Limosilactobacillus reuteri

Limosilactobacillus reuteri is a lactic acid bacterium found in a variety of natural environments, including the gastrointestinal tract of humans and other animals. It does not appear to be pathogenic and may have health effects.

Limosilactobacillus reuteri
Scientific classification
Domain:
Bacteria
Phylum:
Firmicutes
Class:
Bacilli
Order:
Lactobacillales
Family:
Lactobacillaceae
Genus:
Limosilactobacillus
Species:
L. reuteri
Binomial name
Limosilactobacillus reuteri
Zheng et al., 2020
Synonyms
  • Lactobacillus reuteri Kandler et al., 1980
  • Lactobacillus fermentum biotype II Reuter, 1965

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, reclassified the species as L. fermentum biotype II.[2]

Significant differences were found between biotype II and other biotypes of L. fermentum, to the point that in 1980 it was identified as a distinct species and the formal species identity, L. reuteri, was proposed.[3] In April 2020, L. reuteri was reassigned to the genus Limosilactobacillus.[4]

Prevalence

L. reuteri is found in a variety of natural environments. It has been isolated from many foods, especially meats and dairy products.[2][5][6] It appears to be essentially ubiquitous in the animal kingdom, having been found in the gastrointestinal tracts and feces of healthy humans,[7] sheep, chickens,[8] pigs,[9] and rodents.[10] It is the only species to constitute a "major component" of the Lactobacillus species present in the gut of each of the tested host animals,[11] and each host seems to harbor its own specific strain of L. reuteri.[10][12] It is possible that L. reuteri contributes to the health of its host organism in some manner.[13]

L. reuteri is present as a dominant member of fermenting organisms in type II sourdoughs; several metabolic traits of L. reuteri, including exopolysaccharide formation and conversion of glutamine to glutamate, improve bread quality. [14]

Effects

Antimicrobial

L. reuteri is known to produce reuterin,[15] reutericin 6[16] and reutericyclin.[17][18]

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.[15] Reuterin is a multiple-compound dynamic equilibrium (HPA system, HPA) consisting of 3-hydroxypropionaldehyde, its hydrate, and its dimer.[19][20] 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.[21]

Reuterin inhibits the growth of some harmful Gram-negative and Gram-positive bacteria, along with yeasts, fungi and protozoa.[22] 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.[13]

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.[23]

The gene cluster controlling the biosynthesis of reuterin and cobalamin in the L. reuteri genome is a genomic island acquired from an anomalous source.[24]

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.[25] L. reuteri is found in breast milk.[26] 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.[27]

Safety

Manipulation of gut microbiota is a complex process that may cause bacteria-host interactions.[28] Although probiotics in general are considered safe, concerns exist about their use in certain cases.[28][29] 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.[30] Rarely, consumption of probiotics may cause bacteremia, fungemia and sepsis, potentially fatal infections, in children with compromised immune systems or who are already critically ill.[31]

Intestinal health

One of the better documented effects of L. reuteri is a significant reduction of symptom duration in pediatric diarrheal disease.[32][33][34] L. reuteri is effective as a prophylactic for this illness; children fed it while healthy are less likely to fall ill with diarrhea.[35] With regard to prevention of gut infections, comparative research found L. reuteri to be more potent than other probiotics.[36][37] Animal research found it to reduce motor complexes and thus intestinal motility.[38]

L. reuteri may be effective treating necrotizing enterocolitis in preterm 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.[39]

L. reuteri is an effective treatment against infant colic.[40][41] Studies suggest that colicky infants treated with L. reuteri experience a reduction in time spent crying compared to those treated with simethicone[42] or placebo.[43] 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.[44] 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.[45] 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.[46]

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.[47] 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.[48]

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.[49]

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.[50]

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.[51] The same is true for chickens[52] 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.[53]

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[54] and pigs.[13]

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.[55]

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.[56]

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.[57] A similar study on piglets showed L. reuteri is at least as effective as synthetic antibiotics in improving body weight under crowded conditions.[58]

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.[59] This raises the possibility that L. reuteri somehow improves the intestines' ability to absorb and process nutrients.[13]

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,[60] 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,[61] 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[62] or injection with D-galactosamine,[63] 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.[64]

In mice, the absence of L. reuteri has been causally linked to maternal diet.[61] A gut microbial imbalance, lacking in L. reuteri, was linked to behavioral abnormalities consistent with autism in humans.[61] These symptoms were reversible by supplementing L. reuteri.[61]

References
  1. Orla-Jensen, S. 1919. The lactic acid Bacteria. Det Kongelige Danske Videnskasbernes Selskab. Naturvidenskabelige mathematiske Afdeling, NS 8.5.2
  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. Zheng, Jinshui; Wittouck, Stijn; Salvetti, Elisa; Franz, Charles M.A.P.; Harris, Hugh M.B.; Mattarelli, Paola; O’Toole, Paul W.; Pot, Bruno; Vandamme, Peter; Walter, Jens; Watanabe, Koichi (2020). "A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae". International Journal of Systematic and Evolutionary Microbiology. 70 (4): 2782–2858. doi:10.1099/ijsem.0.004107. ISSN 1466-5026. PMID 32293557.
  5. 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.
  6. 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.
  7. 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.
  8. 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.
  9. 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.
  10. 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. S2CID 46249658.
  11. Mitsuoka T (1992). "The human gastrointestinal tract". In Wood BJB (ed.). The lactic acid bacteria in health and disease. 1. The lactic acid bacteria. New York: Elsevier Applied Science. pp. 69–114.
  12. Casas IA; Dobrogosz WJ (1997). "Lactobacillus reuteri: An overview of a new probiotic for humans and animals". Microecol Therap. 25: 221–31.
  13. 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.
  14. Gänzle, Michael G.; Zheng, Jinshui (2019-08-02). "Lifestyles of sourdough lactobacilli - Do they matter for microbial ecology and bread quality?". International Journal of Food Microbiology. 302: 15–23. doi:10.1016/j.ijfoodmicro.2018.08.019. ISSN 1879-3460. PMID 30172443.
  15. 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.
  16. 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.
  17. 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.
  18. Knysh O, Martynov A (2020). "Lactobacillus reuteri cell-free extracts against antibiotic-resistant bacteria". Zaporozhye Medical Journal. 22 (4): 547–553. doi:10.14739/2310-1210.2020.4.208397.
  19. 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.
  20. 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.
  21. 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. S2CID 39296044.
  22. 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.
  23. 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.
  24. 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.
  25. Wolf BW, Garleb KA, Ataya DG, Casas IA (1995). "Safety and tolerance of Lactobacillus reuteri in healthy adult male subjects". Microb Ecol Health Dis. 8 (2): 41–50. doi:10.3109/08910609509141381.
  26. 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.
  27. Abrahamsson T, Jakobsson T, Sinkiewicz G, Fredriksson M, Björkstén B (2005). "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. S2CID 71355253.
  28. Durchschein F, Petritsch W, Hammer HF (2016). "Diet therapy for inflammatory bowel diseases: The established and the new". World J Gastroenterol (Review). 22 (7): 2179–94. doi:10.3748/wjg.v22.i7.2179. PMC 4734995. PMID 26900283.
  29. Boyle RJ, Robins-Browne RM, Tang ML (2006). "Probiotic use in clinical practice: what are the risks?". Am J Clin Nutr (Review). 83 (6): 1256–64, quiz 1446–7. doi:10.1093/ajcn/83.6.1256. PMID 16762934.
  30. Doron S, Snydman DR (2015). "Risk and safety of probiotics". Clin Infect Dis (Review). 60 Suppl 2: S129–34. doi:10.1093/cid/civ085. PMC 4490230. PMID 25922398.
  31. Singhi SC, Kumar S (2016). "Probiotics in critically ill children". F1000Res (Review). 5: 407. doi:10.12688/f1000research.7630.1. PMC 4813632. PMID 27081478.
  32. Urbańska M, Gieruszczak-Białek D, Szajewska H (May 2016). "Systematic review with meta-analysis: Lactobacillus reuteri DSM 17938 for diarrhoeal diseases in children". Aliment Pharmacol Ther. 43 (10): 1025–34. doi:10.1111/apt.13590. PMID 26991503.
  33. 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.
  34. 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.
  35. 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.
  36. 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.
  37. 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.
  38. 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. S2CID 25182003.
  39. 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.
  40. 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. S2CID 3809924.
  41. 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. S2CID 26126920.
  42. 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. S2CID 2306025.
  43. 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. S2CID 207164055.
  44. 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". Kansenshogaku Zasshi. 81 (4): 387–93. doi:10.11150/kansenshogakuzasshi1970.81.387. PMID 17695792.
  45. 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): 407–13. doi:10.1097/MCG.0000000000000007. PMID 24296423. S2CID 25834848.
  46. 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. S2CID 28856447.
  47. 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.
  48. 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.
  49. 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. S2CID 1103712.
  50. 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.
  51. 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.
  52. 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.
  53. 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.
  54. 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.
  55. 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. doi:10.1128/IAI.65.10.4165-4172.1997. PMC 175599. PMID 9317023.
  56. Barnes JH (1993). "Evaluating poult growth and productivity during brooding". Turkeys. 41: 23–4.
  57. Casas IA, Edens FW, Parkhurst CR, Dobrogosz WJ (1998). "Probiotic treatment with Lactobacillus reuteri protects commercial turkeys from avian growth depression". Biosci Microflora. 17 (2): 141–7. doi:10.12938/bifidus1996.17.141.
  58. 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.
  59. 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 (2): 133–9. doi:10.12938/bifidus1996.17.133.
  60. 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.
  61. 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. PMC 5102250. PMID 27315483.
  62. 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.
  63. 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. S2CID 37579834.
  64. 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.
This article is issued from Wikipedia. The text is licensed under Creative Commons - Attribution - Sharealike. Additional terms may apply for the media files.