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Characterization of Enterobacteries Genus in Intestinal Microbiota of Celiac Children

Fatima Lahcene , Aicha Tir Touil Meddah, Karim Bouziane-Nedjadi, Boumediene Meddah, André Leke
International Journal of Celiac Disease. 2017, 5(4), 159-163. DOI: 10.12691/ijcd-5-4-8
Published online: November 24, 2017

Abstract

The imbalance of the intestinal microbiota is link, by several diseases such as celiac disease, which causes inflammation in the small intestine. This inflammation is due by the digestion of gluten present in some type of cereals. In this work, fecal and duodenal biopsy samples were collected to characterize by conventional culture technique the composition of the Enterobacteries group in intestinal mirobiota of celiac children and were compared with control children. A significant difference detected in the intestinal flora of celiac children compared to controls children concerning the Enterobacteries group. We found an increase of E.coli, Enterobacter aerogeneses, and Klebsiella with presence of Salmonella sp, Shigella sp in biopsy and fecal samples of celiac children and a relationship between the increase of Enterobacter cloacea and the presence of positive anti-transglutaminase value.

1. Introduction

Intestinal flora is a complex microbial consortium. It participates actively in our good health. 1, 2. This microbial population hosted in the human digestive tract and contains approximately 1014 bacteria 3. The intestinal microbiota is considered as a full organ which plays an important role in energy metabolism, and nutritional balance 4. It also serves to stimulate the intestinal immune system and opposes the intestinal colonization by pathogenic microorganisms (barrier effect) 5, 6. These functions can be influence if the composition of the flora is changed. Changing the composition of the intestinal flora both, quantitative and qualitative level may be the cause of intestinal disorders like diarrhea or chronic inflammatory diseases such as celiac disease 7.

Celiac disease (CD) is an autoimmune affection that occurs in genetically susceptible individuals 8. This disorder results in damage to the wall of the small intestine mucosa. When foods with gluten consuming. Gluten is a form of protein found in some cereals as (wheat, (hordein and rye) 9, 10. The damage to the intestine mucosa leads to poor absorption of many nutrient specially (fat, calcium, iron, and folate) Which results in a growth retardation in children and a risk of osteoporosis in adults 11, 12 and also causes in change of the bacterial groups of intestinal flora as Enterobacterie 13.

The objective of this study was to determine the composition of Enterobactries group starting at biopsy and fecal samples in celiac children and controls children by classical microbiology technical.

2. Materials and Methods

2.1. Subjects and Samples Collection

The duodenal biopsy samples and fecal samples were collected from two groups of children; (1) group of celiac children, having clinical manifestations evoking the celiac disease, occurring after the introduction of gluten in the diet with a confirmation of the disease by histological analysis according to the classification of Marsh for different types of villous atrophy and serological analysis, such children have no other pathology. For (2) group of controls, are non-celiac children, have a normal villous structure and a negative serology. The two groups of children do not follow any treatment with antibiotics or corticosteroids at least two month prior to sampling period. A total 30 fecal and 19 duodenal biopsy of these children were collected in sterile jars labeled with the name of the child.

2.2. Ethical Consideration

The children were enlisted in the study after informed consent was achieved by their parents and the Ethics Committee of the faculty of Medicine - Oran- Algeria.

2.3. Sample Treatment

One gram of each fecal sample and per milligram of intestinal biopsy (grinding using a scalpel) were weighed and placed into 9 ml of sterile physiological water; it is the mother solution, then decimal dilutions were performed up to (10-8). 100 μl of each dilution was spread on Eosin Methylene Blue agar media (EMB agar) and on Hektoen agar in duplicated. All culture media were incubated in aerobic conditions at 37°C for 48-72 h.

2.4. Bacterial Enumeration

After incubation, Enumeration of germs was conducted on the dishes presenting between 30 and 300 colonies and expressed in log colony forming units (CFU) per gram for statistical reasons by the following formula 14:

2.5. Identification of the Bacterial Strains
2.5.1. Morphological Characters

The macroscopic observation of the colonies used to show some specific characteristics of species such as: appearance, size, contour and pigmentation.

To verify the purity of the isolates using the Gram stain. This allows to make the differentiation between Gram-positive and Gram-negative bacteria and thus to describe the form of bacterial cells and their association mode.


2.5.2. Biochemical Characters

The study of biochemical tests is essentially based on research oxidase, catalase and urease test, B galactosidase (ONPG),Triple Sugar Iron Agar, Simmons Citrate, Indole production, Voges-Proskauer (VP), Methyl red test, and after these classical methods 15, bacterial strains were confirmed by using the kits commerciels API 20E.

2.6. Statistical Analysis

The results achieved were expressed as mean and standard deviation (x ± δ) and for the microbiological analysis of the intestinal microbiota for two groups of children were determined by Colony Forming Unit Log (CFU) and value of p≤ 0.05was considered significant.

3. Results and Discussion

3.1. Subjects

45 Children enrolled in this work with a mean age of (9.62 ±0.90years), celiac children n =24, with 08 boys and control (no celiac children) n=21 with 10 boys. Form the mean of Body Mass Index (BMI) was somewhat weak in children with celiac disease than control children (median 14.82 kg/m2 and 16.26 kg/m2 respectively).This value of BMI in celiac children may be associated with malabsorption of nutrients in the small intestine that is characterize by villous atrophy.

3.2. Enumeration of Enterobacterie Group in the Intestinal Microbiota

Figure 1 indicates that the median of Enterobacteries found in fecal sample (7.60 Log CFU) of celiac children was higher when compared with control children (6.25 Log CFU). Also for duodenal sample, the Enterobacteries genus was more abundant in celiac children with medium of 4.92 Log UFC than in controls with median of 3 Log UFC. Our results obtained were similar with other studies that have examined the fecal matter of celiac children 16, 17, 18. As the study of Björkstén and al was indicated the increase number of Entrobacteries in allergy infants compared to healthy infants suggesting a link between the bacterial group and immune dysregulation 19.

3.3. Biochemical Identification of Enterobacterie Genera

Enterobacteries strains isolated from the EMB agar media were presented different form like dark violet colonies, domedshowa greenish metallic sheen light or blue colonies with dark brown center, flattened and sometimes-brownish colonies, mucosal. Microscopic examination by Gram coloration shows that our strains are gram-negative bacilli and the oxidase test was negative in all cells bacterial. After biochemical tests, the strains of Enterobacteries identified in the intestinal flora of celiac children are: E.coli, Enterobacter aerogeneses, Enterobacter cloacae, Klebsiella oxytoca, Salmonella sp, Citrobacter sp, Shigella sp.

3.4. Composition and Diversity of Enterobacteries genus in Intestinal Flora of Celiac Children

From the results shown in Figure 2 and Figure 2, we detected a difference for Enterobacteries genus in the intestinal (fecal and duodenal) flora of the celiac children compared to the controls. This difference was showed by the increase in the number of the E.coli and Enterobacter aerogeneses from the duodenal flora of the celiac children with medium (3.99 Log CFU/mg, 1.32 Log CFU/mg respectively) compared to the control with medium (2.43 Log CFU/mg, 0.4 Log CFU/mg). Same result obtained for fecal matter, these genera were slightly higher in celiac children with medium (4.33 Log CFU/g , 1.74 Log CFU/g respectively) than control with medium (4.05 Log CFU/g ,1.35 Log CFU/g).

We found also the genera of Enterobacter cloacae and Citrobacter only in the intestinal biopsy of the celiac children with a very high medium (1.00Log CFU/; 0.47 Log FCU/mg respectively) compared to the control (0.13Log CFU / mg; 0.04Log CFU/mg).

And for Salmonella sp, Shigellasp and Klebsiella sp were identified only in the intestinal microbiota of celiac children with different values (0.60 Log CFU / g; 0.48 Log CFU / g and 0.15 Log CFU / mg), and slightly higher rate of Klebsiella oxytoca was recorded in fecal samples of coeliac children compared to controls (0.81LogCFU / g, 0.18 Log CFU / g). The abundance of E. coli in celiac children compared to controls was reported by the study of Schippa et al 20 also at adult and children in Crohn’s disease 21.

In addition, Escherichia coli adherent invasive able to replicate and induce tumor necrosis factor production (TNF-α) in the intestinal mucosa of patients with Crohn's disease 22.

Generally, E. coli was the most common species of the Enterobacteriaceae family detected and isolated from stool samples and intestinal biopsies of celiac children 23, 24.

Our results are in agreement with the work of Di Cagno et al 25, which showed that Salmonella, Shigella and Klebsiella were significantly higher in celiac children. The studies of Sánchez and al 18, 26 have revealed the abundance of family Enterobacteriaceae in celiac children, particularly Klebsiella oxytoca strains, E. coli and Enterobacter cloacae. Enterobacteria of the genus Klebsiella, Enterobacter, and Citrobacte present the passage flora by concentrations below 106 CFU / g, and colonize the digestive tract, during a pathological situation 27.

3.5. Correlation between Anti-Transglutaminase (Anti-tTG) and Genera of Enterobacteries Composition in Celiac children

A significant correlation was observed only between the number of Enterbacter cloacea (r = 0.59), and the level of anti-transglutaminase antibody in intestinal biopsies and feces in celiac children (P < 0,05).

Negative correlations were recorded between the genera of Enterobacteria and anti-gliadin antibody levels in celiac children regardless of the site of biopsy or fecal sampling.

Our study shows positive correlations only between the serological markers anti-tarnsglutaminase antibodies and the numbers of Enterbacter cloacea. This suggests that, the increase in Enterobacter cloacea is related to the positive anti-transglutaminase values in the small intestine in celiac children. No results published so far, for this context, but various studies have demonstrated associations between the disturbance of the intestinal microbiota, and the pathophysiology of celiac disease. Nevertheless, the alteration of the intestinal microbiota is not yet elucidated, if it is the cause or consequence of the celiac disease. Verdu et al 28 have shown that genetically predisposed individuals may exhibit an imbalance of the intestinal microbiota, increasing the immunological responses responsible for intestinal lesions, which would promote the onset of celiac disease. Other studies suggest that auto-antibodies such as anti-transglutaminase antibodies may also modulate haemostasis of the small intestine, the onset of villous atrophy, which alter the permeability of the intestinal barrier and facilitate the passage of bacterial pathogens to colonize the intestinal mucosa 29, 30.

4. Conclusion

Our work demonstrates a quantitative and qualitative diversity in the group of Enterobacteriaceae of the duodenal and fecal microbiota from celiac children compared to the controls. This difference is detected by the increase in the number of E.coli, Enterobacter aerogeneses, Klebsiella sp and the presence of salmonella sp, Shigella sp in celiac children more the increase in Enterobacter cloacea is related to the positive anti-transglutaminase values in the small intestine in celiac children. Therefore, the results show that the imbalance of this bacterial group in the intestinal microbiota can increase the pathogenesis of celiac disease.

Acknowledgments

We wish to thank all the participants for their collaboration to realize this study.

References

[1]  Cano N, Barnoud D, et Hassalmannet M. Adult Artificial Nutrition Treatment.Sringer, Paris. 2007
In article      
 
[2]  Corthier. Intestinal flora and health: what issues?. 47th Annual nutrition and diététique- day "Symposium: intestinal flora and health. CNIT Paris. Elsevier Masson SAS. 2007; 76.
In article      
 
[3]  Hooper LV and Gordon J I. Commensal host-bacterial relationships in the gut .Science. 2001; 292(5519): 1115-8.
In article      View Article  PubMed
 
[4]  Delzenne. M, Cani. D. Involvement of the intestinal flora in the energy metabolism. Revue scientifique MEDECINE/SCIENCES. 2008; 24 : 505-10.
In article      View Article  PubMed
 
[5]  Sekirov I, Russell SL, L Antunes LC, and Finlay BB. Gut microbiota in health and disease.Physiological Reviews . 2010; 90(3): 859-904.
In article      View Article  PubMed
 
[6]  Goulet O. The intestinal flora: a living mode to preserve. Journal of pediatrics and nursery 2009; 22:102-106.
In article      
 
[7]  Hopkins MJ et Macfarlane GT. Changes in predominant bacterial populations in human faeces with age and with Clostridium difficile infection. J Med Microbiol. 2002 51(5): 448-54.
In article      View Article  PubMed
 
[8]  Guandalini S, Setty M. Celiac disease. CurrOpinGastroenterol. 2008 Nov. 24(6): 707-12.
In article      View Article  PubMed
 
[9]  Mulder CJ, and Bartelsman JF. Case-finding in celiac disease should be intensified.Best Pract Res Clin Gastroenterol. 2005; 19: 479-486.
In article      View Article  PubMed
 
[10]  Rewers M. Epidemiology of celiac disease: what are the prevalence, incidence, andprogression of celiac disease? Gastroenterology. 2005; 128: 47-51.
In article      View Article
 
[11]  Cegarra M. The gluten-free diet: difficulties with follow-up. Archives of Pediatrics. 2006; 13: 576-578.
In article      View Article  PubMed
 
[12]  Schmitz J. Gluten-free diet in children. Journal of Pediatrics and Childcare. 2007; 20: 337-344.
In article      View Article
 
[13]  Collado. MC, Sanz Y. Quantification of mucosa-adheredmicrobiota of lambs and calves by the use of culture methods and fluorescent in situ hybridization coupled with flow cytometry techniques. Vet Microbiol . 2007; 121: 299-306.
In article      View Article  PubMed
 
[14]  Béraud M. The technician biological analyzes theoretical and practical guide.TeDc Lavoisier. 2001; 988-990.
In article      
 
[15]  Balows A, Hausler W, Herrmann K, Isenberg H, Shadomy H. Manual of clinical microbiology. Washington (DC): ASM. 1991
In article      
 
[16]  Collado C ,Donat E, Ribes-Koninck C, Calabuig M, Sanz Y. Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease. JCP. 2009; 62(3): 264-9.
In article      View Article
 
[17]  Hopper AD, Cross SS, Sanders DS.Patchy villous atrophy in adult patients with suspected gluten- sensitive enteropathy: is a multiple duodenal biopsy strategy appropriate? Endoscopy. 2008; 40(3): 219-224.
In article      View Article  PubMed
 
[18]  Sánchez E, Donat E, Ribes-Koninckx C,Fernández-MurgaM , and Sanz Y..Duodenal-Mucosal Bacteria Associated with Celiac Disease in Children. Appl Environ Microbiol. 2013; 79(18): 5472.
In article      View Article  PubMed
 
[19]  Björkstén B, Sepp E, Kulge, J, and al. Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol. 2001; 108(4): 516-20
In article      View Article  PubMed
 
[20]  Schippa S, Iebba V, Barbato M, Di Nardo G,Totino V, Checchi MP, Longhi C,Maiella G, Cucchiara S, Conte, MP. A distinctive ‘microbial signature’ in celiac pediatric patients.BMC Microbiol. 2010; 10, 175.
In article      View Article  PubMed
 
[21]  Schippa S, Totino V,Marazzato M, Lepanto M, Santangelo F., Aleandri M., Gagliardi A., Longhi C., Pantanella, F., Iebba V., and al. Escherichia coli population-based study in pediatric crohn’s disease. Adv. Microbiol. 2014, 4, 886-889.
In article      View Article
 
[22]  Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C., Glasser AL, Barnich N, Bringer MA, Swidsinski A, Beaugerie L. Colombel JF. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology.2004; 127: 412-421.
In article      View Article  PubMed
 
[23]  Conte MP, Schippa S, Zamboni I, Penta M., Chiarini F, Seganti L, Osborn J, Falconieri P, Borrelli O, et Cucchiara S.Gut-associated bacterial microbiota in pediatric patients with inflammatorybowel disease. Gut. 2006; 55(12):1760-7.
In article      View Article  PubMed
 
[24]  Collado C, Donat E, Ribes-Koninck C, Calabuig M, Sanz. Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease .JCP. 2009; 62(3): 264-9.
In article      View Article
 
[25]  Di Cagno R, Rizzello CG, Gagliardi F., Ricciuti P, Ndagijimana M, Francavilla R., Guerzoni ME, Crecchio C, Gobbetti M., et De Angelis M. Different fecal microbiotas and volatile organic compounds in treated and untreated children with celiac disease. Appl Environ Microbiol. 20097; 5: 3963-3971.
In article      View Article
 
[26]  Sánchez E, Nadal I, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y.. Reduced diversity and increased virulence-gene carriage in intestinalenterobacteria of coeliac children. BMC Gastroenterol. 2008; 8(50): 10.
In article      View Article
 
[27]  Baron S. Health and Micro nutrition: A global approach adapted to the pharmacy in adults. Doctoral thesis in pharmacy.Universityof Rouen. 2014; 187.
In article      
 
[28]  Verdu EF, Galipeau HJ, et Jabri B. Novel players in coeliac disease pathogenesis: role of the gut microbiota. Nat Rev Gastroenterol Hepatol (sous presse). 2015.
In article      View Article  PubMed
 
[29]  Caja S, Myrsky E, Korponay-Szabo IR, Nadalutti C, Sulic AM, Lavric M, Sblattero D, Marzari R, Collighan R, Mongeot A, Griffin M, Mäki M, Kaukinen K, et Lindfors K. Inhibition of transglutaminase 2 enzymatic activity ameliorates the anti-angiogenic effects of coeliac disease autoantibodies. Scand J Gastroenterol. 2010; 45: 421-427.
In article      View Article  PubMed
 
[30]  De Sousa Moraes LF, Grzeskowiak LM, de Sales Teixeira TF, et Gouveia Peluzio Mdo C. Intestinal Microbiota and Probiotics in Celiac Disease. Clin Microbiol Rev. 2014; 27:482-9.
In article      View Article  PubMed
 

Published with license by Science and Education Publishing, Copyright © 2017 Fatima Lahcene, Aicha Tir Touil Meddah, Karim Bouziane-Nedjadi, Boumediene Meddah and André Leke

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

Cite this article:

Normal Style
Fatima Lahcene, Aicha Tir Touil Meddah, Karim Bouziane-Nedjadi, Boumediene Meddah, André Leke. Characterization of Enterobacteries Genus in Intestinal Microbiota of Celiac Children. International Journal of Celiac Disease. Vol. 5, No. 4, 2017, pp 159-163. http://pubs.sciepub.com/ijcd/5/4/8
MLA Style
Lahcene, Fatima, et al. "Characterization of Enterobacteries Genus in Intestinal Microbiota of Celiac Children." International Journal of Celiac Disease 5.4 (2017): 159-163.
APA Style
Lahcene, F. , Meddah, A. T. T. , Bouziane-Nedjadi, K. , Meddah, B. , & Leke, A. (2017). Characterization of Enterobacteries Genus in Intestinal Microbiota of Celiac Children. International Journal of Celiac Disease, 5(4), 159-163.
Chicago Style
Lahcene, Fatima, Aicha Tir Touil Meddah, Karim Bouziane-Nedjadi, Boumediene Meddah, and André Leke. "Characterization of Enterobacteries Genus in Intestinal Microbiota of Celiac Children." International Journal of Celiac Disease 5, no. 4 (2017): 159-163.
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  • Figure 2. Different genus of Enterobacteries fond in the duodenal microbiota of celiac and controls children (*: P<0, 05, ** : P<0,01)
  • Figure 4. Correlation between anti-Transglutaminase (Anti-tTG) and of Enterobacteries group in celiac children (a) intestinal biopsy and (b) fecal matter
  • Figure 5. Correlation between anti-Gliadine and of Enterobacteries group in celiac children (a) intestinal biopsy and (b) fecal matter
[1]  Cano N, Barnoud D, et Hassalmannet M. Adult Artificial Nutrition Treatment.Sringer, Paris. 2007
In article      
 
[2]  Corthier. Intestinal flora and health: what issues?. 47th Annual nutrition and diététique- day "Symposium: intestinal flora and health. CNIT Paris. Elsevier Masson SAS. 2007; 76.
In article      
 
[3]  Hooper LV and Gordon J I. Commensal host-bacterial relationships in the gut .Science. 2001; 292(5519): 1115-8.
In article      View Article  PubMed
 
[4]  Delzenne. M, Cani. D. Involvement of the intestinal flora in the energy metabolism. Revue scientifique MEDECINE/SCIENCES. 2008; 24 : 505-10.
In article      View Article  PubMed
 
[5]  Sekirov I, Russell SL, L Antunes LC, and Finlay BB. Gut microbiota in health and disease.Physiological Reviews . 2010; 90(3): 859-904.
In article      View Article  PubMed
 
[6]  Goulet O. The intestinal flora: a living mode to preserve. Journal of pediatrics and nursery 2009; 22:102-106.
In article      
 
[7]  Hopkins MJ et Macfarlane GT. Changes in predominant bacterial populations in human faeces with age and with Clostridium difficile infection. J Med Microbiol. 2002 51(5): 448-54.
In article      View Article  PubMed
 
[8]  Guandalini S, Setty M. Celiac disease. CurrOpinGastroenterol. 2008 Nov. 24(6): 707-12.
In article      View Article  PubMed
 
[9]  Mulder CJ, and Bartelsman JF. Case-finding in celiac disease should be intensified.Best Pract Res Clin Gastroenterol. 2005; 19: 479-486.
In article      View Article  PubMed
 
[10]  Rewers M. Epidemiology of celiac disease: what are the prevalence, incidence, andprogression of celiac disease? Gastroenterology. 2005; 128: 47-51.
In article      View Article
 
[11]  Cegarra M. The gluten-free diet: difficulties with follow-up. Archives of Pediatrics. 2006; 13: 576-578.
In article      View Article  PubMed
 
[12]  Schmitz J. Gluten-free diet in children. Journal of Pediatrics and Childcare. 2007; 20: 337-344.
In article      View Article
 
[13]  Collado. MC, Sanz Y. Quantification of mucosa-adheredmicrobiota of lambs and calves by the use of culture methods and fluorescent in situ hybridization coupled with flow cytometry techniques. Vet Microbiol . 2007; 121: 299-306.
In article      View Article  PubMed
 
[14]  Béraud M. The technician biological analyzes theoretical and practical guide.TeDc Lavoisier. 2001; 988-990.
In article      
 
[15]  Balows A, Hausler W, Herrmann K, Isenberg H, Shadomy H. Manual of clinical microbiology. Washington (DC): ASM. 1991
In article      
 
[16]  Collado C ,Donat E, Ribes-Koninck C, Calabuig M, Sanz Y. Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease. JCP. 2009; 62(3): 264-9.
In article      View Article
 
[17]  Hopper AD, Cross SS, Sanders DS.Patchy villous atrophy in adult patients with suspected gluten- sensitive enteropathy: is a multiple duodenal biopsy strategy appropriate? Endoscopy. 2008; 40(3): 219-224.
In article      View Article  PubMed
 
[18]  Sánchez E, Donat E, Ribes-Koninckx C,Fernández-MurgaM , and Sanz Y..Duodenal-Mucosal Bacteria Associated with Celiac Disease in Children. Appl Environ Microbiol. 2013; 79(18): 5472.
In article      View Article  PubMed
 
[19]  Björkstén B, Sepp E, Kulge, J, and al. Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol. 2001; 108(4): 516-20
In article      View Article  PubMed
 
[20]  Schippa S, Iebba V, Barbato M, Di Nardo G,Totino V, Checchi MP, Longhi C,Maiella G, Cucchiara S, Conte, MP. A distinctive ‘microbial signature’ in celiac pediatric patients.BMC Microbiol. 2010; 10, 175.
In article      View Article  PubMed
 
[21]  Schippa S, Totino V,Marazzato M, Lepanto M, Santangelo F., Aleandri M., Gagliardi A., Longhi C., Pantanella, F., Iebba V., and al. Escherichia coli population-based study in pediatric crohn’s disease. Adv. Microbiol. 2014, 4, 886-889.
In article      View Article
 
[22]  Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C., Glasser AL, Barnich N, Bringer MA, Swidsinski A, Beaugerie L. Colombel JF. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology.2004; 127: 412-421.
In article      View Article  PubMed
 
[23]  Conte MP, Schippa S, Zamboni I, Penta M., Chiarini F, Seganti L, Osborn J, Falconieri P, Borrelli O, et Cucchiara S.Gut-associated bacterial microbiota in pediatric patients with inflammatorybowel disease. Gut. 2006; 55(12):1760-7.
In article      View Article  PubMed
 
[24]  Collado C, Donat E, Ribes-Koninck C, Calabuig M, Sanz. Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease .JCP. 2009; 62(3): 264-9.
In article      View Article
 
[25]  Di Cagno R, Rizzello CG, Gagliardi F., Ricciuti P, Ndagijimana M, Francavilla R., Guerzoni ME, Crecchio C, Gobbetti M., et De Angelis M. Different fecal microbiotas and volatile organic compounds in treated and untreated children with celiac disease. Appl Environ Microbiol. 20097; 5: 3963-3971.
In article      View Article
 
[26]  Sánchez E, Nadal I, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y.. Reduced diversity and increased virulence-gene carriage in intestinalenterobacteria of coeliac children. BMC Gastroenterol. 2008; 8(50): 10.
In article      View Article
 
[27]  Baron S. Health and Micro nutrition: A global approach adapted to the pharmacy in adults. Doctoral thesis in pharmacy.Universityof Rouen. 2014; 187.
In article      
 
[28]  Verdu EF, Galipeau HJ, et Jabri B. Novel players in coeliac disease pathogenesis: role of the gut microbiota. Nat Rev Gastroenterol Hepatol (sous presse). 2015.
In article      View Article  PubMed
 
[29]  Caja S, Myrsky E, Korponay-Szabo IR, Nadalutti C, Sulic AM, Lavric M, Sblattero D, Marzari R, Collighan R, Mongeot A, Griffin M, Mäki M, Kaukinen K, et Lindfors K. Inhibition of transglutaminase 2 enzymatic activity ameliorates the anti-angiogenic effects of coeliac disease autoantibodies. Scand J Gastroenterol. 2010; 45: 421-427.
In article      View Article  PubMed
 
[30]  De Sousa Moraes LF, Grzeskowiak LM, de Sales Teixeira TF, et Gouveia Peluzio Mdo C. Intestinal Microbiota and Probiotics in Celiac Disease. Clin Microbiol Rev. 2014; 27:482-9.
In article      View Article  PubMed