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REVIEW ARTICLE
Year : 2020  |  Volume : 10  |  Issue : 3  |  Page : 99-104

The Effect of Bariatric Surgery on the Composition of the Gut Microbiota Community: an Imbalance Associated with Severe Disorders


1 Faculty of Arts and Sciences, The Holy Spirit University of Kaslik USEK, Lebanon
2 Faculty of Arts and Sciences, The Holy Spirit University of Kaslik, Jounieh, Lebanon
3 Department of surgery, Central Military Hospital, Beirut, Lebanon
4 School of Engineering, The Holy Spirit University of Kaslik, Lebanon

Date of Submission27-Dec-2019
Date of Decision15-Jan-2020
Date of Acceptance05-Mar-2020
Date of Web Publication20-Aug-2020

Correspondence Address:
Elham El Darazi
Faculty of Arts and Sciences, The Holy Spirit University of Kaslik USEK
Lebanon
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijnpnd.ijnpnd_84_19

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   Abstract 


Obesity has become an imminently serious public health problem as nearly 40% of the adult population worldwide is obese. Bariatric surgery is considered the most efficient weight loss treatment by mechanically restricting caloric intake. However, evidence proposes a strong association between weight loss and the alteration of the gut microbial composition after bariatric surgery. Modifications in the concentration of gut microbial bacteria affect human health by either increasing or reducing the likelihood of diseases associated with specific bacteria. In this review, we discuss the effect of bariatric surgery on the gut microbial composition in patients. Additionally, we detail the modifications in the abundance of specific phylum and species in the intestinal microbiota after bariatric surgery. Different disorders associated with the increase or decrease of a particular bacterium are mentioned in order to evaluate the impact of the alteration of post-surgery intestinal microbial structure on individuals’ health.

Keywords: Obesity, bariatric surgery, gut microbiota, bacteria


How to cite this article:
Darazi EE, Sacre Y, El-Khoury E, Abdel Nour AM. The Effect of Bariatric Surgery on the Composition of the Gut Microbiota Community: an Imbalance Associated with Severe Disorders. Int J Nutr Pharmacol Neurol Dis 2020;10:99-104

How to cite this URL:
Darazi EE, Sacre Y, El-Khoury E, Abdel Nour AM. The Effect of Bariatric Surgery on the Composition of the Gut Microbiota Community: an Imbalance Associated with Severe Disorders. Int J Nutr Pharmacol Neurol Dis [serial online] 2020 [cited 2020 Sep 28];10:99-104. Available from: http://www.ijnpnd.com/text.asp?2020/10/3/99/292693




   Introduction Top


Obesity is one of the leading public health concerns worldwide.[1] Bariatric surgery is the most efficient method for weight loss, as it results in dramatic decrease in food intake.[2] Besides the complications and comorbidities developed post-surgery, functional and taxonomic modifications were reported in the gut microbiota. Gut microbiota, which are the microorganisms colonizing the digestive tract, have a major role in the storage of energy and mechanism of obesity.[3],[4],[5] Major modifications in the concentration of particular gut microbiota were described after bariatric surgery.[6]

Obesity

In recent years, the increasing incidence of overweight adults and obesity was described as an epidemic problem.[1],[7] In 2015 the World Health Organization (WHO) estimated 2.3 billion adults were overweight and 700 million obese. WHO defines obesity as an excessive or abnormal fat accumulation with a serious impact on personal health.[8] Body mass index (BMI) was invented as a simple and effective way to define levels of obesity. A healthy BMI ranges from 18.5 to 24.9 kg/m2, overweight from 25 to 29.9 kg/m2, and obese is 30 kg/m2 or greater.[9]

Bariatric surgery

Bariatric surgery is a highly effective therapy for obesity, yielding sustained weight loss, improvement of quality of life and reduction of obesity-related comorbidities and mortality.[10] Three classes of bariatric surgery exist: first, restrictive methods, such as laparoscopic adjustable gastric banding (LAGB), sleeve gastrectomy (SG), and vertical banded gastroplasty (VBG); second, malabsorptive techniques including biliopancreatic diversion (BPD) and jejunoileal bypass (JIB); third, roux-en-Y gastric bypass (RYGB) and duodenal switch (DS) with BPD, which combines restrictive and malabsorptive interventions.[11] Bariatric surgery not only reduces food intake and digestion but also alters food preferences, bile acids (BAs) metabolism and gastric emptying time, allowing an efficient weight loss.[11],[12] Adversely, patients often develop multiple post-surgery complications in the short and long term, ranging from pulmonary embolism and deep venous thrombosis to nutritional deficiencies, marginal ulcers, stromal stenosis, internal hernias, and dumping syndrome.[13]

Gut microbiota

Gut microbiota are enteric microorganisms, numbering almost 15000 species of bacteria in variety, which colonize the intestines.[14] Bacteria are divided into six primary phyla that are the following Proteobacteria, Firmicutes, Bacteroidetes, Verrucomicrobia, Fusobacteria, and Actinobacteria.[15] Bacteriodetes and Firmicutes phyla are the main constituents of the gut microbiota implicated in metabolic, immunological and physiological activity in the human body.[16] Gut microbes are normally beneficial to the host and ensure immune functions,[17] the protection against enteropathogens[18],[19] and the extraction of energy and nutrients from the host’s diet.[20],[21] Multiple factors can alter the symbiotic balance between the host and the gut microbiota, such as malnutrition,[22] neurological diseases,[23] cancer[24] and, most particularly, obesity.[25],[26] Modifications in the intestinal microbiota are responsible for a number of diseases discovered so far such as allergies, type 2 diabetes, and inflammatory bowel diseases.[13],[27]

Gut microbiota after bariatric surgery

Obese patients subjected to bariatric surgery often develop various physiological and behavioral abnormalities. One of those abnormalities is the significant alteration of the complex intestinal microbial composition, which subsequently adapts in order to maintain weight loss.[3],[28] Reduction of food intake, food types, and nutrient malabsorption are the main causes of gut microbial modifications.[2] Moreover, alterations in pH,[29] bile acids,[30],[31] hormones,[32],[33] and serum leptin levels are responsible for modifications of post-surgery gut microbiota diversity.[34],[35],[36] Gut microbiota diversity after bariatric surgery has always been a controversial subject as research results have been limited. Four consistent findings were reported showing that post-surgery gut microbiota benefit from a high diversity based on the Shanon index.[37],[38],[39],[40] Differential intestinal microbiota signatures were identified by comparing the microbiota profile between subjects before and after bariatric surgery. These studies evaluate the impact of weight-loss surgery on the composition of gut microbiota. Most studies to date have focused on RYGB’s influence on the gut microbiota composition and function as it is the most common bariatric surgery, whereas little research has been done concerning other types of bariatric surgery.[4],[37],[40] Due to their role in causing infections or worsening inflammatory diseases, a link between the increased and reduced bacteria in the intestinal microbiota of patients subjected to bariatric surgery and their associated diseases needs to be established. Studies that clinically prove the correlation between post-surgery gut microbial composition, and inflammatory and metabolic diseases are lacking currently.

Primary species of bacteria changes after bariatric surgery

In the late decade, many studies have been conducted in order to profile the gut microbiota after bariatric surgery with the aim of evaluating the impact of bariatric surgery on patients’ health. Research has shown wide changes in microbial composition after bariatric surgery. A number of phyla have been shown to increase after surgery while other types of bacteria decreased. Metagenomic data evaluating the changes before and after RYGB identify 1061 species, 729 genera, and 44 phyla.[41] Palleja et al.[37] also demonstrated the increase in gut microbial diversity after bariatric surgery with an increase in the abundance of 31 species.

Proteobacteria

Proteobacteria known as the “microbial signature” of disease was highly increased after bariatric surgery.[37],[42] While a minor population in healthy gut flora, Proteobacteria populations were shown to be increased post-surgery, especially Enterobacter hormaechei, Salmonella enterica, Enterobacter cancerogenus and Scedosporium boydii.[41],[43] High concentration of Proteobacteria reflects an imbalance in the microbiota representing a diagnostic signature for dysbiosis, which is widely implicated in metabolic disorders.[42] The high concentration of Proteobacteria is also associated with a high risk of diseases such as asthma,[44] inflammatory bowel diseases (IBD),[45] and colorectal carcinomas.[41] Moreover, cystic fibrosis and scedosporiosis can be caused by Scedosporium boydii. These results suggest that a high post-operative concentration of Scedosporium boydii can lead to fatal infections.[46] A common association between Salmonella enterica and a set of invasive and noninvasive infections was reported.[47],[48] Enterobacter cancerogenus can also cause pneumonia, wounds, and bronchial asthma according to a clinical study.[49] Further studies are needed in order to identify the impact of high concentrations of Scedosporium boydii and Enterobacter cancerogenus on post-operative patients’ health.

The number of Gamma Proteobacteria increase after SG,[38] RYGB,[50] and DJB[51] surgeries, and facilitate stabilized postoperative weight loss . Escherichia coli among them, the main cause of childhood diarrhea,[52] could give rise to different diseases including meningitis, wound infections, atherosclerosis, and immunological diseases (rheumatoid arthritis).[37],[53] A high concentration of Escherichia coli not only promotes diarrheal diseases but also threatens patients’ health by adhering to intestinal cells, altering neurological electrolyte transport.[53] Klebsiella pneumoniae, a photogenic strain detrimental to public health, is a potential cause for multiple infectious diseases, such as those of the blood and respiratory and urinary systems. For this reason, a high concentration of Klebsiella pneumonia in obese patients after bariatric surgery is a negative prognostic affecting a patient’s quality of life.[54] Moreover, Shigella Boydii, the main cause of shigellosis or bacillary dysentery,[55],[56] was shown increase after surgery.[4] Citrobacter braakii, which is capable of causing infections as well as bacteremia, was reported as increased after surgery [Table 1].[4],[57]
Table 1 Modifications in gut microbiota composition after bariatric surgery

Click here to view


Firmicutes

A low concentration of Firmicutes was reported to increase the incidence of inflammation and colorectal cancers.[41] Firmicutes’ abundance was reported to decrease after bariatric surgery, especially for Dorea, Anaerostipes caccae, Coprococcus comes, Blautia, and F. prausnitzii.[39],[58] Interestingly, Blautias’ concentration was correlated with a severe clinical stage and histoprognostic grade in subjects with breast cancer, suggesting a role in estrogen metabolism.[59] A low concentration of Blautia in the post-intervention state can be a good prognostic. A case study by Workneh et al.[60] demonstrated Anaerostipes caccae, for the first time identified in 2002, as a cause of infection; the exact effects of a low post-surgery concentration of A. caccae remains unknown. Moreover, the decreased concentration of Coprococcus comes post-bariatric surgery can be a preventive factor since it was defined as one of the causes of Crohn’s disease. A study showed Coprococcus comes may have long-term effects due to its capacity to bind IgG through the Fab portion, which suggests a possible role in Crohn’s disease.[61] The relationship between increases in these bacteria and the progression of inflammatory and metabolic disorders is yet to be studied. It should be noted that a high Firmicutes/Bacteroidetes ratio was detected in obese patients compared to healthy patients, which explains the reduced concentration of Firmicutes after weight-loss surgery.[62],[63]

On the other hand, a significant post-surgery increase of Veillonella parvula (V. parvula) and Veillonella dispar (V. dispar) was demonstrated.[37],[41] V. parvula may contribute to multiples infections such as meningitis, osteomyelitis, endocarditis, peritonitis and sepsis.[64],[65],[66],[67],[68],[69],[70] An increased abundance of V. parvula after surgery may be a serious risk not only because of strong infections, but also its crucial role in causing Epidural abscess, a potentially life-threatening disease.[71] Moreover increased concentration of V. dispar was associated with an increase chance of intestinal infections especially for Crohns’ disease.[72] Likewise, Streptococcus gordonii and Enterococcus faecalis concentrations were found to increase after RYGB significantly impacting patients’ health.[37] As the main cause of thoracic empyema, high level of Streptococcus gordonii can be a risk factor in worsening various infections.[73] Enterococcus faecalis is linked to a set of infections such as meningitis, endocarditis, urinary tract infections, bacteremia, and root canal infections.[74] The post-surgery change of Enterococcus faecalis is indicative of a serious life-threatening risk. In addition, Faecalibacterium prausnitzii, with reduced post-surgeryconcentration, especially after RYBG, was seen as a major factor of inflammation and glucose homeostasis in obese persons.[75] The post-surgery concentration of Clostridia decreased, which is a good prognostic for patients, as it produces a high number of toxins related to dangerous diseases.[76],[77],[78] A reduced concentration of Ruminococcus, which correlates with inflammatory bowel disease, was shown in patients after bariatric surgery.[39],[79] Out of these two phyla, Akkermansia, a microbe with probiotic properties, was increased after bariatric surgery.[77],[80]


   Conclusion Top


Bariatric surgery is the most effective weight loss method for severe obesity. Multiple changes occur in the gut microbiota after surgery. Association between modifications of gut microbial composition and the outcome or disappearance of metabolic and inflammatory illness needs to be empirically established. Specific disease diagnostics and prognostics, along with novel therapeutic strategies, can be developed after such correlations are proven. More clinical studies about the health effect of changes in gut bacteria after bariatric surgery would be helpful.

Contributions

All authors contributed equally to the writing of this article.

Financial support and sponsorship

Nil.

Conflicts of interest

The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.



 
   References Top

1.
Pouwels S, Buise MP, Twardowski P, Stepaniak PS, Proczko M. Obesity surgery and anesthesiology risks: a review of key concepts and related physiology. Obesity Surgery 2019;29:2670-7.  Back to cited text no. 1
    
2.
Peat CM, Kleiman SC, Bulik CM, Carroll IM. The intestinal microbiome in bariatric surgery patients. Eur Eat Disord Rev 2015;23:496-503. PubMed PMID: 26426680. Pubmed Central PMCID: PMC5022764. Epub 2015/10/02.  Back to cited text no. 2
    
3.
Anhe FF, Varin TV, Schertzer JD, Marette A. The gut microbiota as a mediator of metabolic benefits after bariatric surgery. Can J Diabetes 2017;41:439-47. PubMed PMID: 28552651. Epub 2017/05/30.  Back to cited text no. 3
    
4.
Tremaroli V, Karlsson F, Werling M, Stahlman M, Kovatcheva-Datchary P, Olbers T et al. Roux-en-Y gastric bypass and vertical banded gastroplasty induce long-term changes on the human gut microbiome contributing to fat mass regulation. Cell Metab 2015;22:228-38. PubMed PMID: 26244932. Pubmed Central PMCID: PMC4537510. Epub 2015/08/06.  Back to cited text no. 4
    
5.
Liou AP, Paziuk M, Luevano JM Jr., Machineni S, Turnbaugh PJ, Kaplan LM. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med 2013;5:178ra41. PubMed PMID: 23536013. Pubmed Central PMCID: PMC3652229. Epub 2013/03/29.  Back to cited text no. 5
    
6.
Campisciano G, Palmisano S, Cason C, Giuricin M, Silvestri M, Guerra M et al. Gut microbiota characterisation in obese patients before and after bariatric surgery. Benef Microbes. 2018;9:367-73. PubMed PMID: 29482339. Epub 2018/02/28.  Back to cited text no. 6
    
7.
Haslam DW, James WP. Obesity. Lancet 2005;366:1197-209. PubMed PMID: 16198769. Epub 2005/10/04.  Back to cited text no. 7
    
8.
WHO. WHO | Obesity. 2015; Available at https://www.who.int/topics/obesity/en/.  Back to cited text no. 8
    
9.
Morais SS, Ide M, Morgan AM, Surita FG. A novel body mass index reference range − an observational study. Clinics (Sao Paulo) 2017;72:698-707. PubMed PMID: 29236917. Pubmed Central PMCID: PMC5706065. Epub 2017/12/14.  Back to cited text no. 9
    
10.
Benaiges D, Goday A, Pedro-Botet J, Más A, Chillarón JJ, Flores-Le Roux JA. Bariatric surgery: to whom and when? Minerva Endocrinologica 2015;40:119-28.  Back to cited text no. 10
    
11.
Quercia I, Dutia R, Kotler DP, Belsley S, Laferrère B. Gastrointestinal changes after bariatric surgery. Diabetes & Metabolism 2014;40:87-94.  Back to cited text no. 11
    
12.
Ulker İ, Yildiran H. The effects of bariatric surgery on gut microbiota in patients with obesity: a review of the literature. Biosci Microbiota Food Health 2019;38:3-9.  Back to cited text no. 12
    
13.
Patel RM, Denning PW. Intestinal microbiota and its relationship with necrotizing enterocolitis. Pediatr Res 2015;78:232-8. eng.  Back to cited text no. 13
    
14.
Mangiola F, Ianiro G, Franceschi F, Fagiuoli S, Gasbarrini G, Gasbarrini A. Gut microbiota in autism and mood disorders. World Journal of Gastroenterology 2016;22:361-8.  Back to cited text no. 14
    
15.
Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature 2012;489:220-30.  Back to cited text no. 15
    
16.
Ottman N, Smidt H, de Vos WM, Belzer C. The function of our microbiota: who is out there and what do they do? Frontiers in Cellular and Infection Microbiology 2012;2.  Back to cited text no. 16
    
17.
Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science (New York, NY) 2012;336:489-93. eng.  Back to cited text no. 17
    
18.
Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 2011;469:543-7. eng.  Back to cited text no. 18
    
19.
Candela M, Perna F, Carnevali P, Vitali B, Ciati R, Gionchetti P et al. Interaction of probiotic lactobacillus and bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol 2008;125:286-92. eng.  Back to cited text no. 19
    
20.
Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222-7. eng.  Back to cited text no. 20
    
21.
Sonnenburg JL, Xu J, Leip DD, Chen C-H, Westover BP, Weatherford J et al. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science (New York, NY). 2005;307:1955-9. eng.  Back to cited text no. 21
    
22.
Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature 2011;474:327-36. eng.  Back to cited text no. 22
    
23.
Gonzalez A, Stombaugh J, Lozupone C, Turnbaugh PJ, Gordon JI, Knight R. The mind-body-microbial continuum. Dialogues Clin Neurosci 2011 2011;13:55-62. eng.  Back to cited text no. 23
    
24.
Lupton JR. Microbial degradation products influence colon cancer risk: the butyrate controversy. J Nutr 2004;134:479-82. eng.  Back to cited text no. 24
    
25.
Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host & Microbe. 2008;3:213-23. eng.  Back to cited text no. 25
    
26.
Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 2006;444:1022-3. eng.  Back to cited text no. 26
    
27.
Daher MI, Matta JM, Abdel Nour AM. Non-nutritive sweeteners and type 2 diabetes: Should we ring the bell? Diabetes Res Clin Pract 2019;19;155:107786. PubMed PMID: 31326455. Epub 2019/07/22.  Back to cited text no. 27
    
28.
Furet J-P, Kong L-C, Tap J, Poitou C, Basdevant A, Bouillot J-L et al. Differential adaptation of human gut microbiota to bariatric surgery–induced weight loss. Diabetes 2010;59:3049-57.  Back to cited text no. 28
    
29.
Murphy R, Tsai P, Jüllig M, Liu A, Plank L, Booth M. Differential changes in gut microbiota after gastric bypass and sleeve gastrectomy bariatric surgery vary according to diabetes remission. Obesity Surgery 2017;27:917-25. eng.  Back to cited text no. 29
    
30.
Santacruz A, Marcos A, Wärnberg J, Martí A, Martin-Matillas M, Campoy C et al. Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity (Silver Spring, Md) 2009;17:1906-15. eng.  Back to cited text no. 30
    
31.
Islam KBMS, Fukiya S, Hagio M, Fujii N, Ishizuka S, Ooka T et al. Bile acid is a host factor that regulates the composition of the cecal microbiota in rats. Gastroenterology 2011;141:1773-81. eng.  Back to cited text no. 31
    
32.
Ravussin Y, Koren O, Spor A, LeDuc C, Gutman R, Stombaugh J et al. Responses of gut microbiota to diet composition and weight loss in lean and obese mice. Obesity (Silver Spring, Md) 2012;20:738-47. eng.  Back to cited text no. 32
    
33.
Cani PD, Delzenne NM. Interplay between obesity and associated metabolic disorders: new insights into the gut microbiota. Curr Opin Pharmacol 2009;9:737-43. PubMed PMID: 19628432. Epub 2009/07/25.  Back to cited text no. 33
    
34.
Arrieta M-C, Stiemsma LT, Amenyogbe N, Brown EM, Finlay B. The intestinal microbiome in early life: health and disease. Frontiers in Immunology 2014;5:427. eng.  Back to cited text no. 34
    
35.
Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA. 2005;102:11070-5. eng.  Back to cited text no. 35
    
36.
Khan MJ, Gerasimidis K, Edwards CA, Shaikh MG. Role of gut microbiota in the aetiology of obesity: proposed mechanisms and review of the literature. Journal of Obesity 2016;2016:7353642. eng.  Back to cited text no. 36
    
37.
Palleja A, Kashani A, Allin KH, Nielsen T, Zhang C, Li Y et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Medicine 2016;8.  Back to cited text no. 37
    
38.
Basso N, Soricelli E, Castagneto-Gissey L, Casella G, Albanese D, Fava F et al. Insulin resistance, microbiota, and fat distribution changes by a new model of vertical sleeve gastrectomy in obese rats. Diabetes 2016;65:2990-3001. en.  Back to cited text no. 38
    
39.
Patrone V, Vajana E, Minuti A, Callegari ML, Federico A, Loguercio C et al. Postoperative changes in fecal bacterial communities and fermentation products in obese patients undergoing bilio-intestinal bypass. Frontiers in Microbiology 2016;7:200. eng.  Back to cited text no. 39
    
40.
Guo Y, Liu C-Q, Shan C-X, Chen Y, Li H-H, Huang Z-P et al. Gut microbiota after Roux-en-Y gastric bypass and sleeve gastrectomy in a diabetic rat model: Increased diversity and associations of discriminant genera with metabolic changes. Diabetes Metab Res Rev 2017;33. eng.  Back to cited text no. 40
    
41.
Graessler J, Qin Y, Zhong H, Zhang J, Licinio J, Wong ML et al. Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: correlation with inflammatory and metabolic parameters. The Pharmacogenomics Journal 2013;13:514-22. en.  Back to cited text no. 41
    
42.
Shin N-R, Whon TW, Bae J-W. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 2015;33:496-503. eng.  Back to cited text no. 42
    
43.
Li JV, Ashrafian H, Bueter M, Kinross J, Sands C, le Roux CW et al. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut 2011;60:1214-23. eng.  Back to cited text no. 43
    
44.
Marri PR, Stern DA, Wright AL, Billheimer D, Martinez FD. Asthma-associated differences in microbial composition of induced sputum. The Journal of Allergy and Clinical Immunology 2013;131:346-52.e1-3.  Back to cited text no. 44
    
45.
Frank DN, St. Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 2007;104:13780-5.  Back to cited text no. 45
    
46.
Bernhardt A, Seibold M, Rickerts V, Tintelnot K. Cluster analysis of Scedosporium boydii infections in a single hospital. International Journal of Medical Microbiology 2015;305:724-8.  Back to cited text no. 46
    
47.
Wagner C, Hensel M. Adhesive Mechanisms of Salmonella enterica. In: Linke D, Goldman A, editors. Bacterial Adhesion: Chemistry, Biology and Physics. Dordrecht: Springer Netherlands 2011. p. 17-34.  Back to cited text no. 47
    
48.
Kwambana-Adams B, Darboe S, Nabwera H, Foster-Nyarko E, Ikumapayi UN, Secka O et al. Salmonella Infections in The Gambia, 2005–2015. Clinical Infectious Diseases 2015;61:S354-S62. en.  Back to cited text no. 48
    
49.
Demir T, Baran G, Buyukguclu T, Sezgin FM, Kaymaz H. Pneumonia due to Enterobacter cancerogenus infection. Folia Microbiol 2014;59:527-30. en.  Back to cited text no. 49
    
50.
Shao Y, Ding R, Xu B, Hua R, Shen Q, He K et al. Alterations of gut microbiota after Roux-en-Y gastric bypass and sleeve gastrectomy in Sprague-Dawley rats. Obesity Surgery 2017;27:295-302. eng.  Back to cited text no. 50
    
51.
Kashihara H, Shimada M, Yoshikawa K, Higashijima J, Nakao T, Nishi M et al. Duodenal-jejunal bypass changes the composition of the gut microbiota. Surg Today 2017;47:137-40. en.  Back to cited text no. 51
    
52.
Benevides-Matos N, Pieri FA, Penatti M, Orlandi PP. Adherence and virulence genes of Escherichia coli from children diarrhoea in the Brazilian Amazon. Braz J Microbiol 2015;46:131-7. eng.  Back to cited text no. 52
    
53.
Olsvik O, Wasteson Y, Lund A, Hornes E. Pathogenic Escherichia coli found in food. Int J Food Microbiol 1991;12:103-13. eng.  Back to cited text no. 53
    
54.
Candan ED, Aksöz N. Klebsiella pneumoniae: characteristics of carbapenem resistance and virulence factors. Acta Biochim Pol 2015;62:867-74. eng.  Back to cited text no. 54
    
55.
Khademi F, Sahebkar A. Fluoroquinolones-resistant Shigella species in Iranian children: a meta-analysis. World Journal of Pediatrics: WJP 2019;15:441-53. eng.  Back to cited text no. 55
    
56.
Kesika P, Balamurugan K. Studies on Shigella boydii infection in Caenorhabditis elegans and bioinformatics analysis of immune regulatory protein interactions. Biochim Biophys Acta 2012;1824:1449-56. eng.  Back to cited text no. 56
    
57.
Oyeka M, Antony S. Citrobacter braakii bacteremia: case report and review of the literature. Infectious Disorders Drug Targets 2017;17:59-63. eng.  Back to cited text no. 57
    
58.
Kong L-C, Tap J, Aron-Wisnewsky J, Pelloux V, Basdevant A, Bouillot J-L et al. Gut microbiota after gastric bypass in human obesity: increased richness and associations of bacterial genera with adipose tissue genes. The American Journal of Clinical Nutrition 2013;98:16-24.  Back to cited text no. 58
    
59.
Luu TH, Michel C, Bard J-M., Dravet F, Nazih H, Bobin-Dubigeon C. Intestinal proportion of blautia sp. is associated with clinical stage and histoprognostic grade in patients with early-stage breast cancer. Nutrition and Cancer 2017;69:267-75.  Back to cited text no. 59
    
60.
Workneh M, Wang F, Romagnoli M, Simner PJ, Carroll K. Bypass graft infection and bacteremia caused by Anaerostipes caccae: first report of human infection caused by a recently described gut anaerobe. Anaerobe 2016;42:98-100.  Back to cited text no. 60
    
61.
Van de Merwe JP, Stegeman JH. Binding of coprococcus comes to the Fc portion of IgG. A possible role in the pathogenesis of Crohn’s disease? Eur J Immunol 1985;15:860-3. eng.  Back to cited text no. 61
    
62.
Koliada A, Syzenko G, Moseiko V, Budovska L, Puchkov K, Perederiy V et al. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiology 2017;17:120.  Back to cited text no. 62
    
63.
Bervoets L, Van Hoorenbeeck K, Kortleven I, Van Noten C, Hens N, Vael C et al. Differences in gut microbiota composition between obese and lean children: a cross-sectional study. Gut Pathogens 2013;5:10.  Back to cited text no. 63
    
64.
Al-Otaibi FE, Al-Mohizea MM. Non-vertebral Veillonella species septicemia and osteomyelitis in a patient with diabetes: a case report and review of the literature. Journal of Medical Case Reports 2014;8:365. eng.  Back to cited text no. 64
    
65.
Goupil R, Nadeau-Fredette AC, Tennankore KK, Bargman JM. Peritonitis caused by veillonella species and Eggerthella lenta in peritoneal dialysis. Perit Dial Int 2014;34:245-7. eng.  Back to cited text no. 65
    
66.
Pérez-Jacoiste Asín MA, Fernández-Ruiz M, Serrano-Navarro I, Prieto-Rodriguez S, Aguado JM. Polymicrobial endocarditis involving Veillonella parvula in an intravenous drug user: case report and literature review of Veillonella endocarditis. Infection 2013;41:591-4. eng.  Back to cited text no. 66
    
67.
Yagihashi Y, Arakaki Y. Acute pyelonephritis and secondary bacteraemia caused by Veillonella during pregnancy. BMJ Case Reports 2012;2012. eng.  Back to cited text no. 67
    
68.
Kishen TJ, Lindstrom ST, Etherington G, Diwan AD. Veillonella spondylodiscitis in a healthy 76-year-old lady. Eur Spine J 2012;21:413-7. eng.  Back to cited text no. 68
    
69.
Strach M, Siedlar M, Kowalczyk D, Zembala M, Grodzicki T. Sepsis caused by Veillonella parvula infection in a 17-year-old patient with X-linked agammaglobulinemia (Bruton’s disease). J Clin Microbiol 2006;44:2655-6. eng.  Back to cited text no. 69
    
70.
Li J, Chen P, Li J, Gao X, Chen X, Chen J. A new treatment of sepsis caused by veillonella parvula: a case report and literature review. Journal of Clinical Pharmacy and Therapeutics 2017;42:649-52. en.  Back to cited text no. 70
    
71.
Chen Y-C, Ko P-H, Yang C-J, Chen Y-C, Lay C-J, Tsai C-C et al. Epidural abscess caused by Veillonella parvula: case report and review of the literature. Journal of Microbiology, Immunology, and Infection = Wei Mian Yu Gan Ran Za Zhi 2016;49:804-8. eng.  Back to cited text no. 71
    
72.
Enaud R, Hooks KB, Barre A, Barnetche T, Hubert C, Massot M et al. intestinal inflammation in children with cystic fibrosis is associated with Crohn’s-like microbiota disturbances. J Clin Med 2019;8.  Back to cited text no. 72
    
73.
Farooq H, Mohammad T, Farooq A, Mohammad Q. Streptococcus gordonii Empyema: a Rare Presentation of Streptococcus gordonii Infection. Cureus 2019;11:e4611.  Back to cited text no. 73
    
74.
Sava IG, Heikens E, Huebner J. Pathogenesis and immunity in enterococcal infections. Clin Microbiol Infect 2010;16:533-40. eng.  Back to cited text no. 74
    
75.
Paganelli FL, Luyer M, Hazelbag CM, Uh H-W, Rogers MRC, Adriaans D et al. Roux-Y gastric bypass and sleeve gastrectomy directly change gut microbiota composition independent of surgery type. Scientific Reports 2019;9:10979. PubMed PMID: 31358818. eng.  Back to cited text no. 75
    
76.
Damms-Machado A, Mitra S, Schollenberger AE, Kramer KM, Meile T, Königsrainer A et al. Effects of surgical and dietary weight loss therapy for obesity on gut microbiota composition and nutrient absorption. BioMed Research International 2015;2015:806248. eng.  Back to cited text no. 76
    
77.
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 USA 2009;106:2365-70. eng.  Back to cited text no. 77
    
78.
Popoff MR, Bouvet P. Clostridial toxins. Future Microbiology 2009;4:1021-64. eng.  Back to cited text no. 78
    
79.
Hall AB, Yassour M, Sauk J, Garner A, Jiang X, Arthur T et al. A novel Ruminococcus gnavus clade enriched in inflammatory bowel disease patients. Genome Medicine. 2017;9:103. eng.  Back to cited text no. 79
    
80.
Ward EK, Schuster DP, Stowers KH, Royse AK, Ir D, Robertson CE et al. The effect of PPI use on human gut microbiota and weight loss in patients undergoing laparoscopic Roux-en-Y gastric bypass. Obesity Surgery 2014;24:1567-71. eng.  Back to cited text no. 80
    



 
 
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