (2,3). The most common species of lactobacilli isolated from GI tracts are Lactobacillus brevis, L. casei, L. acidophilus, L. plantarum, L. fermentum, and L. salivarius. Lactobacilli have also been isolated from tooth plaque, saliva, and the vaginal tracts of humans and other mammals. Lactobacilli are a rather diverse group of bacteria, as is illustrated by their large GC content, which ranges from 32 to 53 mol% (3). To date, greater than 70 different species of Lactobacillus have been identified; of these, only 34 have been identified to the species level (2,3).

and other metabolites. The clinical significance of isolating Lactobacillus from a normally sterile site is the subject of debate. When isolated by the microbiology laboratory, some individuals believe that lactobacilli should be considered contaminants (7). Lactobacilli may go undetected in the laboratory because their growth requires special media and extended incubation time. Even after recovery, misidentification can occur because morphologically they resemble other genera, including Corynebacterum, Clostridium, and Streptococcus (5,8). Although lactobacilli are considered protective organisms, they have been increasingly implicated as pathogens, especially in the immunocompromised patient (5,9-11). Numerous reports have

Pathogenesis and Clinical Significance

Lactobacilli are required to maintain a healthy GI tract and are not usually considered to be pathogens in the healthy host except when associated with dental caries (5,6). They are considered protective organisms and are thought to inhibit the growth of pathogenic organisms via the production of lactic acid
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Mailing Address: Christine M. Slover, Pharm.D., Manager, Medical Information, Critical Care, Infectious Diseases, Astellas Pharma US, Inc., Three Parkway North, Deerfield, IL 60015. Tel.: 847-317-5028. Fax: 847-317-8229. Cell: 312-718-5334. E-mail: christine.slover@us.astellas.com

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been published of patients with AIDS or neutropenia, or following organ transplantation, with infections caused by Lactobacillus spp. (9-11). Among the more common clinical infections reported to be caused by lactobacilli are endocarditis, bacteremia, neonatal meningitis, dental caries, abscesses, and chorioamnionitis (1,5,12). The three most common infections caused by lactobacilli are endocarditis, bacteremia, and localized infections, such as abscesses.

Endocarditis
Infective endocarditis (IE) with or without associated bacteremia is the most common infection caused by lactobacilli reported in the literature (1,6,12-14). Many of the patients who develop Lactobacillus IE have recent histories of dental procedures or poor dentition, suggesting that this could be considered a risk factor, especially in those patients with underlying immunosuppression (1,12,15). Patients who develop IE also are also likely to have underlying valvular heart disease (7,15). The Lactobacillus species L. rhamnosus and L. casei have been the most frequently reported causes of IE (1,12,14). The ability of these two species of lactobacilli to cause IE is thought to occur, in part, as a result of their ability to induce platelet aggregation and generate fibrin, resulting in clot formation (12,14,16). These characteristics may allow the bacteria to colonize thrombotic vegetations, permitting the lactobacilli to grow and evade host defenses (14). Oakey et al. (14) reported that a factor Xa-like enzyme was produced by L. casei and L. rhamnosus. Factor Xa catalyzes steps in the coagulation cascade leading to the production of fibrin. Numerous antibiotic treatment regimens for endocarditis have been used. Most patients receive penicillin with or

without an aminoglycoside (1,13,15,17). These two regimens have been shown to be moderately successful in treating most cases of IE, but there are still a number of treatment failures. These disappointing results in the treatment of IE may be due to the ability of lactobacilli to lower the pH of their environment via lactic acid production. Kim et al. (17a) found that the autolytic enzyme, which is essential for the bactericidal effect of the -lactam antibiotics, is less active at a lower pH. Sussman et al. (15) have suggested that the large quantities of lactic acid produced by lactobacilli may hinder the activity of the aminoglycoside antbiotics. This problem with loss of aminoglycoside activity at lower pH levels has been well described in the literature in other infections caused by other bacteria. Monotherapy with vancomycin or clindamycin has also been used for treatment of patients with IE (1,7,15,17). When either of these antibiotics was used, patient outcomes have varied. Overall, there tends to be decreased susceptibility to vancomycin for Lactobacillus spp. L. acidophilus and L. delbrueckii seem to be the most susceptible to vancomycin; however, these species are the least likely to cause IE (1,18). Griffiths et al. (17) reported in vitro synergy with daptomycin and an aminoglycoside against clinical isolates of L. acidophilus and L. rhamnosus. This strategy may be a potential treatment option for patients with a penicillin allergy or when the organism is vancomycin resistant. Ciprofloxacin and other fluoroquinolones may also be considered treatment options. In a retrospective review conducted by Cannon et al. (1), Lactobacillus spp. were reported to be just over 60% susceptible to ciprofloxacin. However, the newer fluoroquinolones,

such as moxifloxacin and gatifloxacin, have better gram-positive coverage and may potentially be better choices for endocarditis treatment than ciprofloxacin. The mean duration of treatment in patients with endocarditis has been reported to be about 49 days (1). Even though there are multiple treatment options for Lactobacillus endocarditis, Cannon et al. (1) reported a mortality of >20% in 61 patients with IE. Significant morbidity is also frequently reported in patients with endocarditis. Patient outcomes have included valve replacement, embolisms, and a high risk of IE relapse (1,7,15).

Bacteremia
Lactobacillus bacteremia has a wide array of clinical presentations; patients can have severe sepsis or be asymptomatic (10, 5,17,19-21). Fever is the most common symptom in most patients, followed by leukocytosis and rigors (7). Secondary lactobacillemias have been reported in patients who have abscesses, endocarditis, and pneumonia (10,15,17, 19-22). Lactobacillus bacteremias are believed to occur due to translocation of bacteria across the intestinal mucosa (11,23). Lactobacilli have been found to be among the most frequently translocating bacteria of the indigenous microflora (23). When bacteria translocate across the mucosa, they are typically destroyed by the host immune system (24). This again explains why immunosuppression is the primary risk factor for disease (7,21). Recent surgeries, particularly abdominal procedures, have also been implicated as causes of bacteremia (7,21). Recent antibiotic treatment and prolonged hospitalization have also been reported as risk factors (19,21). The treatment of bacteremia is similar to that for IE; the use of -lactams with or without aminoglycosides is the

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most common therapy (1). The next most commonly reported antibiotic therapeutic regimen is combined therapy using a cephalosporin with vancomycin. In a recent review of the literature, Cannon et al. (1) reported a mean duration of treatment in patients with bacteremia of approximately 14 days. Mortality attributed to lactobacillemia has been reported to be relatively low (1,7,19,21,25). In a review of 45 cases of Lactobacillus bacteremia over a 15year period at a hospital in the United States, only one patient death could be attributed to lactobacillemia infection (7). In many instances, patients will have polymicrobial bacteremias, thus making it difficult to truly discern if infection caused by Lactobacillus spp. was the specific cause of death (19,26).

Localized Infections
Localized infections due to Lactobacillus spp. are also increasingly reported. Abdominal abscesses, pneumonia, other pulmonary infections, and peritonitis are the most commonly described in the literature (1). Once again, underlying immunosuppression is the major risk factor in these infections (5). Other risk factors are diabetes and renal failure (1). Treatment strategies for localized infections differ from those for IE and bacteremia, with most clinical isolates showing susceptibility to erythromycin and the fluoroquinolones (1). Monotherapy was employed most often in localized infection cases. High levels of resistance have been reported to lactam antibiotics and vancomycin in these types of infections. Cannon et al. (1) reported that half of the patients with Lactobacillus sp. abscesses also underwent surgical drainage as part of their treatment. Mortality is low for localized infections, with over 70% of patients making full recoveries.

Probiotics
Due to a resurgence of interest in all-natural products to treat illness, Lactobacillus sp. supplemented products have gained popularity. These products are collectively termed probiotics. A probiotic is defined as a dietary supplement consisting of living microorganisms that are found in normal flora and have little, if any, pathogenicity (27,28). When used, these products are believed to have positive benefits
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for health by preventing or treating disease. Probiotics have been used in a wide variety of gastrointestinal illnesses, including infectious diarrhea, irritable bowel syndrome, and inflammatory bowel disease. A number of mechanisms have been proposed to explain how probiotics exert their effects. Acetic, propionic, and lactic acids produced by lactobacilli may reduce intestinal pH, thereby potentially inhibiting the growth of pathogenic bacteria. However, the exact mechanism by which lactobacilli may exert such beneficial effects remains unknown. In the last few years, the efficacy of Lactobacillus sp. probiotics have been extensively studied. Clinical trials comparing Lactobacillus probiotics to placebo or standard treatment options have been done for numerous gastrointestinal disorders, attempts at cholesterol management, and bacterial vaginoses, and even to attempt immunomodulation. A meta-analysis of published studies evaluating the efficacies of probiotics (including an L. acidophilus mixture) in preventing travelers diarrhea found the pooled risk estimate to be 85%, showing them to be effective and safe for use (29). However, a recently published double-blind, randomized trial using L. acidophilus for prevention of travelers diarrhea found the probiotic to be ineffective (30). Comparable numbers of cases of diarrhea were reported in the two groups: 86.6 versus 63.9 cases per 100 person-months (L. acidophilus versus placebo, respectively; P = 0.29). A randomized clinical trial conducted in adult patients with chronic diverticular disease of the colon, currently in remission, found that those patients treated with a combination of mesalazine and L. casei DG had significant improvements in their symptoms at follow-up and more of these patients remained in remission compared to patients treated with either mesalazine or the probiotic alone (31). Research has also been conducted in pediatric patients using probiotics for the treatment and prevention of a variety of GI disorders. Several studies (32-35) have reported success in treating irritable bowel syndrome in school age children, preventing diarrhea secondary to antibiotic treatment for respiratory infections, decreasing colic symptoms in infants, and decreasing the duration of
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acute diarrhea in young children living in Thailand. Since lactobacilli are common flora of the urogenital tract, several studies have been conducted to evaluate the efficacies of probiotics in treating various conditions of the urogenital tract in women. A recent study conducted in Nigerian women found that two capsules containing L. rhamnosus GR-1 and L. reuteri RC-14 inserted intravaginally at bedtime for 5 days were more successful in treating bacterial vaginosis than 5 days of 0.75% metronidazole gel inserted vaginally twice daily (30% versus 75% positive for bacterial vaginosis on day 6; P = 0.016) (36). However, a randomized trial conducted in women being treated with antibiotics for non-gynecological infections found that post-antibiotic vulvovaginal candidiasis was not prevented by administering oral and/or vaginal probiotic treatments containing L. rhamnosus (37). Even for these two conditions, bacterial vaginosis and vulvovaginal candidiasis, the reports of probiotic efficacy in the literature vary (38,39). In 2006, the American Society for Microbiology released a report on probiotic use (40). The society recommended that carefully designed, randomized, placebo-controlled clinical trials be conducted and also that in vitro studies and in vivo models be standardized to better study the effects of probiotics. The report also detailed the need for affirming the potency and purity of probiotic products prior to human consumption. With renewed interest in probiotics and some clinical studies showing benefits of their use, this area of research is likely to increase over the next decade.

Antimicrobial Properties
As typical flora in the GI and urogenital tracts, lactobacilli have been shown to prevent pathogenic bacteria from causing infection. These bacteria exhibit several properties that make them useful for preventing infectious disease. One such property is the production of low-molecular-weight antimicrobials, also known as bacteriocins (41). Bacteriocins are small proteins produced by bacteria that can have toxic effects on other bacteria (42,43). These proteins are usually active against identical or related species of bacteria
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and eradicate neighboring bacteria by attaching themselves to receptors on their surfaces. Lactobacilli also produce bacteriocinlike substances. These compounds are not as well defined chemically as bacteriocins, but they also control overgrowth of potentially pathogenic bacteria (44). Bacteriocin-like substances tend to have broad spectra of action and inhibit both gram-positive and gram-negative bacteria, along with some fungi. McGroarty and Reid (45) described an antimicrobial compound produced by L. casei GR-1 that had activity against Escherichia coli. The discovery of these agents suggests that the presence of lactobacilli may prevent the overgrowth of various GI and urogenital bacteria, thus preventing infection. The presence of lactic acid and hydrogen peroxide, other byproducts of lactobacillus metabolism, have also been shown to be beneficial for controlling overgrowth of other, potentially pathogenic bacteria (42,46). When hydrogen peroxide-producing lactobacilli are absent from the vaginal tract of humans, there tends to be overgrowth of catalase-negative bacteria, which in turn causes bacterial vaginosis. Interestingly, it has been reported that hydrogen peroxide-producing Lactobacillus spp. were isolated in only 6% of women with the diagnosis of bacterial vaginosis compared to 96% of women without the disease (46). Antonio et al. (47) recently reported that women who were not colonized with these hydrogen peroxideproducing lactobacilli, either rectally or vaginally, were 15 times more likely to have bacterial vaginosis than women who were colonized. Lactic acid also inhibits the growth of pathogenic microorganisms. Young et al. (48) demonstrated in vitro inhibition of Candida albicans growth in a mixed culture with lactobacilli. This was attributed to a more acidic pH (pH 3.7 to 4.2) in the medium due to lactic acid production by lactobacilli. All of these characteristics make the lactobacilli key bacteria in the human bacterial flora for keeping other more pathogenic bacteria in check and not allowing them to cause infection.
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Food Industry
Lactobacilli and other lactic acidproducing bacteria are also important organisms used in industrial food production (49). They are used to ferment common foods, such as yogurt, cheese, pickles, sauerkraut, and sourdough bread (49,50). Fermentation produces lactic acid that causes a drop in pH. This drop in pH then inhibits the growth of putrefactive and pathogenic bacteria. In addition, these organisms also increase the nutritional value of fermented foods. This occurs because lactic acid-producing bacteria cause an increase in the production of essential amino acids and vitamins, along with an increased bioavailability of minerals. Over the last century, the food microbiology industry has extensively studied lactobacilli and deemed the bacteria safe for human consumption.
2.

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Summary
Lactobacilli are an important part of the human flora, but they can be pathogenic under certain conditions. The most common infections caused by lactobacilli are bacteremias, IE, and abscesses. These infections tend to occur in immunosuppressed patients or those patients with underlying anatomic defects. Given the difficulty in isolating these bacteria and the possibility that they may often be misidentified, with increasing improvements of our laboratory technology it is possible that lactobacilli will be implicated with greater frequency as causative organisms in infections. In recent years, there has been an increased focus on the use of probiotics, such as Lactobacillus spp. Various species of lactobacilli may provide benefit in certain infectious diarrheas or other illnesses. While the use of lactobacilli has few significant adverse effects in healthy people, they have been associated with some serious infections in critically ill or immunosuppresed patients (22,51). More research is needed to expand our basic understanding of the conditions under which lactobacilli cause infection, especially with the mounting interest in using Lactobacillus sp. products as natural forms of disease treatment.
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33:1433. 40. Walker, R., M. Buckley, and the American Academy of Microbiology. Probiotic microbes: the scientific basis. http://www.asm.org. Accessed: September 10, 2007. 41. Sablon, E., B. Contreras, and E. Vandamme. 2000. Antimicrobial peptides of lactic acid bacteria: mode of action, genetics and biosynthesis. Adv. Biochem. Eng. Biotechnol. 68:21-60. 42. Tagg, J.R., A.S. Dajani, and L.W. Wannamaker. 1976. Bacteriocins of gram-positive bacteria. Bacteriol. Rev. 40:722-756. 43. Reid, G. et al. 1990. Is there a role for lactobacilli in prevention of urogenital and intestinal infections? Clin. Microbiol. Rev. 3:335-344. 44. Boris, S. and C. Barbes. 2000. Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect. 2:543-546. 45. McGroarty, J.A. and G. Reid. 1988. Detection of lactobacillus substance that inhibits Escherichia coli. Can. J. Microbiol. 34:974-978. 46. Eschenbach, D.A. et al. 1989. Prevalence of hydrogen peroxide-producing Lactobacillus species in normal women and women with bacterial vaginosis. J. Clin. Microbiol. 27:251-256. 47. Antonio, M.A.D., L.K. Rabe, and S.L. Hillier. 2005. Colonization of the rectum by Lactobacillus species and decreased risk of bacterial vaginosis. J. Infect. Dis. 192:391-398. 48. Young, G., R.I. Krasner, and P.L. Yudkofsky. 1956. Interactions of oral strains of Candida albicans and lactobacilli. J. Bacteriol. 75:525-529. 49. Hammes, W.P. and P.S. Tichaczek. 1997. The potential of lactic acid bacteria for the production of safe and wholesome food. Z. Lebgensm. Unters. Forsch. 198:193-201. 50. Bernardeau, M., M. Guguen, and J.P. Vernoux. 2006. Beneficial lactobacilli in food and feed: long-term use, biodiversity and proposals for specific and realistic safety assessments. FEMS Microbial. Rev. 30:487-513. 51. Wood, G.C. et al. 2002. Lactobacillus species as a cause of ventilator associated pneumonia in a critically ill patient. Pharmacotherapy 22:1180-1182.

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