Chemotherapy-driven dysbiosis in the intestinal microbiome

Alimentary Pharmacology and Therapeutics

Volumn 42, Issue 5, 2015, Pages 515-528

  Montassier, E ^a,b   Gastinne, T ^c   Vangay, P ^d   Al Ghalith, G A ^b,d   Bruley Des Varannes, S ^c   Massart, S ^e   Moreau, P ^c   Potel, G ^a   De La Cochetiere M F ^a   Batard, E ^a   Knights, D ^b,d  

^a UNIVERSITÉ DE NANTES   (France)

^b University of Minnesota   (United States)

^c NANTES UNIVERSITY HOSPITAL   (France)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CARMUSTINE; COTRIMOXAZOLE; CYTARABINE; ETOPOSIDE; GLYCAN; MELPHALAN; PENICILLIN V; XENOBIOTIC AGENT; ANTINEOPLASTIC AGENT; RNA 16S;

ABDOMINAL PAIN; ACTINOBACTERIA; ADULT; ANTIBIOTIC PROPHYLAXIS; ARTICLE; BACTERIUM; BIODEGRADATION; CARBOHYDRATE METABOLISM; CELL DEATH; CELL GROWTH; CHEMOTHERAPY; CLINICAL ARTICLE; DIARRHEA; DNA SEQUENCE; DYSBIOSIS; ENERGY METABOLISM; FECES ANALYSIS; FECES MICROFLORA; FEMALE; FIRMICUTES; HUMAN; INTESTINAL MICROBIOME; MALE; MICROBIAL COMMUNITY; MICROBIOME; NAUSEA; NONHODGKIN LYMPHOMA; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEOBACTERIA; SIGNAL TRANSDUCTION; TREATMENT DURATION; VITAMIN METABOLISM; VOMITING; CHEMICALLY INDUCED; DRUG EFFECTS; FECES; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HIGH THROUGHPUT SEQUENCING; INTESTINE FLORA; LYMPHOMA, NON-HODGKIN; METABOLISM; MICROBIOLOGY; MIDDLE AGED; MUCOSA INFLAMMATION; PROCEDURES;

ACTINOBACTERIA; ADULT; ANTINEOPLASTIC AGENTS; DYSBIOSIS; FECES; FEMALE; FIRMICUTES; GASTROINTESTINAL MICROBIOME; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LYMPHOMA, NON-HODGKIN; MALE; MIDDLE AGED; MUCOSITIS; PROTEOBACTERIA; RNA, RIBOSOMAL, 16S;

EID: 84938555496     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/apt.13302     Document Type: Article

References (73)

1. Vose JM, Anderson JR, Kessinger A, et al,. High-dose chemotherapy and autologous hematopoietic stem-cell transplantation for aggressive non-Hodgkin's lymphoma. J Clin Oncol 1993; 11: 1846-51.
2. Elting LS, Cooksley C, Chambers M, Cantor SB, Manzullo E, Rubenstein EB,. The burdens of cancer therapy. Clinical and economic outcomes of chemotherapy-induced mucositis. Cancer 2003; 98: 1531-9.
3. Blijlevens NMA, Lutgens LCHW, Schattenberg AVMB, Donnelly JP,. Citrulline: a potentially simple quantitative marker of intestinal epithelial damage following myeloablative therapy. Bone Marrow Transplant 2004; 34: 193-6.
4. Keefe DM, Brealey J, Goland GJ, Cummins AG,. Chemotherapy for cancer causes apoptosis that precedes hypoplasia in crypts of the small intestine in humans. Gut 2000; 47: 632-7.
5. Sonis ST,. The pathobiology of mucositis. Nat Rev Cancer 2004; 4: 277-84.
6. Marin M, Gudiol C, Ardanuy C, et al,. Bloodstream infections in neutropenic patients with cancer: differences between patients with haematological malignancies and solid tumours. J Infect 2014; 69: 417-23.
7. Touchefeu Y, Montassier E, Nieman K, et al,. Systematic review: the role of the gut microbiota in chemotherapy- or radiation-induced gastrointestinal mucositis-current evidence and potential clinical applications. Aliment Pharmacol Ther 2014; 40: 409-21.
8. Van Vliet MJ, Harmsen HJM, de Bont ESJM, Tissing WJE,. The role of intestinal microbiota in the development and severity of chemotherapy-induced mucositis. PLoS Pathog 2010; 6: e1000879.
9. Montassier E, Batard E, Massart S, et al,. 16S rRNA gene pyrosequencing reveals shift in patient faecal microbiota during high-dose chemotherapy as conditioning regimen for bone marrow transplantation. Microb Ecol 2014; 67: 690-9.
10. Andersson AF, Lindberg M, Jakobsson H, Bäckhed F, Nyrén P, Engstrand L,. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE 2008; 3: e2836.
11. Caporaso JG, Kuczynski J, Stombaugh J, et al,. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7: 335-6.
12. DeSantis TZ, Hugenholtz P, Larsen N, et al,. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006; 72: 5069-72.
13. Knights D, Costello EK, Knight R,. Supervised classification of human microbiota. FEMS Microbiol Rev 2011; 35: 343-59.
14. Yatsunenko T, Rey FE, Manary MJ, et al,. Human gut microbiome viewed across age and geography. Nature 2012; 486: 222-7.
15. Lozupone CA, Li M, Campbell TB, et al,. Alterations in the gut microbiota associated with HIV-1 infection. Cell Host Microbe 2013; 14: 329-39.
16. Langille MGI, Zaneveld J, Caporaso JG, et al,. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 2013; 31: 814-21.
17. Team RC. R: a Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2012) ISBN 3-900051-07-0.
18. Saito R, Smoot ME, Ono K, et al,. A travel guide to Cytoscape plugins. Nat Methods 2012; 9: 1069-76.
19. Dethlefsen L, Relman DA,. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci USA 2011; 108: 4554-61.
20. Rooks MG, Veiga P, Wardwell-Scott LH, et al,. Gut microbiome composition and function in experimental colitis during active disease and treatment-induced remission. ISME J 2014; 8: 1403-17.
21. Morgan XC, Tickle TL, Sokol H, et al,. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012; 13: R79.
22. Schwab C, Berry D, Rauch I, et al,. Longitudinal study of murine microbiota activity and interactions with the host during acute inflammation and recovery. ISME J 2014; 8: 1101-14.
23. Gevers D, Kugathasan S, Denson LA, et al,. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 2014; 15: 382-92.
24. Ottemann KM, Miller JF,. Roles for motility in bacterial-host interactions. Mol Microbiol 1997; 24: 1109-17.
25. Ramos HC, Rumbo M, Sirard J-C,. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol 2004; 12: 509-17.
26. Lyte M, Vulchanova L, Brown DR,. Stress at the intestinal surface: catecholamines and mucosa-bacteria interactions. Cell Tissue Res 2011; 343: 23-32.
27. Freestone PPE, Walton NJ, Haigh RD, Lyte M,. Influence of dietary catechols on the growth of enteropathogenic bacteria. Int J Food Microbiol 2007; 119: 159-69.
28. Jha G, Rajeshwari R, Sonti RV,. Bacterial type two secretion system secreted proteins: double-edged swords for plant pathogens. Mol Plant Microbe Interact 2005; 18: 891-8.
29. Sandkvist M,. Type II secretion and pathogenesis. Infect Immun 2001; 69: 3523-35.
30. Tong M, McHardy I, Ruegger P, et al,. Reprograming of gut microbiome energy metabolism by the FUT2 Crohn's disease risk polymorphism. ISME J 2014; 8: 2193-206.
31. De Fazio L, Cavazza E, Spisni E, et al,. Longitudinal analysis of inflammation and microbiota dynamics in a model of mild chronic dextran sulfate sodium-induced colitis in mice. World J Gastroenterol 2014; 20: 2051-61.
32. Huttenhower C, Knight R, Brown CT, et al,. Advancing the microbiome research community. Cell 2014; 159: 227-30.
33. Manichanh C, Rigottier-Gois L, Bonnaud E, et al,. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 2006; 55: 205-11.
34. Turnbaugh PJ, Hamady M, Yatsunenko T, et al,. A core gut microbiome in obese and lean twins. Nature 2009; 457: 480-4.
35. Claesson MJ, Jeffery IB, Conde S, et al,. Gut microbiota composition correlates with diet and health in the elderly. Nature 2012; 488: 178-84.
36. Fijlstra M, Ferdous M, Koning AM, Rings EHHM, Harmsen HJM, Tissing WJE,. Substantial decreases in the number and diversity of microbiota during chemotherapy-induced gastrointestinal mucositis in a rat model. Support Care Cancer 2015; 23: 1513-22.
37. Bergman EN,. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev 1990; 70: 567-90.
38. Giles GI, Jacob C,. Reactive sulfur species: an emerging concept in oxidative stress. Biol Chem 2002; 383: 375-88.
39. Ashoori M, Saedisomeolia A,. Riboflavin (vitamin B2) and oxidative stress: a review. Br J Nutr 2014; 000: 1-7.
40. Mytilineou C, Kramer BC, Yabut JA,. Glutathione depletion and oxidative stress. Parkinsonism Relat Disord 2002; 8: 385-7.
41. Reedquist KA, Tak PP,. Signal transduction pathways in chronic inflammatory autoimmune disease: small GTPases. Open Rheumatol J 2012; 6: 259-72.
42. Lakhdari O, Tap J, Béguet-Crespel F, et al,. Identification of NF-κB modulation capabilities within human intestinal commensal bacteria. J Biomed Biotechnol 2011; 2011: 282356.
43. Khokhlova EV, Smeianov VV, Efimov BA, Kafarskaia LI, Pavlova SI, Shkoporov AN,. Anti-inflammatory properties of intestinal Bifidobacterium strains isolated from healthy infants. Microbiol Immunol 2012; 56: 27-39.
44. Riedel C-U, Foata F, Philippe D, Adolfsson O, Eikmanns B-J, Blum S,. Anti-inflammatory effects of bifidobacteria by inhibition of LPS-induced NF-kappaB activation. World J Gastroenterol 2006; 12: 3729-35.
45. Segain JP, Raingeard de la Blétière D, Bourreille A, et al,. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut 2000; 47: 397-403.
46. Wang Y, Xiang G-S, Kourouma F, Umar S,. Citrobacter rodentium-induced NF-kappaB activation in hyperproliferating colonic epithelia: role of p65 (Ser536) phosphorylation. Br J Pharmacol 2006; 148: 814-24.
47. Garrett WS, Gallini CA, Yatsunenko T, et al,. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 2010; 8: 292-300.
48. Naik SR, Rupawalla EN, Sheth UK,. Anti-inflammatory activity of thiamine and nicotinic acid. Biochem Pharmacol 1970; 19: 2867-73.
49. Moallem SA, Hosseinzadeh H, Farahi S,. A study of acute and chronic anti-nociceptive and anti-inflammatory effects of thiamine in mice. Iran Biomed J 2008; 12: 173-8.
50. Verhasselt V, Buelens C, Willems F, De Groote D, Haeffner-Cavaillon N, Goldman M,. Bacterial lipopolysaccharide stimulates the production of cytokines and the expression of costimulatory molecules by human peripheral blood dendritic cells: evidence for a soluble CD14-dependent pathway. J Immunol 1950; 1997: 2919-25.
51. Carneiro-Filho BA, Lima IPF, Araujo DH, et al,. Intestinal barrier function and secretion in methotrexate-induced rat intestinal mucositis. Dig Dis Sci 2004; 49: 65-72.
52. Russo F, Linsalata M, Clemente C, et al,. The effects of fluorouracil, epirubicin, and cyclophosphamide (FEC60) on the intestinal barrier function and gut peptides in breast cancer patients: an observational study. BMC Cancer 2013; 13: 56.
53. Nejdfors P, Ekelund M, Weström BR, Willén R, Jeppsson B,. Intestinal permeability in humans is increased after radiation therapy. Dis Colon Rectum 2000; 43: 1582-7; discussion 1587-1588.
54. Melichar B, Zezulová M,. The significance of altered gastrointestinal permeability in cancer patients. Curr Opin Support Palliat Care 2011; 5: 47-54.
55. Resta-Lenert S, Barrett KE,. Probiotics and commensals reverse TNF-alpha- and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology 2006; 130: 731-46.
56. Strowski MZ, Wiedenmann B,. Probiotic carbohydrates reduce intestinal permeability and inflammation in metabolic diseases. Gut 2009; 58: 1044-5.
57. Ewaschuk JB, Diaz H, Meddings L, et al,. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am J Physiol Gastrointest Liver Physiol 2008; 295: G1025-34.
58. Canani RB, Costanzo MD, Leone L, Pedata M, Meli R, Calignano A,. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol 2011; 17: 1519-28.
59. Vázquez-Castellanos JF, Serrano-Villar S, Latorre A, et al,. Altered metabolism of gut microbiota contributes to chronic immune activation in HIV-infected individuals. Mucosal Immunol 2015; 8: 760-72.
60. Guo S, Al-Sadi R, Said HM, Ma TY,. Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. Am J Pathol 2013; 182: 375-87.
61. Eutamene H, Theodorou V, Schmidlin F, et al,. LPS-induced lung inflammation is linked to increased epithelial permeability: role of MLCK. Eur Respir J 2005; 25: 789-96.
62. Lee H-S, Han S-Y, Ryu K-Y, Kim D-H,. The degradation of glycosaminoglycans by intestinal microflora deteriorates colitis in mice. Inflammation 2009; 32: 27-36.
63. Burger-van Paassen N, Vincent A, Puiman PJ, et al,. The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection. Biochem J 2009; 420: 211-9.
64. Johansson MEV, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC,. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci USA 2008; 105: 15064-9.
65. Faure M, Mettraux C, Moennoz D, et al,. Specific amino acids increase mucin synthesis and microbiota in dextran sulfate sodium-treated rats. J Nutr 2006; 136: 1558-64.
66. Watanabe T, Ohara S, Miyazawa S, Saigenji K, Hotta K,. Augmentative effects of L-cysteine and methylmethionine sulfonium chloride on mucin secretion in rabbit gastric mucous cells. J Gastroenterol Hepatol 2000; 15: 45-52.
67. Watanabe T, Ohara S, Ichikawa T, Saigenji K, Hotta K,. Mechanisms for cytoprotection by vitamin U from ethanol-induced gastric mucosal damage in rats. Dig Dis Sci 1996; 41: 49-54.
68. Bergstrom KSB, Kissoon-Singh V, Gibson DL, et al,. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog 2010; 6: e1000902.
69. Montassier E, Batard E, Gastinne T, Potel G, de La Cochetière MF,. Recent changes in bacteremia in patients with cancer: a systematic review of epidemiology and antibiotic resistance. Eur J Clin Microbiol Infect Dis 2013; 32: 841-50.
70. Almyroudis NG, Fuller A, Jakubowski A, et al,. Pre- and post-engraftment bloodstream infection rates and associated mortality in allogeneic hematopoietic stem cell transplant recipients. Transpl Infect Dis 2005; 7: 11-7.
71. Poutsiaka DD, Price LL, Ucuzian A, Chan GW, Miller KB, Snydman DR,. Blood stream infection after hematopoietic stem cell transplantation is associated with increased mortality. Bone Marrow Transplant 2007; 40: 63-70.
72. Mikulska M, Del Bono V, Raiola AM, et al,. Enterococcal bloodstream infection after hematopoietic stem cell transplant: experience of a center with a low prevalence of vancomycin-resistant enterococci. Clin Infect Dis 2012; 55: 1744.
73. Blennow O, Ljungman P, Sparrelid E, Mattsson J, Remberger M,. Incidence, risk factors, and outcome of bloodstream infections during the pre-engraftment phase in 521 allogeneic hematopoietic stem cell transplantations. Transpl Infect Dis 2014; 16: 106-14.