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Published in: Gut Pathogens 1/2016

Open Access 01-12-2016 | Research

Use of molecular typing to investigate bacterial translocation from the intestinal tract of chlorpyrifos-exposed rats

Authors: Claire Joly Condette, Bertin Elion Dzon, Farida Hamdad, Maurice Biendo, Véronique Bach, Hafida Khorsi-Cauet

Published in: Gut Pathogens | Issue 1/2016

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Abstract

Background

Human are confronted on a daily basis with contaminant pesticide residues in food, water and other components of the environment. Although the digestive system is the first organ to come into contact with food contaminants, very few data are available on the impact of low-dose pesticide exposure during the in utero and postnatal periods on intestinal bacterial translocation (BT). Previous studies have revealed that chlorpyrifos (CPF) exposure is associated with intestinal dysbiosis and the contamination of sterile organs. Here, molecular typing was used to investigate intestinal bacterial translocation in rats exposed to chlorpyrifos in utero and during lactation. The translocated bacteria were profiled, and CPF tolerance and antibiotic resistance traits were determined.

Methods

A total of 72 intestinal segments and extra-intestinal organs were obtained from 14 CPF-exposed rats. The samples were cultured to isolate bacterial strains that had tolerated treatment with 1 or 5 mg CPF/kg bodyweight/day in vivo. Strains were identified using matrix-assisted laser desorption/ionization (MALDI) Biotyper. The disk diffusion method was used to determine the antibiotic susceptibility. The isolates were genotyped with PCR assays for the enterobacterial repetitive intergenic consensus sequence and random amplification polymorphic DNA.

Results

Bacterial translocation was confirmed for 7 of the 31 strains (22.6 %) isolated from extra-intestinal sites. Overall, the most prevalent bacteria were Staphylococcus aureus (55.5 % of the 72 intestinal and extra-intestinal isolates), Enterococcus faecalis (27.7 %) and Bacillus cereus (9.8 %). 5 % of the S. aureus isolates displayed methicillin resistance. Seventy two strains were identified phenotypically, and seven translocated strains (mainly S. aureus) were identified by genotyping. Genotypically confirmed translocation was mainly observed found in pesticide-exposed groups (6 out of 7).

Conclusion

BT from the intestinal tract colonized normally sterile extra-intestinal organs in CPF-exposed rats. Our findings validate the use of molecular typing for the assessment of intestinal BT in CPF-exposed rats during critical periods of development.
Literature
1.
go back to reference Ambali SF, Idris SB, Onukak C, Shittu M, Ayo JO. Ameliorative effects of vitamin C on short-term sensorimotor and cognitive changes induced by acute chlorpyrifos exposure in Wistar rats. Toxicol Ind Health. 2010;26:547–58.CrossRefPubMed Ambali SF, Idris SB, Onukak C, Shittu M, Ayo JO. Ameliorative effects of vitamin C on short-term sensorimotor and cognitive changes induced by acute chlorpyrifos exposure in Wistar rats. Toxicol Ind Health. 2010;26:547–58.CrossRefPubMed
2.
go back to reference Middlemore-Risher ML, Adam BL, Lambert NA, Terry AV Jr. Effects of chlorpyrifos and chlorpyrifos-oxon on the dynamics and movement of mitochondria in rat cortical neurons. J Pharmacol Exp Ther. 2011;339:341–9.CrossRefPubMedPubMedCentral Middlemore-Risher ML, Adam BL, Lambert NA, Terry AV Jr. Effects of chlorpyrifos and chlorpyrifos-oxon on the dynamics and movement of mitochondria in rat cortical neurons. J Pharmacol Exp Ther. 2011;339:341–9.CrossRefPubMedPubMedCentral
3.
go back to reference Tirelli V, Catone T, Turco L, Di Consiglio E, Testai E, De Angelis I. Effects of the pesticide clorpyrifos on an in vitro model of intestinal barrier. Toxicol In Vitro. 2007;21:308–13.CrossRefPubMed Tirelli V, Catone T, Turco L, Di Consiglio E, Testai E, De Angelis I. Effects of the pesticide clorpyrifos on an in vitro model of intestinal barrier. Toxicol In Vitro. 2007;21:308–13.CrossRefPubMed
4.
go back to reference Joly Condette C, Khorsi-Cauet H, Morliere P, Zabijak L, Reygner J, Bach V, et al. Increased gut permeability and bacterial translocation after chronic chlorpyrifos exposure in rats. Plos ONE. 2014;9:e102217.CrossRefPubMedPubMedCentral Joly Condette C, Khorsi-Cauet H, Morliere P, Zabijak L, Reygner J, Bach V, et al. Increased gut permeability and bacterial translocation after chronic chlorpyrifos exposure in rats. Plos ONE. 2014;9:e102217.CrossRefPubMedPubMedCentral
5.
go back to reference Joly Condette C, Bach V, Mayeur C, Gay-Queheillard J, Khorsi-Cauet H. Chlorpyrifos exposure during perinatal period affects intestinal microbiota associated with delay of maturation of digestive tract in rats. J Pediatr Gastroenterol Nutr. 2015;61:30–40.PubMed Joly Condette C, Bach V, Mayeur C, Gay-Queheillard J, Khorsi-Cauet H. Chlorpyrifos exposure during perinatal period affects intestinal microbiota associated with delay of maturation of digestive tract in rats. J Pediatr Gastroenterol Nutr. 2015;61:30–40.PubMed
6.
go back to reference Berg RD. Bacterial translocation from the gastrointestinal tract. Adv Exp Med Biol. 1999;473:11–30.CrossRefPubMed Berg RD. Bacterial translocation from the gastrointestinal tract. Adv Exp Med Biol. 1999;473:11–30.CrossRefPubMed
7.
go back to reference Andersen K, Kesper MS, Marschner JA, Konrad L, Ryu M, Kumar Vr S, Kulkarni OP, Mulay SR, Romoli S, Demleitner J, Schiller P, Dietrich A, Müller S, Gross O, Ruscheweyh HJ, Huson DH, Stecher B, Anders HJ. Intestinal dysbiosis, barrier dysfunction, and bacterial translocation account for CKD-related systemic inflammation. J Am Soc Nephrol. 2016. doi:10.1681/ASN.2015111285. Andersen K, Kesper MS, Marschner JA, Konrad L, Ryu M, Kumar Vr S, Kulkarni OP, Mulay SR, Romoli S, Demleitner J, Schiller P, Dietrich A, Müller S, Gross O, Ruscheweyh HJ, Huson DH, Stecher B, Anders HJ. Intestinal dysbiosis, barrier dysfunction, and bacterial translocation account for CKD-related systemic inflammation. J Am Soc Nephrol. 2016. doi:10.​1681/​ASN.​2015111285.
8.
go back to reference Balzan S, de Almeida Quadros C, de Cleva R, Zilberstein B, Cecconello I. Bacterial translocation: overview of mechanisms and clinical impact. J Gastroenterol Hepatol. 2007;22:464–71.CrossRefPubMed Balzan S, de Almeida Quadros C, de Cleva R, Zilberstein B, Cecconello I. Bacterial translocation: overview of mechanisms and clinical impact. J Gastroenterol Hepatol. 2007;22:464–71.CrossRefPubMed
9.
go back to reference Swank GM, Deitch EA. Role of the gut in multiple organ failure: bacterial translocation and permeability changes. World J Surg. 1996;20:411–7.CrossRefPubMed Swank GM, Deitch EA. Role of the gut in multiple organ failure: bacterial translocation and permeability changes. World J Surg. 1996;20:411–7.CrossRefPubMed
10.
go back to reference Chiodini RJ, Dowd SE, Galandiuk S, Davis B, Glassing A. The predominant site of bacterial translocation across the intestinal mucosal barrier occurs at the advancing disease margin in Crohn’s disease. Microbiology. 2016;162:1–2.CrossRef Chiodini RJ, Dowd SE, Galandiuk S, Davis B, Glassing A. The predominant site of bacterial translocation across the intestinal mucosal barrier occurs at the advancing disease margin in Crohn’s disease. Microbiology. 2016;162:1–2.CrossRef
11.
go back to reference Plantefève G, Bleichner G. Translocation bactérienne: mythe ou réalité? Réanimation. 2001;10:550–61.CrossRef Plantefève G, Bleichner G. Translocation bactérienne: mythe ou réalité? Réanimation. 2001;10:550–61.CrossRef
12.
go back to reference Mabbott NA, Donaldson DS, Ohno H, Williams IR, Mahajan A. Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol. 2013;6:666–77.CrossRefPubMedPubMedCentral Mabbott NA, Donaldson DS, Ohno H, Williams IR, Mahajan A. Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol. 2013;6:666–77.CrossRefPubMedPubMedCentral
13.
go back to reference Go LL, Ford HR, Watkins SC, Healey PJ, Albanese CT, Donhalek A, et al. Quantitative and morphologic analysis of bacterial translocation in neonates. Arch Surg. 1994;129:1184–90.CrossRefPubMed Go LL, Ford HR, Watkins SC, Healey PJ, Albanese CT, Donhalek A, et al. Quantitative and morphologic analysis of bacterial translocation in neonates. Arch Surg. 1994;129:1184–90.CrossRefPubMed
14.
go back to reference Van Camp JM, Tomaselli V, Coran AG. Bacterial translocation in the neonate. Curr Opin Pediatr. 1994;6:327–33.PubMed Van Camp JM, Tomaselli V, Coran AG. Bacterial translocation in the neonate. Curr Opin Pediatr. 1994;6:327–33.PubMed
15.
go back to reference Yajima M, Nakayama M, Hatano S, Yamazaki K, Aoyama Y, Yajima T, et al. Bacterial translocation in neonatal rats: the relation between intestinal flora, translocated bacteria, and influence of milk. J Pediatr Gastroenterol Nutr. 2001;33:592–601.CrossRefPubMed Yajima M, Nakayama M, Hatano S, Yamazaki K, Aoyama Y, Yajima T, et al. Bacterial translocation in neonatal rats: the relation between intestinal flora, translocated bacteria, and influence of milk. J Pediatr Gastroenterol Nutr. 2001;33:592–601.CrossRefPubMed
17.
go back to reference Belmekki M, Mammeri H, Hamdad F, Rousseau F, Canarelli B, Biendo M. Comparison of Xpert MRSA/SA Nasal and MRSA/SA ELITe MGB assays for detection of the mecA gene with susceptibility testing methods for determination of methicillin resistance in Staphylococcus aureus isolates. J Clin Microbiol. 2013;51:3183–91.CrossRefPubMedPubMedCentral Belmekki M, Mammeri H, Hamdad F, Rousseau F, Canarelli B, Biendo M. Comparison of Xpert MRSA/SA Nasal and MRSA/SA ELITe MGB assays for detection of the mecA gene with susceptibility testing methods for determination of methicillin resistance in Staphylococcus aureus isolates. J Clin Microbiol. 2013;51:3183–91.CrossRefPubMedPubMedCentral
18.
go back to reference Biendo M, Mammeri H, Pluquet E, Guillon H, Rousseau F, Canarelli B, et al. Value of Xpert MRSA/SA blood culture assay on the Gene Xpert(R) Dx System for rapid detection of Staphylococcus aureus and coagulase-negative staphylococci in patients with staphylococcal bacteremia. Diagn Microbiol Infect Dis. 2013;75:139–43.CrossRefPubMed Biendo M, Mammeri H, Pluquet E, Guillon H, Rousseau F, Canarelli B, et al. Value of Xpert MRSA/SA blood culture assay on the Gene Xpert(R) Dx System for rapid detection of Staphylococcus aureus and coagulase-negative staphylococci in patients with staphylococcal bacteremia. Diagn Microbiol Infect Dis. 2013;75:139–43.CrossRefPubMed
19.
go back to reference Carbonnelle E, Beretti JL, Cottyn S, Quesne G, Berche P, Nassif X, et al. Rapid identification of Staphylococci isolated in clinical microbiology laboratories by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol. 2007;45:2156–61.CrossRefPubMedPubMedCentral Carbonnelle E, Beretti JL, Cottyn S, Quesne G, Berche P, Nassif X, et al. Rapid identification of Staphylococci isolated in clinical microbiology laboratories by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol. 2007;45:2156–61.CrossRefPubMedPubMedCentral
20.
go back to reference Seng P, Drancourt M, Gouriet F, La Scola B, Fournier PE, Rolain JM, et al. Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clin Infect Dis. 2009;49:543–51.CrossRefPubMed Seng P, Drancourt M, Gouriet F, La Scola B, Fournier PE, Rolain JM, et al. Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clin Infect Dis. 2009;49:543–51.CrossRefPubMed
21.
go back to reference Comité de l’antibiogramme de la Société Française de Microbiologie (CA-SFM EUCAST). Détermination de la sensibilité aux antibiotiques, 2014. Comité de l’antibiogramme de la Société Française de Microbiologie (CA-SFM EUCAST). Détermination de la sensibilité aux antibiotiques, 2014.
22.
go back to reference Tzouvelekis LS, Tzelepi E, Prinarakis E, Gazouli M, Katrahoura A, Giakkoupi P, et al. Sporadic emergence of Klebsiella pneumoniae strains resistant to cefepime and cefpirome in Greek hospitals. J Clin Microbiol. 1998;36:266–8.PubMedPubMedCentral Tzouvelekis LS, Tzelepi E, Prinarakis E, Gazouli M, Katrahoura A, Giakkoupi P, et al. Sporadic emergence of Klebsiella pneumoniae strains resistant to cefepime and cefpirome in Greek hospitals. J Clin Microbiol. 1998;36:266–8.PubMedPubMedCentral
23.
go back to reference Skibsted U, Baggesen DL, Dessau R, Lisby G. Random amplification of polymorphic DNA (RAPD), pulsed-field gel electrophoresis (PFGE) and phage-typing in the analysis of a hospital outbreak of Salmonella enteritidis. J Hosp Infect. 1998;38:207–16.CrossRefPubMed Skibsted U, Baggesen DL, Dessau R, Lisby G. Random amplification of polymorphic DNA (RAPD), pulsed-field gel electrophoresis (PFGE) and phage-typing in the analysis of a hospital outbreak of Salmonella enteritidis. J Hosp Infect. 1998;38:207–16.CrossRefPubMed
24.
go back to reference Manan N, Chin Chin S, Abdullah N, Wan H. Differentiation of Lactobacillus-probiotic strains by visual comparison of random amplified polymorphic DNA (RAPD) profiles. Afr J Biotechnol. 2009;8:3964–9. Manan N, Chin Chin S, Abdullah N, Wan H. Differentiation of Lactobacillus-probiotic strains by visual comparison of random amplified polymorphic DNA (RAPD) profiles. Afr J Biotechnol. 2009;8:3964–9.
25.
go back to reference Youssef M, Al Shurman A, Chachaty E, Bsoul AR, Andremont A. Use of molecular typing to investigate bacterial translocation from the intestinal tract in malnourished children with gram-negative bacteremia. Clin Microbiol Infect. 1998;4:70–4.CrossRefPubMed Youssef M, Al Shurman A, Chachaty E, Bsoul AR, Andremont A. Use of molecular typing to investigate bacterial translocation from the intestinal tract in malnourished children with gram-negative bacteremia. Clin Microbiol Infect. 1998;4:70–4.CrossRefPubMed
26.
go back to reference van der Heijden KM, van der Heijden IM, Galvao FH, Lopes CG, Costa SF, Abdala E, et al. Intestinal translocation of clinical isolates of vancomycin-resistant Enterococcus faecalis and ESBL-producing Escherichia coli in a rat model of bacterial colonization and liver ischemia/reperfusion injury. Plos ONE. 2014;9:e108453.CrossRefPubMedPubMedCentral van der Heijden KM, van der Heijden IM, Galvao FH, Lopes CG, Costa SF, Abdala E, et al. Intestinal translocation of clinical isolates of vancomycin-resistant Enterococcus faecalis and ESBL-producing Escherichia coli in a rat model of bacterial colonization and liver ischemia/reperfusion injury. Plos ONE. 2014;9:e108453.CrossRefPubMedPubMedCentral
27.
go back to reference Garcia-Tsao G, Lee FY, Barden GE, Cartun R, West AB. Bacterial translocation to mesenteric lymph nodes is increased in cirrhotic rats with ascites. Gastroenterology. 1995;108:1835–41.CrossRefPubMed Garcia-Tsao G, Lee FY, Barden GE, Cartun R, West AB. Bacterial translocation to mesenteric lymph nodes is increased in cirrhotic rats with ascites. Gastroenterology. 1995;108:1835–41.CrossRefPubMed
28.
go back to reference Guarner C, Gonzalez-Navajas JM, Sanchez E, Soriando G, Frances R, Chiva M, et al. The detection of bacterial DNA in blood of rats with CCl4-induced cirrhosis with ascites represents episodes of bacterial translocation. Hepatology. 2006;44:633–9.CrossRefPubMed Guarner C, Gonzalez-Navajas JM, Sanchez E, Soriando G, Frances R, Chiva M, et al. The detection of bacterial DNA in blood of rats with CCl4-induced cirrhosis with ascites represents episodes of bacterial translocation. Hepatology. 2006;44:633–9.CrossRefPubMed
29.
go back to reference Guarner C, Runyon BA, Young S, Heck M, Sheikh MY. Intestinal bacterial overgrowth and bacterial translocation in cirrhotic rats with ascites. J Hepatol. 1997;26:1372–8.CrossRefPubMed Guarner C, Runyon BA, Young S, Heck M, Sheikh MY. Intestinal bacterial overgrowth and bacterial translocation in cirrhotic rats with ascites. J Hepatol. 1997;26:1372–8.CrossRefPubMed
30.
go back to reference Llovet JM, Bartoli R, Planas R, Cabre E, Jimenez M, Urban A, et al. Bacterial translocation in cirrhotic rats. Its role in the development of spontaneous bacterial peritonitis. Gut. 1994;35:1648–52.CrossRefPubMedPubMedCentral Llovet JM, Bartoli R, Planas R, Cabre E, Jimenez M, Urban A, et al. Bacterial translocation in cirrhotic rats. Its role in the development of spontaneous bacterial peritonitis. Gut. 1994;35:1648–52.CrossRefPubMedPubMedCentral
31.
go back to reference Such J, Frances R, Munoz C, Zapater P, Casellas JA, Cifuentes A, et al. Detection and identification of bacterial DNA in patients with cirrhosis and culture-negative, nonneutrocytic ascites. Hepatology. 2002;36:135–41.CrossRefPubMed Such J, Frances R, Munoz C, Zapater P, Casellas JA, Cifuentes A, et al. Detection and identification of bacterial DNA in patients with cirrhosis and culture-negative, nonneutrocytic ascites. Hepatology. 2002;36:135–41.CrossRefPubMed
32.
go back to reference Berg RD. Bacterial translocation from the gastrointestinal tract. Trends Microbiol. 1995;3:149–54.CrossRefPubMed Berg RD. Bacterial translocation from the gastrointestinal tract. Trends Microbiol. 1995;3:149–54.CrossRefPubMed
33.
go back to reference El Solh N, Fouace JM, Pillet J, Chabbert YA. Plasmid DNA content of multiresistant Staphylococcus aureus strains. Ann Microbiol. 1981;132B:131–56. El Solh N, Fouace JM, Pillet J, Chabbert YA. Plasmid DNA content of multiresistant Staphylococcus aureus strains. Ann Microbiol. 1981;132B:131–56.
34.
go back to reference El Solh N, Fouace JM, Shalita Z, Bouanchaud DH, Novick RP, Chabbert YA. Epidemiological and structural studies of Staphylococcus aureus R plasmids mediating resistance to tobramycin and streptogramin. Plasmid. 1980;4:117–20.CrossRefPubMed El Solh N, Fouace JM, Shalita Z, Bouanchaud DH, Novick RP, Chabbert YA. Epidemiological and structural studies of Staphylococcus aureus R plasmids mediating resistance to tobramycin and streptogramin. Plasmid. 1980;4:117–20.CrossRefPubMed
35.
go back to reference Le Goffic F, Capmau ML, Abbe J, Cerceau C, Dublanchet A, Duval J. Plasmid mediated pristinamycin resistance: PH 1A, a pristinamycin 1A hydrolase. Ann Microbiol. 1977;128B:471–4. Le Goffic F, Capmau ML, Abbe J, Cerceau C, Dublanchet A, Duval J. Plasmid mediated pristinamycin resistance: PH 1A, a pristinamycin 1A hydrolase. Ann Microbiol. 1977;128B:471–4.
36.
go back to reference Le Goffic F, Capmau ML, Bonnet D, Cerceau C, Soussy C, Dublanchet A, et al. Plasmid-mediated pristinamycin resistance. PAC IIA: a new enzyme which modifies pristinamycin IIA. J Antibiot. 1977;30:665–9.CrossRefPubMed Le Goffic F, Capmau ML, Bonnet D, Cerceau C, Soussy C, Dublanchet A, et al. Plasmid-mediated pristinamycin resistance. PAC IIA: a new enzyme which modifies pristinamycin IIA. J Antibiot. 1977;30:665–9.CrossRefPubMed
37.
go back to reference Garcia-Alvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, et al. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis. 2011;11:595–603.CrossRefPubMedPubMedCentral Garcia-Alvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, et al. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis. 2011;11:595–603.CrossRefPubMedPubMedCentral
38.
go back to reference Ito T, Katayama Y, Hiramatsu K. Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrob Agents Chemother. 1999;43:1449–58.PubMedPubMedCentral Ito T, Katayama Y, Hiramatsu K. Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrob Agents Chemother. 1999;43:1449–58.PubMedPubMedCentral
39.
40.
go back to reference Stegger M, Andersen PS, Kearns A, Pichon B, Holmes MA, Edwards G, et al. Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecA (LGA251). Clin Microbiol Infect. 2012;18:395–400.CrossRefPubMed Stegger M, Andersen PS, Kearns A, Pichon B, Holmes MA, Edwards G, et al. Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecA (LGA251). Clin Microbiol Infect. 2012;18:395–400.CrossRefPubMed
41.
go back to reference Naphade SR, Durve AA, Bhot M, Varghese J, Chandra N. Isolation, characterization and identification of pesticide tolerating bacteria from garden soil. Eur J Exp Biol. 2012;2:1943–51. Naphade SR, Durve AA, Bhot M, Varghese J, Chandra N. Isolation, characterization and identification of pesticide tolerating bacteria from garden soil. Eur J Exp Biol. 2012;2:1943–51.
42.
go back to reference Harishankar MK, Sasikala C, Ramya M. Efficiency of the intestinal bacteria in the degradation of the toxic pesticide, chlorpyrifos. 3 Biotech. 2013;3:137–42.CrossRef Harishankar MK, Sasikala C, Ramya M. Efficiency of the intestinal bacteria in the degradation of the toxic pesticide, chlorpyrifos. 3 Biotech. 2013;3:137–42.CrossRef
43.
go back to reference Kale SP, Murthy NB, Raghu K. Effect of carbofuran, carbaryl, and their metabolites on the growth of Rhizobium sp. and Azotobacter chroococcum. Bull Environ Contam Toxicol. 1989;42:769–72.CrossRefPubMed Kale SP, Murthy NB, Raghu K. Effect of carbofuran, carbaryl, and their metabolites on the growth of Rhizobium sp. and Azotobacter chroococcum. Bull Environ Contam Toxicol. 1989;42:769–72.CrossRefPubMed
44.
go back to reference Shafiani S, Malik A. Tolerance of pesticides and antibiotic resistance in bacteria isolated from wastewater-irrigated soil. World J Microbiol Biotechnol. 2003;19:897–901.CrossRef Shafiani S, Malik A. Tolerance of pesticides and antibiotic resistance in bacteria isolated from wastewater-irrigated soil. World J Microbiol Biotechnol. 2003;19:897–901.CrossRef
45.
go back to reference Sepperumal U, Palanimanickam A, Sivalingam G. Plasmid mediated endosulfan degradation by Bacillus ciradans and Acinetobacter species. J Microbiol Biotech Res. 2013;3:15–20. Sepperumal U, Palanimanickam A, Sivalingam G. Plasmid mediated endosulfan degradation by Bacillus ciradans and Acinetobacter species. J Microbiol Biotech Res. 2013;3:15–20.
46.
47.
go back to reference Ducluzeau R, Raibaud P. Les interactions bactériennes dans le tube digestif. Rev sci tech Off int Epiz. 1989;8:291–311.CrossRef Ducluzeau R, Raibaud P. Les interactions bactériennes dans le tube digestif. Rev sci tech Off int Epiz. 1989;8:291–311.CrossRef
48.
go back to reference Raibaud P, Ducluzeau R. Etude de la colonisation bactérienne du tractus gastro-intestinal à l’aide de modèles expérimentaux. Rev sci tech Off int Epiz. 1989;8:361–73.CrossRef Raibaud P, Ducluzeau R. Etude de la colonisation bactérienne du tractus gastro-intestinal à l’aide de modèles expérimentaux. Rev sci tech Off int Epiz. 1989;8:361–73.CrossRef
49.
go back to reference Raibaud P, Dickison AB, Sacquet E, Charlier H, Mocquot G. La microflore du tube digestif du rat. II. Dénombrement de différents genres microbiens dans l’estomac et l’intestin de rats conventionnels. Variations quantitatives individuelles et en fonction de l’âge. Ann Inst Pasteur. 1966;110:861–76. Raibaud P, Dickison AB, Sacquet E, Charlier H, Mocquot G. La microflore du tube digestif du rat. II. Dénombrement de différents genres microbiens dans l’estomac et l’intestin de rats conventionnels. Variations quantitatives individuelles et en fonction de l’âge. Ann Inst Pasteur. 1966;110:861–76.
Metadata
Title
Use of molecular typing to investigate bacterial translocation from the intestinal tract of chlorpyrifos-exposed rats
Authors
Claire Joly Condette
Bertin Elion Dzon
Farida Hamdad
Maurice Biendo
Véronique Bach
Hafida Khorsi-Cauet
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2016
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-016-0129-x

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