Antipsychotics and the gut microbiome: Olanzapine-induced metabolic dysfunction is attenuated by antibiotic administration in the rat

Translational Psychiatry

Volumn 3, Issue , 2013, Pages

  Davey, K J ^a,b   Cotter, P D ^a,c   O'Sullivan, O ^a,c   Crispie, F ^c   Dinan, T G ^a,b   Cryan, J F ^a,b   O'Mahony, S M ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c ASHTOWN FOOD RESEARCH CENTRE   (Ireland)

Author keywords

antipsychotics; metabolism; microbiota; obesity; olanzapine; weight gain

Indexed keywords

CD68 ANTIGEN; FATTY ACID; FATTY ACID SYNTHASE; METRONIDAZOLE; NEOMYCIN; OLANZAPINE; POLYMYXIN B; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; ANTIINFECTIVE AGENT; BENZODIAZEPINE DERIVATIVE; NEUROLEPTIC AGENT;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC THERAPY; ANTIGEN EXPRESSION; ARTICLE; BODY WEIGHT; CELL INFILTRATION; CONTROLLED STUDY; ENZYME BLOOD LEVEL; FATTY ACID BLOOD LEVEL; FEMALE; FIRMICUTES; FOOD INTAKE; GENE EXPRESSION; INTESTINE FLORA; LIPID STORAGE; LOCOMOTION; MACROPHAGE; METABOLIC SYNDROME X; NONHUMAN; QUANTITATIVE INSULIN SENSITIVITY CHECK INDEX; RAT; UTERUS; WEIGHT GAIN; ANIMAL; BLOOD; DRUG EFFECT; IMMUNOLOGY; INTESTINE; INTRAABDOMINAL FAT; MICROBIOLOGY; MICROFLORA; SPRAGUE DAWLEY RAT;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIPSYCHOTIC AGENTS; BENZODIAZEPINES; FATTY ACIDS, NONESTERIFIED; FEMALE; INTESTINES; INTRA-ABDOMINAL FAT; MACROPHAGES; METRONIDAZOLE; MICROBIOTA; NEOMYCIN; POLYMYXIN B; RATS; RATS, SPRAGUE-DAWLEY; WEIGHT GAIN;

EID: 84885135911     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2013.83     Document Type: Article

References (55)

1. Albaugh VL, Judson JG, She P, Lang CH, Maresca KP, Joyal JL et al. Olanzapine promotes fat accumulation in male rats by decreasing physical activity, repartitioning energy and increasing adipose tissue lipogenesis while impairing lipolysis. Mol Psychiatry 2011; 16: 569-581.
2. Newcomer JW. Metabolic risk during antipsychotic treatment. Clin Ther 2004; 26: 1936-1946.
3. Correll CU, Manu P, Olshanskiy V, Napolitano B, Kane JM, Malhotra AK. Cardiometabolic risk of second-Generation antipsychotic medications during first-Time use in children and adolescents. JAMA 2009; 302: 1765-1773.
4. Farwell WR, Stump TE, Wang J, Tafesse E, L?Italien G, Tierney WM. Weight gain and new onset diabetes associated with olanzapine and risperidone. J Gen Intern Med 2004; 19: 1200-1205.
5. Foley Dl, Morley KI. Systematic review of early cardiometabolic outcomes of the first treated episode of psychosis. Arch Gen Psychiatry 2011; 68: 609-616.
6. Osby U, Correia N, Brandt L, Ekbom A, Sparen P. Mortality and causes of death in schizophrenia in Stockholm County, Sweden. Schizophr Res 2000; 45: 21-28.
7. Tiihonen J, Lonnqvist J, Wahlbeck K, Klaukka T, Niskanen L, Tanskanen A et al. No mental health without physical health. Lancet 2011; 377: 611.
8. Maayan L, Vakhrusheva J, Correll CU. Effectiveness of medications used to attenuate antipsychotic-Related weight gain and metabolic abnormalities: A systematic review and meta-Analysis. Neuropsychopharmacology 2010; 35: 1520-1530.
9. Boyda HN, Tse L, Procyshyn RM, Honer WG, Barr AM. Preclinical models of antipsychotic drug-Induced metabolic side effects. Trends Pharmacolog Sci 2010; 31: 484-497.
10. Newcomer JW. Second-Generation (atypical) antipsychotics and metabolic effects: A comprehensive literature review. CNS Drugs 2005; 19(Suppl 1): 1-93.
11. Davoodi N, Kalinichev M, Korneev SA, Clifton PG. Hyperphagia and increased meal size are responsible for weight gain in rats treated sub-Chronically with olanzapine. Psychopharmacology (Berl) 2009; 203: 693-702.
12. Kirk SL, Glazebrook J, Grayson B, Neill JC, Reynolds GP. Olanzapine-Induced weight gain in the rat: Role of 5-HT2C and histamine H1 receptors. Psychopharmacology (Berl) 2009; 207: 119-125.
13. Matsui-Sakata A, Ohtani H, Sawada Y. Receptor occupancy-Based analysis of the contributions of various receptors to antipsychotics-Induced weight gain and diabetes mellitus. Drug Metab Pharmacokinet 2005; 20: 368-378.
14. Reynolds GP. Pharmacogenetic aspects of antipsychotic drug-Induced weight gain-A critical review. Clin Psychopharmacol Neurosci 2012; 10: 71-77.
15. Minet-Ringuet J, Even PC, Goubern M, Tome D, De Beaurepaire R. Long term treatment with olanzapine mixed with the food in male rats induces body fat deposition with no increase in body weight and no thermogenic alteration. Appetite 2006; 46: 254-262.
16. Victoriano M, Hermier D, Even PC, Fromentin G, Huneau JF, Tome D et al. Early perturbation in feeding behaviour and energy homeostasy in olanzapine-Treated rats. Psychopharmacology (Berl) 2009; 206: 167-176.
17. Zhang Z-J, Yao Z-J, Liu WEN, Fang QUN, Reynolds GP. Effects of antipsychotics on fat deposition and changes in leptin and insulin levels: Magnetic resonance imaging study of previously untreated people with schizophrenia. Br J Psychiatry 2004; 184: 58-62.
18. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-Bacterial mutualism in the human intestine. Science 2005; 307: 1915-1920.
19. Fraher MH, O?Toole PW, Quigley EMM. Techniques used to characterize the gut microbiota: A guide for the clinician. Nat Rev Gastroenterol Hepatol 2012; 9: 312-322.
20. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 2004; 101: 15718-15723.
21. Backhed F, Manchester JK, Semenkovich CF, Gordon JI. Mechanisms underlying the resistance to diet-Induced obesity in germ-Free mice. Proc Natl Acad Sci USA 2007; 104: 979-984.
22. Nadal I, Santacruz A, Marcos A, Warnberg J, Garagorri M, Moreno LA et al. Shifts in clostridia, bacteroides and immunoglobulin-Coating fecal bacteria associated with weight loss in obese adolescents. Int J Obes 2009; 33: 758-767.
23. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE et al. A core gut microbiome in obese and lean twins. Nature 2009; 457: 480-U7.
24. Zaneveld J, Turnbaugh PJ, Lozupone C, Ley RE, Hamady M, Gordon JI et al. Host-Bacterial coevolution and the search for new drug targets. Curr Opin Chem Biol 2008; 12: 109-114.
25. Jia W, Li HK, Zhao LP, Nicholson JK. Gut microbiota: A potential new territory for drug targeting. Nat Rev Drug Discov 2008; 7: 123-129.
26. Cani PD, Bibiloni R, Knauf C, Neyrinck AM, Neyrinck AM, Delzenne NM et al. Changes in gut microbiota control metabolic endotoxemia-Induced inflammation in high-Fat diet-Induced obesity and diabetes in mice. Diabetes 2008; 57: 1470-1481.
27. Murphy EF, Cotter PD, Hogan A, O?Sullivan O, Joyce A, Fouhy F et al. Divergent metabolic outcomes arising from targeted manipulation of the gut microbiota in diet-Induced obesity. Gut 2012; 62: 220-226.
28. Davey KJ, O?Mahony SM, Schellekens H, O?Sullivan O, Bienenstock J, Cotter PD et al. Gender-Dependent consequences of chronic olanzapine in the rat: Effects on body weight, inflammatory, metabolic and microbiota parameters. Psychopharmacology 2012; 221: 155-169.
29. Cooper GD, Pickavance LC, Wilding JP, Halford JC, Goudie AJ. A parametric analysis of olanzapine-Induced weight gain in female rats. Psychopharmacology (Berl) 2005; 181: 80-89.
30. Juno RJ, Knott AW, Jarboe MD, Profitt SA, Erwin CR, Warner BW. Characterization of small bowel resection and intestinal adaptation in germ-Free rats. Surgery 2003; 134: 582-589.
31. Claesson C, Nilsson LE, Kronvall G, Walder M, Sorberg M. Antimicrobial activity of tigecycline and comparative agents against clinical isolates of staphylococci and enterococci from ICUs and general hospital wards at three Swedish university hospitals. Scand J Infect Dis 2009; 41: 171-181.
32. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 1997; 25: 3389-3402.
33. Urich T, Lanzen A, Qi J, Huson DH, Schleper C, Schuster SC. Simultaneous assessment of soil microbial community structure and function through analysis of the meta-Transcriptome. PLoS One 2008; 3: E2527.
34. Huson DH, Auch AF, Qi J, Schuster SC. MEGAN analysis of metagenomic data. Genome Res 2007; 17: 377-386.
35. Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G et al. Quantitative insulin sensitivity check index: A simple accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 2000; 85: 2402-2410.
36. Fell MJ, Anjum N, Dickinson K, Marshall KM, Peltola LM, Vickers S et al. The distinct effects of subchronic antipsychotic drug treatment on macronutrient selection, body weight, adiposity, and metabolism in female rats. Psychopharmacology (Berl) 2007; 194: 221-231.
37. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA [Article] 2005; 102: 11070-11075.
38. Backhed F. Programming of host metabolism by the gut microbiota. Ann Nutr Metab 2011; 58(Suppl): 244-252.
39. Burcelin R, Serino M, Chabo C, Blasco-Baque V, Amar J. Gut microbiota and diabetes: From pathogenesis to therapeutic perspective. Acta Diabetol 2011; 48: 257-273.
40. Cummings JH, Antoine JM, Azpiroz F, Bourdet-Sicard R, Brandtzaeg P, Calder PC et al. PASSCLAIM-Gut health and immunity. Eur J Nutr 2004; 43: 118-173.
41. Jensen MD. Role of body fat distribution and the metabolic complications of obesity. J Clin Endocrinol Metab 2008; 93(Suppl 1): S57-S63.
42. Kamphues J. Antibiotic growth promoters in animal nutrition. Berliner Und Munchener Tierarztliche Wochenschrift 1999; 112: 370-379.
43. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003; 112: 1796-1808.
44. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res [Article] 2005; 46: 2347-2355.
45. Wang C-J, Zhang Z-J, Sun J, Zhang X-B, Mou X-D, Zhang X-R et al. Serum free fatty acids and glucose metabolism, insulin resistance in schizophrenia with chronic antipsychotics. Biol Psychiatry 2006; 60: 1309-1313.
46. Jassim G, Skrede S, Jesus Vazquez M, Wergedal H, Vik-Mo AO, Lunder N et al. Acute effects of orexigenic antipsychotic drugs on lipid and carbohydrate metabolism in rat. Psychopharmacology 2012; 219: 783-794.
47. Pegorier J-P, CdL May, Girard J. Control of Gene Expression by Fatty Acids. J Nutr 2004; 134: 2444S-2449SS.
48. Cani PD, Delzenne NM. The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des [Review] 2009; 15: 1546-1558.
49. Gosmain Y, Dif N, Berbe V, Loizon E, Rieusset J, Vidal H et al. Regulation of SREBP-1 expression and transcriptional action on HKII and FAS genes during fasting and refeeding in rat tissues. J Lipid Res 2005; 46: 697-705.
50. Cacho J, Sevillano J, De Castro J, Herrera E, Ramos MP. Validation of simple indexes to assess insulin sensitivity during pregnancy in Wistar and Sprague-Dawley rats. Am J Physiol Endocrinol Metab 2008; 295: E1269-E1276.
51. Houseknecht KL, Robertson AS, Zavadoski W, Gibbs EM, Johnson DE, Rollema H. Acute effects of atypical antipsychotics on whole-Body insulin resistance in rats: Implications for adverse metabolic effects. Neuropsychopharmacology 2007; 32: 289-297.
52. Smith RC, Lindenmayer JP, Davis JM, Kelly E, Viviano TF, Cornwell J et al. Effects of olanzapine and risperidone on glucose metabolism and insulin sensitivity in chronic schizophrenic patients with long-Term antipsychotic treatment: A randomized 5-Month study. J Clin Psychiatry 2009; 70: 1501-1513.
53. Chintoh AF, Mann SW, Lam L, Lam C, Cohn TA, Fletcher PJ et al. Insulin resistance and decreased glucose-Stimulated insulin secretion after acute olanzapine administration. J Clin Psychopharmacol 2008; 28: 494-499.
54. Mallappa RH, Rokana N, Duary RK, Panwar H, Batish VK, Grover S. Management of metabolic syndrome through probiotic and prebiotic interventions. Indian J Endocrinol Metab 2012; 16: 20-27.
55. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB et al. Cross-Talk between Akkermansia muciniphila and intestinal epithelium controls diet-Induced obesity. Proc Natl Acad Sci USA 2013; 110: 9066-9071.