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Research Paper

The gut microbiome contributes to somatic morphine withdrawal behavior and implicates a TLR2 mediated mechanism

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Article: 2242610 | Received 20 Apr 2023, Accepted 26 Jul 2023, Published online: 17 Aug 2023

References

  • Azadfard M, Huecker MR, Leaming JM. Opioid addiction. 2023.
  • Ahmad F, Rossen L, Sutton P. Products—Vital statistics rapid release—Provisional drug overdose data. 2022.
  • Koob GF, Volkow ND. Neurobiology of addiction: a neurocircuitry analysis. Lancet Psychiatry. 2016;3(8):760–19. Preprint at. doi: 10.1016/S2215-0366(16)00104-8.
  • Sherman SG, Latkin CA. Drug users’ involvement in the drug economy: implications for harm reduction and HIV prevention programs. J Urban Health. 2002;79(2):266–277. doi: 10.1093/jurban/79.2.266.
  • Wakeman S. The moral economy of heroin in ‘Austerity Britain’. Crit Criminol. 2016;24(3):363–377. doi: 10.1007/s10612-015-9312-5.
  • Richardson L, Mammel M, Milloy M-J, Hayashi K. Employment cessation, long term labour market engagement and HIV Infection risk among people who inject drugs in an urban Canadian setting. AIDS Behav. 2019;23(12):3267–3276. doi: 10.1007/s10461-019-02472-1.
  • Darke S, Larney S, Farrell M. Yes, people can die from opiate withdrawal. Addiction. 2017;112(2):199–200. doi: 10.1111/add.13512.
  • Weiss RD, Potter JS, Griffin ML, McHugh RK, Haller D, Jacobs P, Gardin J, Fischer D, Rosen KD. Reasons for opioid use among patients with dependence on prescription opioids: the role of chronic pain. J Subst Abuse Treat. 2014;47(2):140–145. doi: 10.1016/j.jsat.2014.03.004.
  • Oesterle TS, Thusius NJ, Rummans TA, Gold MS. Medication-assisted treatment for opioid-use disorder. Mayo Clin Proc. 2019;94(10):2072–2086. doi: 10.1016/j.mayocp.2019.03.029.
  • Blanco C, Volkow ND. Management of opioid use disorder in the USA: present status and future directions. Lancet. 2019;393(10182):1760–1772. doi: 10.1016/S0140-6736(18)33078-2.
  • Bisaga A, Mannelli P, Yu M, Nangia N, Graham CE, Tompkins DA, Kosten TR, Akerman SC, Silverman BL, Sullivan MA, et al. Outpatient transition to extended-release injectable naltrexone for patients with opioid use disorder: a phase 3 randomized trial. Drug Alcohol Depend. 2018;187:171–178. doi:10.1016/j.drugalcdep.2018.02.023.
  • Lee JD, Nunes EV, Novo P, Bachrach K, Bailey GL, Bhatt S, Farkas S, Fishman M, Gauthier P, Hodgkins CC, et al. Comparative effectiveness of extended-release naltrexone versus buprenorphine-naloxone for opioid relapse prevention (X: BOT): a multicentre, open-label, randomised controlled trial. Lancet. 2018;391(10118):309–318. doi: 10.1016/S0140-6736(17)32812-X.
  • McElrath K. Medication-assisted treatment for opioid addiction in the United States: critique and commentary. Subst Use Misuse. 2018;53(2):334–343. doi: 10.1080/10826084.2017.1342662.
  • Srivastava AB, Mariani JJ, Levin FR. New directions in the treatment of opioid withdrawal. Lancet. 2020;395(10241):1938–1948. doi: 10.1016/S0140-6736(20)30852-7.
  • Wang F, Meng J, Zhang L, Johnson T, Chen C, Roy S. Morphine induces changes in the gut microbiome and metabolome in a morphine dependence model. Sci Rep. 2018;8(1):3596. doi: 10.1038/s41598-018-21915-8.
  • Zhang Li, Meng J, Ban Y, Jalodia R, Chupikova I, Fernandez I, Brito N, Sharma U, Abreu MT, Ramakrishnan S, et al. Morphine tolerance is attenuated in germfree mice and reversed by probiotics, implicating the role of gut microbiome. 2019;116:13523–13532. doi: 10.1073/pnas.1901182116. PMID: 31209039.
  • Banerjee S, Sindberg G, Wang F, Meng J, Sharma U, Zhang L, Dauer P, Chen C, Dalluge J, Johnson T, et al. Opioid-induced gut microbial disruption and bile dysregulation leads to gut barrier compromise and sustained systemic inflammation. Mucosal Immunol. 2016;9(6):1418–1428. doi: 10.1038/mi.2016.9.
  • Meng J, Yu H, Ma J, Wang J, Banerjee S, Charboneau R, Barke RA, Roy S. Morphine induces bacterial translocation in mice by compromising intestinal barrier function in a TLR-Dependent manner. PLoS One. 2013;8(1):e54040. doi: 10.1371/journal.pone.0054040.
  • Patrick GA, Dewey WL, Spaulding TC, Harris LS. Relationship of brain morphine levels to analgesic activity in acutely treated mice and rats and in pellet implanted mice. J Pharmacol Exp Ther. 1975;193:876–883.
  • McLane VD, Bergquist I, Cormier J, Barlow DJ, Houseknecht KL, Bilsky EJ, Cao L. Long-term morphine delivery via slow release morphine pellets or osmotic pumps: Plasma concentration, analgesia, and naloxone-precipitated withdrawal. Life Sci. 2017;185:1–7. doi:10.1016/j.lfs.2017.07.016.
  • Bobzean SAM, Kokane SS, Butler BD, Perrotti LI. Sex differences in the expression of morphine withdrawal symptoms and associated activity in the tail of the ventral tegmental area. Neurosci Lett. 2019;705:124–130. doi:10.1016/j.neulet.2019.04.057.
  • Hadschieff V, Drdla-Schutting R, Springer DN, Siegert ASM, Schroeder H, Sandkühler J. Fundamental sex differences in morphine withdrawal-induced neuronal plasticity. Pain. 2020;161(9):2022–2034. doi: 10.1097/j.pain.0000000000001901.
  • Brewer AL, Lewis CC, Eggerman L, Blokker A, Burkland JA, Johnsen M, Quock RM. Modeling spontaneous opioid withdrawal in male and female outbred mice using traditional endpoints and hyperalgesia. Behav Pharmacol. 2023;34(2–3):112–122. doi: 10.1097/FBP.0000000000000714.
  • Papaleo F, Contarino A. Gender- and morphine dose-linked expression of spontaneous somatic opiate withdrawal in mice. Behav Brain Res. 2006;170(1):110–118. doi: 10.1016/j.bbr.2006.02.009.
  • Radke AK, Gewirtz JC, Carroll ME. Effects of age, but not sex, on elevated startle during withdrawal from acute morphine in adolescent and adult rats. Behav Pharmacol. 2015;26(5):485–488. doi: 10.1097/FBP.0000000000000151.
  • Meng J, Banerjee S, Li D, Sindberg GM, Wang F, Ma J, Roy S. Opioid exacerbation of gram-positive sepsis, induced by gut microbial modulation, is rescued by IL-17A neutralization. Sci Rep. 2015;5(1):10918. doi: 10.1038/srep10918.
  • Heijtz RD, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S. Normal gut microbiota modulates brain development and behavior. 2011;108:3047–3052. doi: 10.1073/pnas.1010529108.
  • Park AJ, Collins J, Blennerhassett PA, Ghia JE, Verdu EF, Bercik P, Collins SM. Altered colonic function and microbiota profile in a mouse model of chronic depression. Neurogastroenterol Motil. 2013;25(9):733–e575. doi: 10.1111/nmo.12153.
  • Loos M, Koopmans B, Aarts E, Maroteaux G, van der Sluis S, Verhage M, Smit AB. Within-strain variation in behavior differs consistently between common inbred strains of mice. Mamm Genome. 2015;26(7–8):348–354. doi: 10.1007/s00335-015-9578-7.
  • Nigri M, Åhlgren J, Wolfer DP, Voikar V. Role of environment and experimenter in reproducibility of behavioral studies with laboratory mice. Front Behav Neurosci. 2022;16. doi:10.3389/fnbeh.2022.835444.
  • van der Veen R, Bonapersona V, Joëls M. The relevance of a rodent cohort in the consortium on individual development. Dev Cogn Neurosci. 2020;45:100846. doi:10.1016/j.dcn.2020.100846.
  • Taylor JR, Punch LJ, Elsworth JD. A comparison of the effects of clonidine and CNQX infusion into the locus coeruleus and the amygdala on naloxone-precipitated opiate withdrawal in the rat. Psychopharmacol (Berl). 1998;138(2):133–142. doi: 10.1007/s002130050655.
  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi: 10.1038/nmeth.3869.