Biology:Lactobacillus reuteri

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Lactobacillus reuteri
Scientific classification
Domain:
Bacteria
Phylum:
Firmicutes
Class:
Bacilli
Order:
Lactobacillales
Family:
Lactobacillaceae
Genus:
Lactobacillus
Species:
L. reuteri
Binomial name
Lactobacillus reuteri
Kandler et al., 1982

Discovery

At 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 microbiologist Gerhard Reuter – for whom the species eventually was 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. L. reuteri was then recognized as a separate species within Lactobacillus.

Prevalence

In the early 1980s scientists began to find L. reuteri in many natural environments. It has been isolated from many foods, especially meat and milk.[2][4][5]

Interest in L. reuteri began to increase when scientists found it colonizing the intestines of healthy animals. Reuter first isolated L. reuteri from human fecal and intestinal samples in the 1960s.[6] The same experiments – attempting to isolate L. reuteri from feces and intestine of healthy animals – were done on nonhuman species, demonstrating that L. reuteri seems to be present 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 in the gut microbiota, including L. acidophilus, in a variety of animals found that L. reuteri was the only species to constitute a "major component" of the Lactobacillus species present in the gut of each of the tested host animals.[10] It is one of the most ubiquitous members of the mammalian gut microbiota.

In a related discovery, each 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, 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 colleagues discovered that L. reuteri produced a novel broad-spectrum antibiotic substance via the organism's fermentation of glycerol. They named this substance reuterin, after 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 inhibits the growth of some harmful Gram-negative and Gram-positive bacteria, along with yeasts, fungi and protozoa.[19] Researchers found that L. reuteri can secrete sufficient amounts of reuterin to achieve 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 without harming other gut microbiota.[12]

Some studies questioned whether reuterin production is essential for L. reuteri 's health-promoting activity. The discovery that it produces an antibiotic substance led to a great deal of further research. In early 2008, L. reuteri was confirmed to be capable of producing reuterin in the gastrointestinal tract, improving 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. Dietary supplementation can sustain high levels of it in those with deficiencies. Oral intake of L. reuteri has been shown to effectively colonize the intestines of healthy individuals. Colonization begins within days of ingestion, although levels drop months later if intake is stopped.[22] L. reuteri is found in breast milk.[23] Oral intake on the mother's part increases the amount of L. reuteri present in her milk, and the likelihood that it will be transferred to the child.[24]

L. reuteri benefits its host in a variety of ways, particularly by fighting off harmful infections and mediating the immune system.[citation needed]

Safety

The manipulation of the gut microbiota is complex and may cause bacteria-host interactions.[25] Although probiotics, in general, are considered safe, concerns exist about their use in certain cases.[25][26] Some people, such as those with compromised immune systems, short bowel syndrome, central venous catheters, heart valve disease and premature infants, may be at higher risk for adverse events.[27] Rarely, consumption of probiotics may cause bacteremia, fungemia and sepsis, potentially fatal infections, in children with lowered immune systems or who are already critically ill.[28]

Intestinal health

One of the better documented effects of L. reuteri is in the treatment of diarrheal diseases in children, where it significantly decreases symptom duration.[29][30] Treatment of rotaviral diarrhea with L. reuteri significantly shortens the duration of the illness as compared to placebo. This effect is dose-dependent: the more L. reuteri consumed, the faster the diarrhea stops.[31] L. reuteri is effective as a prophylactic for this illness; children fed it while healthy are less likely to fall ill with diarrhea.[32] With regard to prevention of gut infections, comparative research found L. reuteri to be more potent than other probiotics.[33][34] Animal research found it to reduce motor complexes and thus intestinal motility.[35]

L. reuteri may be effective treating necrotizing enterocolitis in pre-term infants. Meta-analysis of randomized studies suggests that L. reuteri can reduce the incidence of sepsis and shorten the required duration of hospital treatment in this population.[36]

L. reuteri is an effective treatment against infant colic.[37][38] Studies suggest that colicky infants treated with L. reuteri experience a reduction in time spent crying compared to those treated with simethicone[39] or placebo.[40] However, colic is still poorly understood, and it is not clear why or how L. reuteri ameliorates its symptoms. One theory holds that affected infants cry because of gastrointestinal discomfort; if this is the case, it is 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 eradicate, H. pylori in the gut.[41] 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.[42] Yet another study showed that L. reuteri effectively suppressed H. pylori infection and decreased the occurrence of dyspeptic symptoms, although it did not improve the outcome of antibiotic therapy.[43]

Oral health

L. reuteri may 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 tested species able to block S. mutans. Before testing in humans began, another study showed L. reuteri had no harmful effects on teeth. Clinical trials proved that people whose mouths are colonized with L. reuteri (via dietary supplementation) have significantly less S. mutans.[44] Since these studies were short-term, it is not 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 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.[45]

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 center compared to placebo and to the competing probiotic Bifidobacterium lactis.[46]

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.[47]

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 L. reuteri's benefits have been studied only in different animal species, such as pigs and mice.

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

Protection against pathogens

L. reuteri confers a high level of resistance to the pathogen Salmonella typhimurium, halving mortality rates in mice.[48] The same is true for chickens[49] and turkeys; L. reuteri greatly moderates the morbidity and mortality caused by this dangerous food-borne pathogen.

L. reuteri is 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.[50]

The protozoic parasite Cryptosporidium parvum causes severe watery diarrhea, which can become life-threatening in immunocompromised (as in individuals infected with HIV) patients. L. reuteri is known to lessen the symptoms of C. parvum infection in mice[51] and pigs.[12]

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.[52]

General health

In juvenile commercial livestock, such as turkey poults and piglets, body weight and growth rate are good health indicators. 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 spaces. In turkeys, for example, this phenomenon is known as "poult growth depression", or PGD.[53]

Supplementing the diets of these young animals with L. reuteri helps them to largely overcome the stresses imposed by unhealthy environs. Commercial turkeys fed L. reuteri from birth had nearly a 10% higher adult body weight than their peers raised in the same conditions.[54] A similar study on piglets showed L. reuteri is at least as effective as synthetic antibiotics in improving body weight under crowded conditions.[55]

The mechanism by which L. reuteri is able to support healthy growth is not entirely understood. It possibly serves to protect against illness caused by S. typhimurium and other pathogens (see above), which are much more common in crowded commercial farms. However, other studies found that it can help when the growth depression is caused entirely by a lack of dietary protein, and not by contagious disease.[56] 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,[57] 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[58], etc., from "leaking" into the bloodstream. This leaking, known as bacterial "translocation", 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[59] or injection with D-galactosamine,[60] a chemical which 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.[61]

Links to fat in diet of mice, and reversible symptoms of behavioral abnormalities

In mice, the absence of L. reuteri has been causally linked to maternal diet.[58] A gut microbial imbalance, lacking in L. reuteri, was linked to behavioral abnormalities consistent with autism in humans.[58] These symptoms were reversible by supplementing L. reuteri.[58]

References

  1. ↑ Orla-Jensen, S. 1919. The lactic acid Bacteria. Det Kongelige Danske Videnskasbernes Selskab. Naturvidenskabelige mathematiske Afdeling, NS 8.5.2
  2. ↑ 2.0 2.1 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. ↑ "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. 1965. 
  5. ↑ "Classification of citratefermenting lactobacilli isolated from lamb stomach, sheep milk, and pecorino romano cheese". ZBL. Bakt. Hyg. Abt. Orig. C2: 349–56. 1981. 
  6. ↑ "Numerical taxonomy of Lactobacillus spp. associated with healthy and diseased mucosa of the human intestines". J. Appl. Bacteriol. 74 (3): 314–23. March 1993. doi:10.1111/j.1365-2672.1993.tb03031.x. PMID 8468264. 
  7. ↑ "Taxonomy of lactobacilli isolated from the alimentary tract of chickens". Syst Appl Microbiol 6: 86–9. 1985. doi:10.1016/s0723-2020(85)80017-5. 
  8. ↑ "Development of intestinal lactobacilli in normal piglets". J. Appl. Bacteriol. 79 (2): 230–6. August 1995. doi:10.1111/j.1365-2672.1995.tb00940.x. PMID 7592119. 
  9. ↑ 9.0 9.1 "Systematics of the Lactobacillus population on rat intestinal mucosa with special reference to Lactobacillus reuteri". Antonie van Leeuwenhoek 61 (3): 175–83. April 1992. 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. ↑ 12.0 12.1 12.2 12.3 Casas IA; Dobrogosz WJ (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. ↑ 13.0 13.1 "Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri". Antimicrobial Agents and Chemotherapy 32 (12): 1854–8. 1988. doi:10.1128/aac.32.12.1854. PMID 3245697. 
  14. ↑ "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. 1997. doi:10.1016/s0168-1605(96)01180-4. PMID 9039561. 
  15. ↑ "Characterization of reutericyclin produced by Lactobacillus reuteri LTH2584". Applied and Environmental Microbiology 66 (10): 4325–33. 2000. doi:10.1128/aem.66.10.4325-4333.2000. PMID 11010877. 
  16. ↑ "Acid-catalysed hydration of acrylalde. Kinetics of the reaction and isolation of β-hydroxypropionaldehyde". J Chem Soc: 490–8. 1950. 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. ↑ "Purification and structural characterization of 3-hydroxypropionaldehyde and its derivatives". J. Agric. Food Chem. 51 (11): 3287–93. May 2003. doi:10.1021/jf021086d. PMID 12744656. https://semanticscholar.org/paper/5abe6ef4148e5e42938fc8b33f975a278e061e82. 
  19. ↑ "Chemical characterization of an antimicrobial substance produced by Lactobacillus reuteri". Antimicrob. Agents Chemother. 33 (5): 674–9. May 1989. doi:10.1128/aac.33.5.674. PMID 2751282. 
  20. ↑ "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. January 2008. doi:10.1111/j.1574-6941.2007.00412.x. PMID 18028400. 
  21. ↑ "Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobalamin production". DNA Res. 15 (3): 151–61. June 2008. doi:10.1093/dnares/dsn009. PMID 18487258. PMC 2650639. http://dnaresearch.oxfordjournals.org/cgi/pmidlookup?view=long&pmid=18487258. 
  22. ↑ "Safety and tolerance of Lactobacillus reuteri in healthy adult male subjects". Microbial Ecol Health Dis 8 (2): 41–50. 1995. doi:10.3109/08910609509141381. 
  23. ↑ "Occurrence of Lactobacillus reuteri, lactobacilli and bifidobacteria in human breast milk". Pediatr Res 58 (2): 415, abstract 353. 2005. doi:10.1203/00006450-200508000-00381. 
  24. ↑ "Intestinal microbiota in infants supplemented with the probiotic bacterium Lactobacillus reuteri". J Ped Gastroenterol Nutr 40 (5): 692, abstract PN 1–17. 2005. doi:10.1097/00005176-200505000-00232. 
  25. ↑ 25.0 25.1 "Diet therapy for inflammatory bowel diseases: The established and the new". World J Gastroenterol 22 (7): 2179–94. 2016. doi:10.3748/wjg.v22.i7.2179. PMID 26900283. 
  26. ↑ "Probiotic use in clinical practice: what are the risks?". Am J Clin Nutr 83 (6): 1256–64; quiz 1446–7. 2006. doi:10.1093/ajcn/83.6.1256. PMID 16762934. 
  27. ↑ "Risk and safety of probiotics.". Clin Infect Dis 60 Suppl 2: S129–34. 2015. doi:10.1093/cid/civ085. PMID 25922398. PMC 4490230. http://cid.oxfordjournals.org/content/60/suppl_2/S129.full. 
  28. ↑ "Probiotics in critically ill children". F1000Res 5: 407. 2016. doi:10.12688/f1000research.7630.1. PMID 27081478. 
  29. ↑ "Systematic review with meta-analysis: Lactobacillus reuteri DSM 17938 for diarrhoeal diseases in children". Aliment Pharmacol Ther 43 (10): 1025–34. May 2016. doi:10.1111/apt.13590. PMID 26991503. 
  30. ↑ Szajewska, H; Urbańska, M; Chmielewska, A; Weizman, Z; Shamir, R (September 2015). "Meta-analysis: Lactobacillus reuteri strain DSM 17938 (and the original strain ATCC 55730) for treating acute gastroenteritis in children". Benef Microbes 5 (3): 285–93. doi:10.3920/BM2013.0056. PMID 24463209. 
  31. ↑ "Bacteriotherapy with Lactobacillus reuteri in rotavirus gastroenteritis". Pediatr. Infect. Dis. J. 16 (12): 1103–7. December 1997. doi:10.1097/00006454-199712000-00002. PMID 9427453. 
  32. ↑ "Feeding of a probiotic for the prevention of community-acquired diarrhea in young Mexican children". Pediatr Res 39 (4 Part 2): 184A, abstract 1089. 1996. doi:10.1203/00006450-199604001-01111. 
  33. ↑ 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.
  34. ↑ 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.
  35. ↑ 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. 
  36. ↑ Athalye-Jape, G; Rao, S; Patole, S (June 9, 2015). "Lactobacillus reuteri DSM 17938 as a Probiotic for Preterm Neonates: A Strain-Specific Systematic Review.". JPEN J Parenter Enteral Nutr 40 (6): 783–94. doi:10.1177/0148607115588113. PMID 26059900. 
  37. ↑ Schreck, Bird A; Gregory, PJ; Jalloh, MA; Risoldi Cochrane, Z; Hein, DN (March 2, 2016). "Probiotics for the Treatment of Infantile Colic: A Systematic Review.". J Pharm Pract 30 (3): 366–374. doi:10.1177/0897190016634516. PMID 26940647. 
  38. ↑ Harb, T; Matsuyama, M; David, M; Hill, RJ (May 2016). "Infant Colic-What works: A Systematic Review of Interventions for Breast-fed Infants". J Pediatr Gastroenterol Nutr 62 (5): 668–86. doi:10.1097/MPG.0000000000001075. PMID 26655941. https://semanticscholar.org/paper/5777f4f72ca06b9f2a3e33f9f5747d92e6b08b50. 
  39. ↑ Savino F.; Pelle E.; Palumeri E.; Oggero R.; 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. https://semanticscholar.org/paper/4fc57967c2ea4d78dd7c4ec96cf1b22488bc822d. 
  40. ↑ Savino F.; Cordisco L.; Tarasco V.; Palumeri E.; Calabrese R.; Oggero R.; Roos S.; 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. 
  41. ↑ "Lactobacillus reuteri tablets suppress Helicobacter pylori infection—a double-blind randomised placebo-controlled cross-over clinical study". Kansenshogaku Zasshi 81 (4): 387–93. July 2007. doi:10.11150/kansenshogakuzasshi1970.81.387. PMID 17695792. 
  42. ↑ "Helicobacter pylori eradication with Lactobacillus reuteri. A double blind placebo-controlled study". Dig Liver Dis 37 (Suppl 1): 407–13. 2005. doi:10.1097/MCG.0000000000000007. PMID 24296423. 
  43. ↑ "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. April 2008. doi:10.1111/j.1523-5378.2008.00593.x. PMID 18321302. 
  44. ↑ "Lactobacillus reuteri in bovine milk fermented decreases the oral carriage of mutans streptococci". Int. J. Food Microbiol. 95 (2): 219–23. September 2004. doi:10.1016/j.ijfoodmicro.2004.03.006. PMID 15282133. 
  45. ↑ "Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri". Swed Dent J 30 (2): 55–60. 2006. PMID 16878680. 
  46. ↑ "Effect of a probiotic infant formula on infections in child care centers: comparison of two probiotic agents". Pediatrics 115 (1): 5–9. January 2005. doi:10.1542/peds.2004-1815. PMID 15629974. http://pediatrics.aappublications.org/cgi/pmidlookup?view=long&pmid=15629974. 
  47. ↑ "Increasing work-place healthiness with the probiotic Lactobacillus reuteri: a randomised, double-blind placebo-controlled study". Environ Health 4: 25. 2005. doi:10.1186/1476-069X-4-25. PMID 16274475. 
  48. ↑ 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.
  49. ↑ 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.
  50. ↑ "Principles of ex ovo competitive exclusion and in ovo administration of Lactobacillus reuteri". Poult. Sci. 76 (1): 179–96. January 1997. doi:10.1093/ps/76.1.179. PMID 9037704. http://ps.fass.org/cgi/pmidlookup?view=long&pmid=9037704. 
  51. ↑ "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. January 1997. doi:10.1093/infdis/175.1.218. PMID 8985225. 
  52. ↑ "Biotherapeutic effects of probiotic bacteria on candidiasis in immunodeficient mice". Infect. Immun. 65 (10): 4165–72. October 1997. doi:10.1128/IAI.65.10.4165-4172.1997. PMID 9317023. 
  53. ↑ Barnes JH (1993). "Evaluating poult growth and productivity during brooding". Turkeys 41: 23–4. 
  54. ↑ "Probiotic treatment with Lactobacillus reuteri protects commercial turkeys from avian growth depression". Biosci Microflora 17 (2): 141–7. 1998. doi:10.12938/bifidus1996.17.141. 
  55. ↑ 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.
  56. ↑ "Avian growth depression in chickens induced by environmental, microbiological, or nutritional stress is moderated by probiotic administrations of Lactobacillus reuteri". Biosci Microflora 17 (2): 133–9. 1998. doi:10.12938/bifidus1996.17.133. 
  57. ↑ "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. February 1993. doi:10.3109/00365529309096063. PMID 8382837. 
  58. ↑ 58.0 58.1 58.2 58.3 Buffington, Shelly A.; Prisco, Gonzalo Viana Di; Auchtung, Thomas A.; Ajami, Nadim J.; Petrosino, Joseph F.; Costa-Mattioli, Mauro (2016). "Microbial Reconstitution Reverses Maternal Diet-Induced Social and Synaptic Deficits in Offspring". Cell 165 (7): 1762–1775. doi:10.1016/j.cell.2016.06.001. PMID 27315483. 
  59. ↑ "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. February 1995. doi:10.3109/00365529509093259. PMID 7732342. 
  60. ↑ "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. March 1997. doi:10.1002/hep.510250325. PMID 9049212. 
  61. ↑ "The effects of Lactobacillus strains and oat fiber on methotrexate-induced enterocolitis in rats". Gastroenterology 111 (2): 334–44. August 1996. doi:10.1053/gast.1996.v111.pm8690198. PMID 8690198. 

External links

Wikidata ☰ Q597078 entry




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