Lactobacillus reuteri

Lactobacillus reuteri
Scientific classification
Domain: Bacteria
Phylum: Firmicutes
Class: Bacilli
Order: Lactobacillales
Family: Lactobacillaceae
Genus: Lactobacillus
Species: L. reuteri
Binomial name
Lactobacillus reuteri
N/A

Lactobacillus reuteri is a Gram-positive bacterium that naturally inhabits the gut of mammals and birds. First described in the early 1980s, some strains of L. reuteri are used as probiotics. BioGaia AB in Sweden owns several commercially important strains and a large number of different patents for commercial usage of L. reuteri.

Discovery

Though the species Lactobacillus reuteri has been recognized for some time, knowledge of its probiotic properties did not come until much later.

As early as the turn of the 20th century, L. reuteri was recorded in scientific classifications of lactic acid bacteria,[1] though at this time it was mistakenly grouped as a member of Lactobacillus fermentum. In the 1960s, further work by German microbiologist Gerhard Reuter – for whom the species eventually would be named – began to distinguish L. reuteri from L. fermentum. Reuter reclassified the species as "Lactobacillus fermentum biotype II".[2]

L. reuteri was eventually identified as a distinct species in 1980 by Kandler et al.[3] This group found significant differences between L. reuteri and other biotypes of L. fermentum, and thus proposed it be given formal species identity. They chose the species name "reuteri", after discoverer Gerhard Reuter, and L. reuteri has since been recognized as a separate species within the Lactobacillus genus.

Prevalence

In the early 1980s, shortly after its recognition as a distinct species, scientists began to find L. reuteri in many natural environments; it has been isolated from many foods, especially meat and milk products.[2][4][5]

Interest in L. reuteri began to increase as scientists began to find it colonizing the intestines of healthy animals. Gerhard Reuter first isolated L. reuteri from human fecal and intestinal samples in the 1960s, and this work was later repeated by other researchers.[6] The same experiments – attempting to isolate L. reuteri from feces and intestine of healthy animals – were also done for nonhuman species, proving that L. reuteri seems to be present almost universally throughout the animal kingdom. For example, L. reuteri was discovered to be present naturally in the intestines of healthy sheep, chickens,[7] pigs,[8] and rodents.[9]

Furthermore, a study searching for 18 major species of gut flora, including Lactobacillus acidophilus, in a variety of animals found L. reuteri was the only bacterium to constitute a "major component" of the Lactobacillus species present in the gut of each of the host animals tested.[10] It is now well-established as one of the most ubiquitous members of the naturally occurring gut bacteria.

In a related discovery, each animal host seems to have a host-specific strain of L. reuteri, e.g. a rat strain for rats, a pig strain for pigs, etc.[9][11] The universality of L. reuteri, in conjunction with this evolved host-specificity, has led scientists to make inferences about its importance in promoting the health of the host organism.[12]

Effects

Antimicrobial

L. reuteri is known to produce reuterin,[13] reutericin 6,[14] and reutericyclin.[15]

Reuterin

In the late 1980s, Walter Dobrogosz, Ivan Casas, and their colleagues discovered L. reuteri produced a novel broad-spectrum antibiotic substance via the organism's fermentation of glycerol. They named this substance reuterin, also after Gerhard Reuter.[13] Reuterin is a multiple-compound dynamic equilibrium (HPA system, HPA) consisting of 3-hydroxypropionaldehyde, its hydrate, and its dimer.[16][17] At concentrations above 1.4 M, the HPA dimer was predominant. However, at concentrations relevant for biological systems, HPA hydrate was the most abundant, followed by the aldehyde form.[18]

Reuterin was found to inhibit the growth of some harmful Gram-negative and Gram-positive bacteria, along with yeasts, fungi, and protozoa.[19] Naturally, a gut organism capable of fighting off other, harmful gut organisms was of great interest. Researchers found L. reuteri can indeed secrete sufficient amounts of reuterin to cause the desired antimicrobial effects. Furthermore, since about four to five times the amount of reuterin is needed to kill "good" gut bacteria (i.e. L. reuteri and other Lactobacillus species) as "bad", this would allow L. reuteri to remove gut invaders while keeping normal gut flora intact.[12]

Some studies have called into question whether or not reuterin production is essential for L. reuteri 's health-promoting activity. However, the discovery that it naturally produces an antibiotic substance was nevertheless important, as it has led to a great deal of further research. In fact, in early 2008, L. reuteri was confirmed to be capable of producing reuterin in the gastrointestinal tract, and this improves its ability to inhibit the growth of E. coli.[20]

The gene cluster controlling the biosynthesis of reuterin and cobalamin in the L. reuteri genome is a genomic island acquired from an anomalous source.[21]

Clinical results in humans

Although L. reuteri occurs naturally in humans, it is not found in all individuals. Therefore, dietary supplementation is needed to introduce and maintain high levels of it in some people. Oral intake of L. reuteri has been shown to effectively colonize the intestine of healthy people; colonization begins rapidly within days of ingestion, although the levels in the body drop within several months after intake is stopped.[22] Furthermore, L. reuteri is found in breast milk,[23] and oral intake on the mother's part likewise increases the amount of L. reuteri present in her milk, and the likelihood that it will be transferred to the child's body.[24]

Once present in the body, L. reuteri benefits its host in a variety of ways, particularly by fighting off harmful infections and mediating the body's immune system.

Safety

L. reuteri has been tested for host tolerance in children,[25] healthy adults,[26] and the immunosuppressed (HIV patients).[27] No adverse serious medical consequences have been observed up to the maximum tested dosage of 1010 colony-forming units per day, and no significant differences in standard medical laboratory tests were found, including complete blood count, urinalysis, complete metabolic panel, and liver function tests between those subjects given L. reuteri and those given placebo.

Intestinal health

One of the most well-documented effects of L. reuteri is in the treatment of rotavirus-induced diarrhea, especially in children. Treatment of rotaviral diarrhea by consumption of L. reuteri significantly shortens the duration of the illness as compared to placebo. Furthermore, this effect is dose-dependent: the more L. reuteri consumed, the faster the diarrhea stops.[28] L. reuteri is also effective as a prophylactic for this illness; children fed it while healthy are less likely to fall ill with diarrhea in the first place.[29] With regard to prevention of gut infections, comparative research has found L. reuteri to be more potent than other probiotic organisms.[30][31] It has also been found in animal research to reduce motor complexes and thus intestinal motility.[32]

L. reuteri is also an effective treatment against infant colic. Over a period of several weeks, infants who are given L. reuteri steadily decrease the amount of time each day spent crying – the defining symptom of colic. In fact, it was much better in decreasing the infants' crying time than the standard therapy of simethicone treatment.[33] A randomized, double-blind, placebo-controlled trial of 50 exclusively breast-fed, colicky infants found a significant decrease in daily crying time amounts when treated with L. reuteri DSM 17 938 compared with placebo. It further found a significant increase in lactobacilli colonization, a decrease in fecal Escherichia coli and ammonia when compared with placebo.[34] However, colic is still poorly understood, and it is not clear why or how L. reuteri ameliorates its symptoms. One theory of colic, though, holds that affected infants cry because of severe gastrointestinal discomfort; if this is indeed the case, it is quite plausible that L. reuteri somehow acts to lessen this discomfort, since its primary residence is inside the gut.

Growing evidence indicates L. reuteri is capable of fighting the gut pathogen Helicobacter pylori, which causes peptic ulcers and is endemic in parts of the developing world. One study showed dietary supplementation of L. reuteri alone reduces, but does not fully eradicate, H. pylori in the gut.[35] Another study found the addition of L. reuteri to omeprazole therapy dramatically increased (from 0% to 60%) the cure rate of H. pylori-infected patients compared to the drug alone.[36] Yet another study showed L. reuteri effectively suppressed H. pylori infection and decreased the occurrence of dyspeptic symptoms, although it did not improve the outcome of antibiotic therapy.[37]

Oral health

L. reuteri may also be capable of promoting dental health, as it has been proven to kill Streptococcus mutans, a bacterium responsible for tooth decay. A screen of several probiotic bacteria found L. reuteri was the only species of those tested able to block S. mutans. Before testing in humans was begun, another study showed L. reuteri had no harmful effects on teeth. Clinical trials have since proven those people whose mouths are colonized with L. reuteri (via dietary supplementation) have significantly less of the harmful S. mutans.[38] Since these studies have been short-term, it is not yet known whether L. reuteri prevents tooth decay. However, since it is able to reduce the numbers of an important decay-causing bacterium, this would be expected.

Gingivitis also may be ameliorated by consumption of L. reuteri. Patients afflicted with severe gingivitis showed decreased gum bleeding, plaque formation, and other gingivitis-associated symptoms compared with placebo after chewing gum containing L. reuteri.[39]

General health

By protecting against many common infections, L. reuteri promotes overall wellness in both children and adults. Double-blind, randomized studies in child care centers have found L. reuteri-fed infants fall sick less often, require fewer doctor visits, and are absent fewer days from the day care center compared to placebo and to the competing probiotic Bifidobacterium lactis.[40]

Similar results have been found in adults; those consuming L. reuteri daily end up falling ill 50% less often, as measured by their decrease use of sick leave.[41]

Results in animal models

Scientific studies that require harming the subjects (for example, exposing them to a dangerous virus) cannot be conducted in humans. Therefore, many of the benefits of L. reuteri have been studied only in different animal species, such as pigs and mice. Given the similarity of mammalian species, however, it is likely – though not scientifically proven – that these benefits hold true for humans, as well.

In general, animal studies on L. reuteri are done using the species-specific strain of the bacterium (see above).

Protection against pathogens

L. reuteri confers a high level of resistance to the pathogen Salmonella typhimurium, halving mortality rates in mice.[42] The same is true for chickens[43] and turkeys; L. reuteri greatly moderates the morbidity and mortality caused by this dangerous food-borne pathogen.

L. reuteri is also effective in stopping harmful strains of E. coli from affecting their hosts. A study performed in chickens showed L. reuteri was as potent as the antibiotic gentamicin in preventing E. coli-related deaths.[44]

The protozoic parasite Cryptosporidium parvum causes severe watery diarrhea, which can become life-threatening if the patient is immunocompromised (as in individuals infected with HIV). L. reuteri is known to lessen the symptoms of C. parvum infection in mice[45] and pigs.[12] With no known direct treatment for C. parvum (the antibiotic paromomycin has limited effect),[46] L. reuteri may prove valuable in protecting patients suffering from this disease.

Some protective effect against the yeast Candida albicans has been found in mice, but in this case, L. reuteri did not work as well as other probiotic organisms, such as L. acidophilus and L. casei.[47]

General health

In young commercial livestock, such as turkey poults and piglets, body weight and growth rate are good indicators of the health of the animal. Animals raised in the dirty, crowded environments of commercial farms are generally less healthy (and therefore weigh less) than their counterparts born and bred in cleaner homes. In turkeys, for example, this phenomenon is known as "poult growth depression", or PGD.[48]

Supplementing the diets of these young farm animals with L. reuteri helps them to largely overcome the stresses imposed by their unhealthy habitats. Commercial turkeys fed L. reuteri from birth had nearly a 10% higher adult body weight than their peers raised in the same conditions.[49] A similar study on piglets showed L. reuteri is at least as effective as synthetic antibiotics in improving body weight under crowded conditions.[50]

The mechanism by which L. reuteri is able to support the healthy growth of these animals is not entirely understood. It possibly serves to protect livestock against illness caused by Salmonella typhimurium and other pathogens (see above), which are much more common in crowded commercial farms. However, other studies have revealed it can also help when the growth depression is caused entirely by a lack of dietary protein, and not by contagious disease.[51] This raises the possibility that L. reuteri somehow improves the intestines' ability to absorb and process nutrients.[12]

Chemical and trauma-induced injury

Treating colonic tissue from rats with acetic acid causes an injury similar to the human condition ulcerative colitis. Treating the injured tissue with L. reuteri immediately after removing the acid almost completely reverses any ill effects,[52] leading to the possibility that L. reuteri may be beneficial in the treatment of human colitis patients.

In addition to its role in digestion, the intestinal wall is also vital in preventing harmful bacteria, endotoxins, etc., from "leaking" into the bloodstream. This leaking, known as bacterial "translocation", is very dangerous and can lead to lethal conditions such as sepsis. In humans, translocation is more likely to occur following such events as liver injury and ingestion of some poisons. In rodent studies, L. reuteri was found to greatly reduce the amount of bacterial translocation following either the surgical removal of the liver[53] or injection with D-galactosamine,[54] a chemical which also causes liver damage.

The anticancer drug methotrexate causes severe enterocolitis in high doses. L. reuteri greatly mitigates the symptoms of methotrexate-induced enterocolitis in rats, one of which is bacterial translocation.[55]

References

  1. Orla-Jensen, S. 1919. The lactic acid Bacteria. Det Kongelige Danske Videnskasbernes Selskab. Naturvidenskabelige mathematiske Afdeling, NS 8.5.2
  2. 1 2 Reuter G. (1965). "Das vorkommen von laktobazillen in lebensmitteln und ihr verhalten im menschlichen intestinaltrakt". Zbl Bak Parasit Infec Hyg I Orig 197 (S): 468–87.
  3. Kandler O., Stetter K., Kohl R. (1980). "Lactobacillus reuteri sp. nov. a new species of heterofermentative lactobacilli". Zbl. Bakt. Hyg. Abt. Orig. C1: 264–9.
  4. Lerche M, Reuter G (1965). "Das vorkommen aerob wachsender grampositiver stabchen des genus Lactobacuillus beijerinck im darminhalt erwachsener menchen". Zbl Bak Parasit Infec Hyg I Orig 185 (S): 446–81.
  5. Dellaglio F, Arrizza FS, Leda A (1981). "Classification of citratefermenting lactobacilli isolated from lamb stomach, sheep milk, and pecorino romano cheese". Zbl Bakt Hyg Abt Orig C2: 349–56.
  6. Molin G, Jeppsson B, Johansson ML, et al. (March 1993). "Numerical taxonomy of Lactobacillus spp. associated with healthy and diseased mucosa of the human intestines". J. Appl. Bacteriol. 74 (3): 314–23. doi:10.1111/j.1365-2672.1993.tb03031.x. PMID 8468264.
  7. Sarra PG, Dellaglio F, Bottazzi V (1985). "Taxonomy of lactobacilli isolated from the alimentary tract of chickens". Syst Appl Microbiol 6: 86–9. doi:10.1016/s0723-2020(85)80017-5.
  8. Naito S, Hayashidani H, Kaneko K, Ogawa M, Benno Y (August 1995). "Development of intestinal lactobacilli in normal piglets". J. Appl. Bacteriol. 79 (2): 230–6. doi:10.1111/j.1365-2672.1995.tb00940.x. PMID 7592119.
  9. 1 2 Molin G, Johansson ML, Ståhl M, et al. (April 1992). "Systematics of the Lactobacillus population on rat intestinal mucosa with special reference to Lactobacillus reuteri". Antonie Van Leeuwenhoek 61 (3): 175–83. doi:10.1007/BF00584224. PMID 1325752.
  10. Mitsuoka T (1992). "The human gastrointestinal tract". In Wood BJB. The lactic acid bacteria in health and disease. 1. The lactic acid bacteria. New York: Elsevier Applied Science. pp. 69–114.
  11. Casas IA, Dobrogosz WJ (1997). "Lactobacillus reuteri: An overview of a new probiotic for humans and animals". Microecol Therap 25: 221–31.
  12. 1 2 3 4 Casas, Ivan A., Dobrogosz, Walter J. (December 1, 2000). "Validation of the Probiotic Concept: Lactobacillus reuteri Confers Broad-spectrum Protection against Disease in Humans and Animals". Microbial Ecology in Health and Disease 12 (4). doi:10.3402/mehd.v12i4.8196.
  13. 1 2 Talarico TL, Casas IA, Chung TC, Dobrogosz WJ (1988). "Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri". Antimicrobial Agents and Chemotherapy 32 (12): 1854–8. doi:10.1128/aac.32.12.1854. PMC 176032. PMID 3245697. Retrieved 2015-01-19.
  14. Kabuki T, Saito T, Kawai Y, Uemura J, Itoh T (1997). "Production, purification and characterization of reutericin 6, a bacteriocin with lytic activity produced by Lactobacillus reuteri LA6". International Journal of Food Microbiology 34 (2): 145–56. doi:10.1016/s0168-1605(96)01180-4. PMID 9039561. Retrieved 2015-01-19.
  15. Gänzle MG, Höltzel A, Walter J, Jung G, Hammes WP (2000). "Characterization of reutericyclin produced by Lactobacillus reuteri LTH2584". Applied and Environmental Microbiology 66 (10): 4325–33. doi:10.1128/aem.66.10.4325-4333.2000. PMC 92303. PMID 11010877. Retrieved 2015-01-19.
  16. Hall RH, Stern ES (1950). "Acid-catalysed hydration of acrylalde. Kinetics of the reaction and isolation of β-hydroxypropionaldehyde". J Chem Soc: 490–8. doi:10.1039/jr9500000490.
  17. Nielsen AT, Moore DW, Schuetze Jr. A. "13C and 1H NMR study of formaldehyde reactions with acetaldehyde and acrolein. Synthesis of 2-(hydroxymethyl)-1,3-propanediol". Pol J Chem 55: 1393–1403.
  18. Vollenweider S, Grassi G, König I, Puhan Z (May 2003). "Purification and structural characterization of 3-hydroxypropionaldehyde and its derivatives". J. Agric. Food Chem. 51 (11): 3287–93. doi:10.1021/jf021086d. PMID 12744656.
  19. Talarico TL, Dobrogosz WJ (May 1989). "Chemical characterization of an antimicrobial substance produced by Lactobacillus reuteri". Antimicrob. Agents Chemother. 33 (5): 674–9. doi:10.1128/aac.33.5.674. PMC 172512. PMID 2751282.
  20. Cleusix V, Lacroix C, Vollenweider S, Le Blay G (January 2008). "Glycerol induces reuterin production and decreases Escherichia coli population in an in vitro model of colonic fermentation with immobilized human feces". FEMS Microbiol. Ecol. 63 (1): 56–64. doi:10.1111/j.1574-6941.2007.00412.x. PMID 18028400.
  21. Morita H, Toh H, Fukuda S, et al. (June 2008). "Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobalamin production". DNA Res. 15 (3): 151–61. doi:10.1093/dnares/dsn009. PMC 2650639. PMID 18487258.
  22. Wolf BW, Garleb KA, Ataya DG, Casas IA (1995). "Safety and tolerance of Lactobacillus reuteri in healthy adult male subjects". Microbial Ecol Health Dis 8 (2): 41–50. doi:10.3109/08910609509141381.
  23. Sinkiewicz G, Nordström EA (2005). "Occurrence of Lactobacillus reuteri, lactobacilli and bifidobacteria in human breast milk". Pediatr Res 58 (2): 415, abstract 353. doi:10.1203/00006450-200508000-00381.
  24. Abrahamsson T, Jakobsson T, Sinkiewicz G, Fredriksson M, Björkstén B. "Intestinal microbiota in infants supplemented with the probiotic bacterium Lactobacillus reuteri". J Ped Gastroenterol Nutr 40 (5): 692, abstract PN 1–17. doi:10.1097/00005176-200505000-00232.
  25. Ruiz-Palacios G, Tuz F, Arteaga F, Guerrero ML, Dohnalek M, Hilty M (1992). "Tolerance and fecal colonization with Lactobacillus reuteri in children fed a beverage with a mixture of Lactobacillus spp". Pediatr Res 39: 1090 Abstract.
  26. Wolf BW, Garleb KA, Ataya DG, Casas IA (1995). "Safety and tolerance of Lactobacillus reuteri in healthy adult male subjects". Microbial Ecol Health Dis 8 (2): 41–50. doi:10.3109/08910609509141381.
  27. Wolf BW, Wheeler KB, Ataya DG, Garleb KA (December 1998). "Safety and tolerance of Lactobacillus reuteri supplementation to a population infected with the human immunodeficiency virus". Food Chem. Toxicol. 36 (12): 1085–94. doi:10.1016/S0278-6915(98)00090-8. PMID 9862651.
  28. Shornikova AV, Casas IA, Mykkänen H, Salo E, Vesikari T (December 1997). "Bacteriotherapy with Lactobacillus reuteri in rotavirus gastroenteritis". Pediatr. Infect. Dis. J. 16 (12): 1103–7. doi:10.1097/00006454-199712000-00002. PMID 9427453.
  29. Ruiz-Palacios G, Guerrero ML, Hilty M (1996). "Feeding of a probiotic for the prevention of community-acquired diarrhea in young Mexican children". Pediatr Res 39 (4 Part 2): 184A, abstract 1089. doi:10.1203/00006450-199604001-01111.
  30. Romeo MG, Betta P, Oliveri S. (2006) Presented at the 5th Annual meeting of the Italian Society of Perinatal Medicine, Parma, Italy, 15–17 June 2006. Abstract published in J Perinat Med 34(Suppl 1): A9, abstract MSL_24.
  31. Guerrero M, Dohnalek M, Newton P, Kuznetsova O, Ruiz-Palacios G, Murphy T, Calva J, Hilty M, Costigan T., 1st World Congress of Pediatric Infectious Diseases, Dec. 1996, abstract no. 610:45-2.
  32. Wang, B.; Mao, YK.; Diorio, C.; Pasyk, M.; Wu, RY.; Bienenstock, J.; Kunze, WA. (Oct 2010). "Luminal administration ex vivo of a live Lactobacillus species moderates mouse jejunal motility within minutes.". FASEB J 24 (10): 4078–88. doi:10.1096/fj.09-153841. PMID 20519636.
  33. Savino F., Pelle E., Palumeri E., Oggero R. and Miniero R. (2007). "Lactobacillus reuteri (ATCC strain 55730) versus simethicone in the treatment of infantile colic: a prospective randomized study". Pediatrics 119 (1): 124–130. doi:10.1542/peds.2006-1222. PMID 17200238.
  34. Savino F., Cordisco L.,Tarasco V., Palumeri E., Calabrese R., Oggero R., Roos S. and Diego Matteuzzi. (2010). "Lactobacillus reuteri DSM 17938 in Infantile Colic: A Randomized, Double-Blind, Placebo-Controlled Trial". Pediatrics 126 (3): e526–e533. doi:10.1542/peds.2010-0433. PMID 20713478.
  35. Imase K, Tanaka A, Tokunaga K, Sugano H, Ishida H, Takahashi S (July 2007). "Lactobacillus reuteri tablets suppress Helicobacter pylori infection—a double-blind randomised placebo-controlled cross-over clinical study". Kansenshōgaku Zasshi 81 (4): 387–93. PMID 17695792.
  36. Saggioro A, Caroli M, Pasini M, Bortoluzzi F, Girardi L, Pilone G (2005). "Helicobacter pylori eradication with Lactobacillus reuteri. A double blind placebo-controlled study". Dig Liver Dis 37 (Suppl 1): S88, abstr. PO1.49.
  37. Francavilla R, Lionetti E, Castellaneta SP, et al. (April 2008). "Inhibition of Helicobacter pylori infection in humans by Lactobacillus reuteri ATCC 55730 and effect on eradication therapy: a pilot study". Helicobacter 13 (2): 127–34. doi:10.1111/j.1523-5378.2008.00593.x. PMID 18321302.
  38. Nikawa H, Makihira S, Fukushima H, et al. (September 2004). "Lactobacillus reuteri in bovine milk fermented decreases the oral carriage of mutans streptococci". Int. J. Food Microbiol. 95 (2): 219–23. doi:10.1016/j.ijfoodmicro.2004.03.006. PMID 15282133.
  39. Krasse P, Carlsson B, Dahl C, Paulsson A, Nilsson A, Sinkiewicz G (2006). "Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri". Swed Dent J 30 (2): 55–60. PMID 16878680.
  40. Weizman Z, Asli G, Alsheikh A (January 2005). "Effect of a probiotic infant formula on infections in child care centers: comparison of two probiotic agents". Pediatrics 115 (1): 5–9. doi:10.1542/peds.2004-1815. PMID 15629974.
  41. Tubelius P, Stan V, Zachrisson A (2005). "Increasing work-place healthiness with the probiotic Lactobacillus reuteri: a randomised, double-blind placebo-controlled study". Environ Health 4: 25. doi:10.1186/1476-069X-4-25. PMC 1298318. PMID 16274475.
  42. Carbajal N, Sriburi A, Carter P, Dobrogosz W, Casas, I. Probiotic administrations of Lactobacillus reuteri protect mice from Salmonella typhimurium infection. Proceedings of the 36th Annual Meeting of the Association for Gnotobiotics. 1998 Jun 14–16; Bethesda (MD): Association for Gnotobiotics; 1998.
  43. Casas IA, Edens FW, Dobrogosz WJ. Lactobacillus reuteri: an effective probiotic for poultry and other animals. Lactic acid bacteria, 2nd ed. New York: Marcel Dekker, 1998: 475–518.
  44. Edens FW, Parkhurst CR, Casas IA, Dobrogosz WJ (January 1997). "Principles of ex ovo competitive exclusion and in ovo administration of Lactobacillus reuteri". Poult. Sci. 76 (1): 179–96. doi:10.1093/ps/76.1.179. PMID 9037704.
  45. Alak JI, Wolf BW, Mdurvwa EG, Pimentel-Smith GE, Adeyemo O (January 1997). "Effect of Lactobacillus reuteri on intestinal resistance to Cryptosporidium parvum infection in a murine model of acquired immunodeficiency syndrome". J. Infect. Dis. 175 (1): 218–21. doi:10.1093/infdis/175.1.218. PMID 8985225.
  46. Cryptosporidium parvum
  47. Wagner RD, Pierson C, Warner T, et al. (October 1997). "Biotherapeutic effects of probiotic bacteria on candidiasis in immunodeficient mice". Infect. Immun. 65 (10): 4165–72. PMC 175599. PMID 9317023.
  48. Barnes JH (1993). "Evaluating poult growth and productivity during brooding". Turkeys 41: 23–4.
  49. Casas IA, Edens FW, Parkhurst CR, Dobrogosz WJ (1998). "Probiotic treatment with Lactobacillus reuteri protects commercial turkeys from avian growth depression". Biosci Microflora 17: 141–7. doi:10.12938/bifidus1996.17.141.
  50. Blanchard P, Gill P, Schulze H. Efficacy of Lactobacillus reuteri 1063-IA in pre- and post-weaning pigs. Hertfordshire SG5 4JG (UK): MLC Stotfold Pig Development Unit; 1998. Study Reference No. FF9801.
  51. Dunham HJ, Casas IA, Edens FW, Parkhurst CR, Garlich JD, Dobrogosz WJ (1998). "Avian growth depression in chickens induced by environmental, microbiological, or nutritional stress is moderated by probiotic administrations of Lactobacillus reuteri". Biosci Microflora 17: 133–9. doi:10.12938/bifidus1996.17.133.
  52. Fabia R, Ar'Rajab A, Johansson ML, et al. (February 1993). "The effect of exogenous administration of Lactobacillus reuteri R2LC and oat fiber on acetic acid-induced colitis in the rat". Scand. J. Gastroenterol. 28 (2): 155–62. doi:10.3109/00365529309096063. PMID 8382837.
  53. Wang XD, Soltesz V, Molin G, Andersson R (February 1995). "The role of oral administration of oatmeal fermented by Lactobacillus reuteri R2LC on bacterial translocation after acute liver failure induced by subtotal liver resection in the rat". Scand. J. Gastroenterol. 30 (2): 180–5. doi:10.3109/00365529509093259. PMID 7732342.
  54. Adawi D, Kasravi FB, Molin G, Jeppsson B (March 1997). "Effect of Lactobacillus supplementation with and without arginine on liver damage and bacterial translocation in an acute liver injury model in the rat". Hepatology 25 (3): 642–7. doi:10.1002/hep.510250325. PMID 9049212.
  55. Mao Y, Nobaek S, Kasravi B, et al. (August 1996). "The effects of Lactobacillus strains and oat fiber on methotrexate-induced enterocolitis in rats". Gastroenterology 111 (2): 334–44. doi:10.1053/gast.1996.v111.pm8690198. PMID 8690198.

External links

This article is issued from Wikipedia - version of the Thursday, May 05, 2016. The text is available under the Creative Commons Attribution/Share Alike but additional terms may apply for the media files.