Cite Score:
0.7
CITE SCORE SCOPUS

Effect of Overgrowth or Decrease in Gut Microbiota on Health and Disease

AUTHORS

Farshad Nojoomi 1 , Abdolmajid Ghasemian 1 , *

1 Microbiology Department, Faculty of medicine, Aja University of Medical Sciences, Tehran, IR Iran

How to Cite: Nojoomi F, Ghasemian A. Effect of Overgrowth or Decrease in Gut Microbiota on Health and Disease, Arch Pediatr Infect Dis. 2016 ; 4(2):e34558. doi: 10.5812/pedinfect.34558.

ARTICLE INFORMATION

Archives of Pediatric Infectious Diseases: 4 (2); e34558
Published Online: April 16, 2016
Article Type: Review Article
Received: November 9, 2015
Revised: January 3, 2016
Accepted: January 12, 2016
Crossmark

Crossmark

CHEKING

READ FULL TEXT
Abstract

Context: The composition and function of the gut microbiota develop with their host from birth. The human microbiome, especially the gut microbiota, plays a critical role in a myriad of health and normal activities. However, the increase or decrease in number of gut bacteria may cause several disorders. This review aimed to assess the importance of human gut microflora and their roles in the health and possible diseases caused by fluctuations in the number of these bacteria.

Evidence Acquisition: For the current review, we searched for the terms “bacterial gut flora”, “role,” “number,” and “increase” and “decrease” on the Google scholar, PubMed, Science Direct, SciVerse, and Scopus search engines and databases. The exclusion criteria were “genetic factors,” “veterinary flora,” “protozoal flora,” “mold,” “fungal,” and “yeast flora”.

Results: The gut microbiota is accompanied by the regulation of several host metabolic pathways, giving rise to interactive host-microbiota signaling, metabolic, and immune-inflammatory responses that physiologically connect the gut, muscle, liver, and brain. A more thorough understanding of these axes is an early essential for reaching therapeutic strategies to use the gut microbiota for combating disease and improving health. Bacterial species of Bacteroides, Clostridia, and Bifidobacterium consist of a large proportion of the gut bacterial flora. Increase in the proportion of these genera in the gut could cause abscess formation, sepsis, inflammatory bowel disease (IBD), Crohn’s disease, toxicity, infection, and malnutrition. However, the decrease in the proportion of these species is accompanied by allergies in infants, inflammation, malabsorption syndrome, carbohydrate/fiber intolerance, atopic eczema, and IBD.

Conclusions: The results showed that although the human gut microbiome plays a pivotal role in health in a normal concentration, fluctuation in their number (increase or decrease) is a possible factor in the appearance of major diseases.

Keywords

Gut Flora Health Clinical Disorders

Copyright © 2016, Pediartric Infections Research Center. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.

1. Context

The composition and function of the gut microbiota develop with their host from birth. The human microbiome, particularly the gut microbiota, plays a critical role in a myriad of health and normal activities (1). These include immune system function and prohibition of pathogen propagation, nutrition, and several other health-related situations (2). However, the increase in the number of gut bacteria may cause several disorders. There is an interplay that depends on the host genetics, nutrition, and lifestyle (3). The gut microbiota is extremely diverse, varies between individuals, and may fluctuate over time, such as during disease and early development (4). The gut microbiota is accompanied by the regulation of several host metabolic pathways, giving rise to interactive host-microbiota signaling, and metabolic and immune-inflammatory responses that physiologically connect the gut, muscle, liver, and brain. A more thorough understanding of these axes is an early essential for reaching therapeutic strategies to use the gut microbiota for combating disease and improving health (1).

2. Evidence Acquisition

For the current review, we identified studies using the search terms “bacterial gut flora,” “role,” “number,” “increase” and “decrease,” and “health” on the Google scholar, PubMed, Science Direct, SciVerse, and Scopus databases and search engines. We tried to include abstracts from conferences as well.

The terms “genetic factors,” “veterinary flora,” “protozoal flora,” “mold,” “fungal,” and “yeast flora” were used as the exclusion criteria. Among the results, publications published from 1997 to 2015 were selected and used for data collection.

3. Results

The most numerous gut bacterial flora include of different species of Bacteroides, Clostridia, Bifidobacterium, and non-pathogenic Enterobactereaceae. The increase in number of these genera could cause abscess formation, sepsis, inflammatory bowel disease (IBD), Crohn’s disease, toxicity, infection and malnutrition (5-8). However, a decrease in the number of these bacteria is accompanied by allergies in infants, inflammation, malabsorption syndrome, carbohydrate/fiber intolerance, atopic eczema, and IBD. This review was performed with the aim of assessing the importance of bacteria in the human gut and to determine their roles in health and possible diseases due to fluctuations in the bacterial populations. Tables 1 and 2 describe the functions and effects of gut bacterial flora under healthy and diseased conditions. Tables 1 and 2 (9-37) describe the roles of some important gut bacteria and their effects on health and disease.

Table 1. [Part 1] Approximate Number and Normal Roles of Gut Bacteria
Bacterial GenusNumber/gNormal Effects/Roles
Bacteroides1010 - 11Vitamin production; barrier; production of carcinogens; immune activation and modulation; Paneth cell protein production; degrading and de-conjugation of bile acids; production of biotin, cobalamin, folic acid (5, 6), pantothenic acid, pyridoxine, and riboflavin; E coli sepsis
Bifidobacterium103 - 4Hydrolysis of (7), barrier, liver damage, cancer, immune activation and modulation, anti-allergic, metabolism of xenobiotics/toxins, degradation of N-nitrosamines, degradation of polycyclic aromatic hydrocarbons, generating a Th2 cell population, sepsis by E. coli (8, 9)
Escherichia coli102 - 103Diarrhea, barrier impeding the growth of pathogens, degradation of N-nitrosamines and polycyclic aromatic amines and N-hydroxyl aryl amines, reduction of blood (10) ammonia levels and reversal of MHE , reduction of endotoxemia, improvement of liver functions
Enterococcus102Immune modulation, inhibition of pathogens and opportunistic species, attachment to epithelial cells, IBD prevention and treatment (11, 12)
Table 1. [Part 2] Approximate Number and Normal Roles of Gut Bacteria
Bacterial GenusNumber/gNormal Effects/Roles
Lactobacillus102 - 3Blockage of adherence receptors, prevention of colon cancer, produce organic acids, production of H202, degradation of N-nitrosamines, anti-tumor glycopeptides, stimulating balanced immune responses, prevention of food allergy in infants, reduction in blood (13) ammonia levels and reversal of MHE, suppression of the expression of proinflammatory cytokines IL-6 and IL-17 and promotion of the expression of the major tight junction proteins claudin-1 and occludin (14), bacteriocin production (15)
Streptococcus103 - 104Fermentation of sugars and lactic acid production (16), barrier function
PeptococcusNDImmune modulation
PeptostreptococcusNDImmune modulation, short-chain fatty acids
RuminococcusNDBlockage of adherence receptors, sulfur degradation, gut barrier protection (17), anti-inflammatory effects (18)
Clostridia104Vitamin production, degradation of proteins and polysaccharides, anti-inflammatory effects (18)
MicrococcusNDBarrier function, short-chain fatty acids
VeillonellaNDPropionic acid from lactic acid; NO production; anti-inflammatory properties; production of biotin, cobalamin, folic acid, pantothenic acid, pyridoxine, and riboflavin (19)
Proteus102Inhibition of pathogen attachment
Eubacterium102 - 103Short-chain fatty acids, anti-inflammatory properties, metabolism of xenobiotics/toxins, prevention of colonization by pathogens, conversion of dietary flavonoids to active aglycones
Fusobacterium102Prevention of colonization by pathogens, propionic acid

Abbreviation: ND, not detected.

Table 2. [Part 1] Effects of Overgrowth and Decrease in the Gut Bacterial Species on Health and Disease Conditions
Bacteria GenusEffect of OvergrowthEffect of Decrease
BacteroidesBacteroides infections, capsule, abscess formation, sepsis, inflammatory bowel disease (IBD), Crohn’s disease (20), achlorhydria/hypochlorhydria, malnutrition, auto-immune disorders, disruption of cellular adhesion molecules by proteases (21)Inflammation, IBD, Crohn’s disease, malabsorption syndromes (22)
BifidobacteriumCancer: colon/breast inflammatory bowel disease, irritable bowel syndrome, achlorhydria/hypochlorhydria, malnutrition, autoimmune disorders, increased paracellular permeability, colorectal cancer (CRC) (23)Allergies in infants, inflammation, malabsorption syndrome, carbohydrate/fiber intolerance, atopic eczema, IBD (22), Crohn’s disease (22), obesity (24), visceral hypersensitivity, contractile hyper-responsiveness, intestinal permeability, and inflammation (14)
E. coliIntestinal giardiasis, malnutrition, vitamin B12 deficiency, impaired formation of micelles, bile salt dehydroxylation, formation of hydroxy fatty acids (25), bile salt deconjugation, increased colonic water secretion, inhibited monosaccharide transport, inhibition of folate conjugases, increased fecal nitrogen, hypoalbuminemia Lamina propria: Increased mononuclear cells, mucosal damage by bacterial enzymes, loss of brush border, endotoxemia/antigenemia Liver damage Joint disease, cystic acne: endotoxemia, ulcerative colitis, colorectal cancer (CRC), increased paracellular permeability, Crohn’s disease, intestinal inflammatory disorders (26), obesity, eczema (1)Inflammation
Table 2. [Part 2] Effects of Overgrowth and Decrease in the Gut Bacterial Species on Health and Disease Conditions
Bacteria GenusEffect of OvergrowthEffect of Decrease
EnterococciRheumatoid arthritis, formation of hydroxy fatty acids Bile salt deconjugation, increased colonic water secretion Inhibition of monosaccharide transport, mucosal damage by bacterial enzymes Loss of brush borderAtopic eczema, lower gut flora, health of pet rabbits (27)
LactobacilliIntestinal giardiasis, vitamin B12 deficiency bile salt dehydroxylation, impaired formation of micelles, Formation of hydroxy fatty acids Bile salt deconjugation, Increase colonic water secretion, inhibition of monosaccharide transport, inhibition of folate conjugases, increased fecal nitrogen, hypoalbuminemia Lamina propria: Increased mononunuclear cells, mucosal damage by bacterial enzymes Loss of brush border, severe decrease in pH (28)Atopic eczema, IBD (34), visceral hypersensitivity, contractile hyper-responsiveness, intestinal permeability, and inflammation (14)
StreptococcusIntestinal giardiasis; high levels of lactic acid, plasma diamine oxidase (DAO), and D-lactate; chitosan and chitooligosaccharide degradation (29)Inflammation and pathogen growth (23)
Table 2. [Part 3] Effects of Overgrowth and Decrease in the Gut Bacterial Species on Health and Disease Conditions
Bacteria GenusEffect of OvergrowthEffect of Decrease
CorynebacteriumAcneInflammation
EubacteriumMalnutrition, achlorhydria/hypochlorhydria, sepsis, IBD, diverticulosis, autoimmune disorders, inflammation from complement or cytokine cascades, Crohn’s disease, hyperlipidemia, hypertension, disruption of cellular adhesion molecules by proteases (30, 31)Carbohydrate/fiber intolerance, malabsorption syndrome, fatigue and maldigestion (32)
FusobacteriumEndotoxemia/antigenemia Liver damage Joint disease, autoimmune disorders, inflammation from complement or cytokine cascades, Crohn’s disease, hyperlipidemia, hypertension (33)Inflammation and infection, tumorigenesis (32, 34)
ProteusRheumatoid arthritis (RA), cystic acne: endotoxemia, atopic eczema,-
RuminococcusColorectal cancer (CRC)Decreased sulfur metabolism (23)
ClostridiumToxicity and infectionDigestive system infections, T2D, allergy sensitization (1)
VeillonellaEndotoxin lipopolysaccharide (35)High lactic acid, low NO production for pathogen inhibition
PrevotellaAttachment, degradation of chitosan and chitooligosaccharideInflammation and infection (36, 37)

Several studies have determined that obesity is associated with an increase in the phylum Firmicutes and a relatively lower abundance of the phylum Bacteroidetes (38-41). Research into Crohn’s disease has revealed that patients with Crohn’s disease exhibit a significant reduction in the overall diversity of the gut microbiota (42, 43) and changes in microbial composition (44). A study on type 2 diabetes (T2D) showed that the proportions of the phylum Firmicutes and the class Clostridia in the gut of patients was significantly reduced among patients with T2D (45).

In addition, acidification of colonic secretions attenuates the absorption of ammonia by non-ionic diffusion. Treatment with fermentable fiber alone has also been reported to be beneficial. There is a risk of fecal carriage of fluoroquinolone-resistant strains (46). Moreover, high levels of genetic flux may occur between gram-negative Enterobacteriaceae (47). The intestinal microbial communities are actively regulated by epithelial Paneth cells via their secretion of antimicrobial peptides or α-defensins. α-Defensins can selectively kill non-commensals while increasing the growth of commensals. A study showed that Paneth cells targeted by graft-versus-host disease (GVHD) resulted in increased Escherichia coli growth and septicemia (48). On the other hand, various perioperative treatments were found to affect the number and proportion of gut flora in SD rats (49).

4. Conclusions

The results showed that although the human gut bacterial species play a pivotal role in health, immunity, and nutrition in normal concentrations in the intestine, fluctuations in their number (increase or decrease) is a possible factor in the appearance of major health disorders. Furthermore, gut microflora induce disease even in the normal state, for instance inflammation and invasion of the epithelium may occur. Several factors such as age, hormonal changes, and immune suppression are among the major factors causing the disorders in the gut microbial population.

Footnotes

References

  • 1.

    Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM, Cusack S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012; 488(7410) : 178 -84 [DOI][PubMed]

  • 2.

    Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009; 9(5) : 313 -23 [DOI][PubMed]

  • 3.

    Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. Host-gut microbiota metabolic interactions. Science. 2012; 336(6086) : 1262 -7 [DOI][PubMed]

  • 4.

    Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012; 489(7415) : 220 -30 [DOI][PubMed]

  • 5.

    Toprak NU, Yagci A, Gulluoglu BM, Akin ML, Demirkalem P, Celenk T, et al. A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer. Clin Microbiol Infect. 2006; 12(8) : 782 -6 [DOI][PubMed]

  • 6.

    Comstock LE. Importance of glycans to the host-bacteroides mutualism in the mammalian intestine. Cell Host Microbe. 2009; 5(6) : 522 -6 [DOI][PubMed]

  • 7.

    van den Broek LA, Hinz SW, Beldman G, Vincken JP, Voragen AG. Bifidobacterium carbohydrases-their role in breakdown and synthesis of (potential) prebiotics. Mol Nutr Food Res. 2008; 52(1) : 146 -63 [DOI][PubMed]

  • 8.

    Collado MC, Gueimonde M, Hernandez M, Sanz Y, Salminen S. Adhesion of selected Bifidobacterium strains to human intestinal mucus and the role of adhesion in enteropathogen exclusion. J Food Prot. 2005; 68(12) : 2672 -8 [PubMed]

  • 9.

    Xing HC, Li LJ, Xu KJ, Shen T, Chen YB, Sheng JF, et al. Protective role of supplement with foreign Bifidobacterium and Lactobacillus in experimental hepatic ischemia-reperfusion injury. J Gastroenterol Hepatol. 2006; 21(4) : 647 -56 [DOI][PubMed]

  • 10.

    Yanagisawa N, Haruta I, Shimizu K, Furukawa T, Higuchi T, Shibata N, et al. Identification of commensal flora-associated antigen as a pathogenetic factor of autoimmune pancreatitis. Pancreatology. 2014; 14(2) : 100 -6 [DOI][PubMed]

  • 11.

    Clarke G, Cryan JF, Dinan TG, Quigley EM. Review article: probiotics for the treatment of irritable bowel syndrome--focus on lactic acid bacteria. Aliment Pharmacol Ther. 2012; 35(4) : 403 -13 [DOI][PubMed]

  • 12.

    Saez-Lara MJ, Gomez-Llorente C, Plaza-Diaz J, Gil A. The role of probiotic lactic acid bacteria and bifidobacteria in the prevention and treatment of inflammatory bowel disease and other related diseases: a systematic review of randomized human clinical trials. Biomed Res Int. 2015; 2015 : 505878 [DOI][PubMed]

  • 13.

    Zarrati M, Salehi E, Mofid V, Hossein Zadeh-Attar MJ, Nourijelyani K, Bidad K, et al. Relationship between probiotic consumption and IL-10 and IL-17 secreted by PBMCs in overweight and obese people. Iran J Allergy Asthma Immunol. 2013; 12(4) : 404 -6 [PubMed]

  • 14.

    Wang H, Gong J, Wang W, Long Y, Fu X, Fu Y, et al. Are there any different effects of Bifidobacterium, Lactobacillus and Streptococcus on intestinal sensation, barrier function and intestinal immunity in PI-IBS mouse model? PLoS One. 2014; 9(3)[DOI][PubMed]

  • 15.

    Nezhad M, Amin S, Tajabadi Ebrahimi M, Zilabi R. The Effect of Iran Probiotic Fermented Milk Beverage on Cholesterol and Liver Function Biomarkers of Rat. J Police Med. 2015; 4(1) : 49 -56

  • 16.

    van den Bogert B, Erkus O, Boekhorst J, de Goffau M, Smid EJ, Zoetendal EG, et al. Diversity of human small intestinal Streptococcus and Veillonella populations. FEMS Microbiol Ecol. 2013; 85(2) : 376 -88 [DOI][PubMed]

  • 17.

    Rao RK, Samak G. Protection and Restitution of Gut Barrier by Probiotics: Nutritional and Clinical Implications. Curr Nutr Food Sci. 2013; 9(2) : 99 -107 [PubMed]

  • 18.

    Hakansson A, Molin G. Gut microbiota and inflammation. Nutrients. 2011; 3(6) : 637 -82 [DOI][PubMed]

  • 19.

    Kianifar HR, Farid R, Ahanchian H, Jabbari F, Moghiman T, Sistanian A. Probiotics in the treatment of acute diarrhea in young children. Iran J Med Sci. 2015; 34(3) : 204 -7

  • 20.

    Favier C, Neut C, Mizon C, Cortot A, Colombel JF, Mizon J. Fecal beta-D-galactosidase production and Bifidobacteria are decreased in Crohn's disease. Dig Dis Sci. 1997; 42(4) : 817 -22 [PubMed]

  • 21.

    Sanchez E, Laparra JM, Sanz Y. Discerning the role of Bacteroides fragilis in celiac disease pathogenesis. Appl Environ Microbiol. 2012; 78(18) : 6507 -15 [DOI][PubMed]

  • 22.

    Marteau P, Lepage P, Mangin I, Suau A, Dore J, Pochart P, et al. Review article: gut flora and inflammatory bowel disease. Aliment Pharmacol Ther. 2004; 20 Suppl 4 : 18 -23 [DOI][PubMed]

  • 23.

    Wang T, Cai G, Qiu Y, Fei N, Zhang M, Pang X, et al. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 2012; 6(2) : 320 -9 [DOI][PubMed]

  • 24.

    Eriguchi Y, Takashima S, Oka H, Shimoji S, Nakamura K, Uryu H, et al. Graft-versus-host disease disrupts intestinal microbial ecology by inhibiting Paneth cell production of alpha-defensins. Blood. 2012; 120(1) : 223 -31 [DOI][PubMed]

  • 25.

    Ashok S, Sankaranarayanan M, Ko Y, Jae KE, Ainala SK, Kumar V, et al. Production of 3-hydroxypropionic acid from glycerol by recombinant Klebsiella pneumoniae DeltadhaTDeltayqhD which can produce vitamin B(1)(2) naturally. Biotechnol Bioeng. 2013; 110(2) : 511 -24 [DOI][PubMed]

  • 26.

    Winter SE, Winter MG, Xavier MN, Thiennimitr P, Poon V, Keestra AM, et al. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science. 2013; 339(6120) : 708 -11 [DOI][PubMed]

  • 27.

    Benato L, Hastie P, O'Shaughnessy P, Murray JA, Meredith A. Effects of probiotic Enterococcus faecium and Saccharomyces cerevisiae on the faecal microflora of pet rabbits. J Small Anim Pract. 2014; 55(9) : 442 -6 [DOI][PubMed]

  • 28.

    Davati N, Tabatabaee Yazdi F, Zibaee S, Shahidi F, Edalatian MR. Study of Lactic Acid Bacteria Community From Raw Milk of Iranian One Humped Camel and Evaluation of Their Probiotic Properties. Jundishapur J Microbiol. 2015; 8(5)[DOI][PubMed]

  • 29.

    Koppova I, Bures M, Simunek J. Intestinal bacterial population of healthy rats during the administration of chitosan and chitooligosaccharides. Folia Microbiol (Praha). 2012; 57(4) : 295 -9 [DOI][PubMed]

  • 30.

    Roytio H, Ouwehand AC. The fermentation of polydextrose in the large intestine and its beneficial effects. Benef Microbes. 2014; 5(3) : 305 -13 [DOI][PubMed]

  • 31.

    Damms-Machado A, Mitra S, Schollenberger AE, Kramer KM, Meile T, Konigsrainer A, et al. Effects of surgical and dietary weight loss therapy for obesity on gut microbiota composition and nutrient absorption. Biomed Res Int. 2015; 2015 : 806248 [DOI][PubMed]

  • 32.

    Biagi E, Nylund L, Candela M, Ostan R, Bucci L, Pini E, et al. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One. 2010; 5(5)[DOI][PubMed]

  • 33.

    Allen-Vercoe E. Fusobacterium varium in ulcerative colitis: is it population-based? Dig Dis Sci. 2015; 60(1) : 7 -8 [DOI][PubMed]

  • 34.

    Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 2013; 14(2) : 207 -15 [DOI][PubMed]

  • 35.

    Ginsburg I, Lahav M. How are bacterial cells degraded by leukocytes in vivo? An enigma. Clin Immunol Newsletter. 1983; 4(11) : 147 -53

  • 36.

    Liu Q, Duan ZP, Ha DK, Bengmark S, Kurtovic J, Riordan SM. Synbiotic modulation of gut flora: effect on minimal hepatic encephalopathy in patients with cirrhosis. Hepatology. 2004; 39(5) : 1441 -9 [DOI][PubMed]

  • 37.

    Sudo N, Sawamura S, Tanaka K, Aiba Y, Kubo C, Koga Y. The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J Immunol. 1997; 159(4) : 1739 -45 [PubMed]

  • 38.

    Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009; 457(7228) : 480 -4 [DOI][PubMed]

  • 39.

    Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004; 101(44) : 15718 -23 [DOI][PubMed]

  • 40.

    Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005; 102(31) : 11070 -5 [DOI][PubMed]

  • 41.

    Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009; 106(7) : 2365 -70 [DOI][PubMed]

  • 42.

    Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut. 2006; 55(2) : 205 -11 [DOI][PubMed]

  • 43.

    Ghasemian A, Najar-Peerayeh S, Bakhshi B, Mirzaee M. High Prevalence of icaABCD Genes Responsible for Biofilm Formation in Clinical Isolates of Staphylococcus aureus From Hospitalized Children. Arch Pediatr Infect Dis. 2015; 3(3)

  • 44.

    Joossens M, Huys G, Cnockaert M, De Preter V, Verbeke K, Rutgeerts P, et al. Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives. Gut. 2011; 60(5) : 631 -7 [DOI][PubMed]

  • 45.

    Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012; 490(7418) : 55 -60 [DOI][PubMed]

  • 46.

    Steensels D, Slabbaert K, De Wever L, Vermeersch P, Van Poppel H, Verhaegen J. Fluoroquinolone-resistant E. coli in intestinal flora of patients undergoing transrectal ultrasound-guided prostate biopsy--should we reassess our practices for antibiotic prophylaxis? Clin Microbiol Infect. 2012; 18(6) : 575 -81 [DOI][PubMed]

  • 47.

    Stecher B, Denzler R, Maier L, Bernet F, Sanders MJ, Pickard DJ, et al. Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc Natl Acad Sci U S A. 2012; 109(4) : 1269 -74 [DOI][PubMed]

  • 48.

    Storb R, Gyurkocza B, Storer BE, Maloney DG, Sorror ML, Mielcarek M, et al. Allogeneic hematopoietic cell transplantation following minimal intensity conditioning: predicting acute graft-versus-host disease and graft-versus-tumor effects. Biol Blood Marrow Transplant. 2013; 19(5) : 792 -8 [DOI][PubMed]

  • 49.

    Liu HC, Zhang DZ, Wang DS, Wang ML, Zhou YB. [Effect of different perioperative treatments on gut flora in SD rats]. Zhonghua Wei Chang Wai Ke Za Zhi. 2012; 15(6) : 581 -4 [PubMed]

  • COMMENTS

    LEAVE A COMMENT HERE: