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An interdisciplinary review of the thanatomicrobiome in human decomposition

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Abstract

Death does not occur instantaneously and organs do not decompose at the same rate or in the same way. Nulligravid human uteri and prostate glands are the last internal organs to deteriorate during decomposition; however, the reason for this very important observation is still enigmatic. Recent studies have elucidated that the composition and abundance of microbes in the human thanatomicrobiome (microbiome of death) varies by organ and changes as a function of time and temperature. The ileocecal area has the largest absolute postmortem burden that spreads to the liver and spleen and continues to the heart and brain depending on the cause of death. To truly understand the mechanisms of microbial assembly during decomposition, a thorough examination of different strategies utilized by the trillions of microbes that colonize decaying tissues is needed from a multi-organ and multidisciplinary approach. In this review, we highlight interdisciplinary research and provide an overview of human decomposition investigations of thanatomicrobiomic changes in internal organs.

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References

  1. Ford WW. On the bacteriology of normal organs. Epidemiol Infect. 1901;1:277–84.

    CAS  Google Scholar 

  2. Stewart EJ. Growing unculturable bacteria. J Bacteriol. 2012;194:4151–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Gevers W. Biochemical aspects of cell death. Forensic Sci. 1975;6:25–9.

    Article  CAS  PubMed  Google Scholar 

  4. Can I, Javan GT, Pozhitkov AE, Noble PA. Distinctive thanatomicrobiome signatures found in the blood and internal organs of humans. J Microbiol Methods. 2014;106:1–7.

    Article  CAS  PubMed  Google Scholar 

  5. Javan GT, Finley SJ, Can I, Wilkinson JE, Hanson JD, Tarone AM. Human thanatomicrobiome succession and time since death. Sci Rep. 2016;6:29598.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Javan GT, Finley SJ, Abidin Z, Mulle JG. The thanatomicrobiome: a missing piece of the microbial puzzle of death. Front Microbiol. 2016;7:225.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Adserias Garriga J, Quijada NM, Hernandez M, Lázaro DR, Steadman D, Garcia-Gil J. Dynamics of the oral microbiota as a tool to estimate time since death. Mol Oral Microbiol. 2017;32:511–6.

    CAS  PubMed  Google Scholar 

  8. DeBruyn JM, Hauther KA. Postmortem succession of gut microbial communities in deceased human subjects. PeerJ. 2017;5:e3437.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Vass AA. Beyond the grave-understanding human decomposition. Microbiol Today. 2001;28:190–3.

    Google Scholar 

  10. Stefanuto PH, Perrault KA, Grabherr S, Varlet V, Focant JF. Postmortem internal gas reservoir monitoring using GC× GC-HRTOF-MS. Separations. 2016;3:24.

    Article  Google Scholar 

  11. Carter DO, Tomberlin JK, Benbow ME, Metcalf JL. Perspectives on the future of forensic microbiology. In: Carter DO, Tomberlin JK, Benbow ME, Metcalf JL, editors. Forensic microbiology. New York City: Wiley; 2017. p. 376–8.

    Chapter  Google Scholar 

  12. Pascual J, von Hoermann C, Rottler-Hoermann AM, et al. Function of bacterial community dynamics in the formation of cadaveric semiochemicals during in situ carcass decomposition. Environ Microbiol. 2017;9:3310–22.

    Article  Google Scholar 

  13. Javan GT, Finley SJ, Smith T, Miller J, Wilkinson JE. Cadaver thanatomicrobiome signatures: the ubiquitous nature of Clostridium species in human decomposition. Front Microbiol. 2017;8:2096.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bell CR, Wilkinson JE, Robertson BK, Javan GT. Sex-related differences in the thanatomicrobiome in postmortem heart samples using bacterial gene regions V1-2 and V4. J Appl Microbiol. 2018;67:144–53.

    Article  CAS  Google Scholar 

  15. Pechal JL, Schmidt CJ, Jordan HR, Benbow ME. A large-scale survey of the postmortem human microbiome, and its potential to provide insight into the living health condition. Sci Rep. 2018;8:5724.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Tuomisto S, Pessi T, Collin P, Vuento R, Aittoniemi J, Karhunen PJ. Changes in gut bacterial populations and their translocation into liver and ascites in alcoholic liver cirrhotics. BMC Gastroenterol. 2014;14:40.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Belk A, Xu ZZ, Carter DO, Lynne A, Bucheli S, Knight R, et al. Microbiome data accurately predicts the postmortem interval using random forest regression models. Genes. 2018;9:104.

    Article  PubMed Central  Google Scholar 

  18. Zhou C, Byard RW. Factors and processes causing accelerated decomposition in human cadavers–an overview. J Forensic Legal Med. 2011;18:6–9.

    Article  Google Scholar 

  19. Ellis KJ. Human body composition: in vivo methods. Physiol Rev. 2000;80:649–80.

    Article  CAS  PubMed  Google Scholar 

  20. Matuszewski S, Konwerski S, Frątczak K, Szafałowicz M. Effect of body mass and clothing on decomposition of pig carcasses. Int J Legal Med. 2014;128:1039–48.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Vass AA, Barshick SA, Sega G, et al. Decomposition chemistry of human remains: a new methodology for determining the postmortem interval. J For Sci. 2002;47:542–53.

    CAS  Google Scholar 

  22. Olakanye AO, Nelson A, Ralebitso-Senior TK. A comparative in situ decomposition study using still born piglets and leaf litter from a deciduous forest. Forensic Sci Int. 2017;276:85–92.

    Article  PubMed  Google Scholar 

  23. Dent BB, Forbes SL, Stuart BH. Review of human decomposition processes in soil. Environ Geol. 2004;45:576–85.

    Article  CAS  Google Scholar 

  24. Goff ML. Early post-mortem changes and stages of decomposition in exposed cadavers. Exp Appl Acarol. 2009;49:21–36.

  25. Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell. 2012;148:1258–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. DeVault TL, Rhodes OE Jr, Shivik JA. Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos. 2003;102:225–34.

    Article  Google Scholar 

  27. Wilson EE, Wolkovich EM. Scavenging: how carnivores and carrion structure communities. Trends Ecol Evol. 2011;26:129–35.

    Article  PubMed  Google Scholar 

  28. Benbow ME, Lewis AJ, Tomberlin JK, Pechal JL. Seasonal necrophagous insect community assembly during vertebrate carrion decomposition. J Med Entomol. 2013;50:440–50.

    Article  CAS  PubMed  Google Scholar 

  29. Damann FE, Williams DE, Layton AC. Potential use of bacterial community succession in decaying human bone for estimating postmortem interval. J Forensic Sci. 2015;60:844–50.

    Article  PubMed  Google Scholar 

  30. Molina DK, DiMaio VJ. Normal organ weights in men: part II—the brain, lungs, liver, spleen, and kidneys. Am J Forensic Med Pathol. 2012;33:368–72.

    Article  PubMed  Google Scholar 

  31. Gunn A, Pitt SJ. Microbes as forensic indicators. Trop Biomed. 2012;29:311–30.

    Google Scholar 

  32. Huang C, Sloan EA, Boerkoel CF. Chromatin remodeling and human disease. Curr Opin Genet Dev. 2003;13:246–52.

    Article  CAS  PubMed  Google Scholar 

  33. Bär W, Kratzer A, Mächler M, Schmid W. Postmortem stability of DNA. Forensic Sci Int. 1988;39:59–70.

    Article  PubMed  Google Scholar 

  34. Hynd MR, Lewohl JM, Scott HL, Dodd PR. Biochemical and molecular studies using human autopsy brain tissue. J Neurochem. 2003;85:543–62.

    Article  CAS  PubMed  Google Scholar 

  35. Williams T, Soni S, White J, Can G, Javan GT. Evaluation of DNA degradation using flow cytometry: promising tool for postmortem interval determination. Am J Forensic Med Pathol. 2015;36:104–10.

    Article  PubMed  Google Scholar 

  36. Di Nunno NR, Costantinides F, Bernasconi P, Bottin C, Melato M. Is flow cytometric evaluation of DNA degradation a reliable method to investigate the early postmortem period? Am J Forensic Med Pathol. 1998;19:50–3.

    Article  PubMed  Google Scholar 

  37. Molina DK, DiMaio VJ. Normal organ weights in women: part I-the heart. Am J Forensic Med Pathol. 2015;36:176–81.

    Article  PubMed  Google Scholar 

  38. Payne-James J, Simpson K. Simpson’s forensic medicine. Boca Raton: CRC Press; 2011.

    Google Scholar 

  39. Levy AD, Harcke HT Jr. Essentials of forensic imaging: a text-atlas. Boca Raton: CRC Press; 2010.

    Book  Google Scholar 

  40. Trotter SA, Brill Ii LB, Bennett JP. Stability of gene expression in postmortem brain revealed by cDNA gene array analysis. Brain Res. 2002;942:120–3.

    Article  CAS  PubMed  Google Scholar 

  41. Yasojima K, McGeer EG, McGeer PL. High stability of mRNAs postmortem and protocols for their assessment by RT-PCR. Brain Res Protocol. 2001;8:212–8.

    Article  CAS  Google Scholar 

  42. Donaldson AE, Lamont IL. Biochemistry changes that occur after death: potential markers for determining post-mortem interval. PLoS One. 2013;8:e82011.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Cocariu EA, Mageriu V, Stăniceanu F, Bastian A, Socoliuc C, Zurac S. Correlations between the autolytic changes and postmortem interval in refrigerated cadavers. Rom J Intern Med. 2016;54:105–12.

    PubMed  Google Scholar 

  44. Sibulesky L. Normal liver anatomy. Clin Liver Dis. 2013;2(S1).

  45. Tuomisto S, Karhunen PJ, Vuento R, Aittoniemi J, Pessi T. Evaluation of postmortem bacterial migration using culturing and real-time quantitative PCR. J Forensic Sci. 2013;58:910–6.

    Article  CAS  PubMed  Google Scholar 

  46. Carpenter HM, Wilkins RM. Autopsy bacteriology: review of 2,033 cases. Arch Pathol. 1964;77:73–81.

    CAS  PubMed  Google Scholar 

  47. Wilson SJ, Wilson ML, Reller LB. Diagnostic utility of postmortem blood cultures. Arch Pathol Lab Med. 1993;117:986–8.

    CAS  PubMed  Google Scholar 

  48. Boutin EL, Battle E, Cunha GR. The response of female urogenital tract epithelia to mesenchymal inductors is restricted by the germ layer origin of the epithelium: prostatic inductions. Differentiation. 1991;48:99–105.

    Article  CAS  PubMed  Google Scholar 

  49. Chang K, Zhang L. Steroid hormones and uterine vascular adaptation to pregnancy. Reprod Sci. 2008;15:336–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Casper JL. A handbook of the practice of forensic medicine: based upon personal experience. London: New Sydenham Society; 1861.

    Google Scholar 

  51. Tolbert M, Finley SJ, Visonà SD, Soni S, Osculati A, Javan GT. The thanatotranscriptome: gene expression of male reproductive organs after death. Gene. 2018;675:191–6.

    Article  CAS  PubMed  Google Scholar 

  52. Lee CH, Akin-Olugbade O, Kirschenbaum A. Overview of prostate anatomy, histology, and pathology. Endocrinol Metab Clin N Am. 2011;40:565–75.

    Article  CAS  Google Scholar 

  53. Suzuki Y, Tsujimoto Y, Matsui H, Watanabe K. Decomposition of extremely hard-to-degrade animal proteins by thermophilic bacteria. J Biosci Bioeng. 2006;102:73–81.

    Article  CAS  PubMed  Google Scholar 

  54. Hyde ER, Haarmann DP, Lynne AM, Bucheli SR, Petrosino JF. The living dead: bacterial community structure of a cadaver at the onset and end of the bloat stage of decomposition. PLoS One. 2013;8:e77733.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Hyde E, Haarmann DP, Petrosino JF, Lynne AM, Bucheli SR. Initial insights into bacterial succession during human decomposition. Int J Legal Med. 2015;129:661–71.

    Article  PubMed  Google Scholar 

  56. Metcalf JL, Parfrey LW, Gonzalez A, et al. A microbial clock provides an accurate estimate of the postmortem interval in a mouse model system. elife. 2013;2:e01104.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Thomas TB, Finley SJ, Wilkinson JE, Wescott DJ, Gorski A, Javan GT. Postmortem microbial communities in burial soil layers of skeletonized humans. J Forensic Legal Med. 2017;49:43–9.

  58. Pechal JL, Crippen TL, Tarone AM. Microbial community functional change during vertebrate carrion decomposition. PLoS One. 2013;8:e79035.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Pechal JL, Crippen TL, Benbow ME, Tarone AM, Dowd S, Tomberlin JK. The potential use of bacterial community succession in forensics as described by high throughput metagenomic sequencing. Int J Legal Med. 2014;128:193–205.

    Article  PubMed  Google Scholar 

  60. Benbow ME, Pechal JL, Lang JM, Erb R, Wallace JR. The potential of high-throughput metagenomic sequencing of aquatic bacterial communities to estimate the postmortem submersion interval. J Forensic Sci. 2015;60:1500–10.

    Article  PubMed  Google Scholar 

  61. Fredette JW. Bacteremias in the agonal period. Transl Res. 1916;2:180–8.

    Google Scholar 

  62. Fouts DE, Torralba M, Nelson KE, Brenner DA, Schnabl B. Bacterial translocation and changes in the intestinal microbiome in mouse models of liver disease. J Hepatol. 2012;56:1283–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Heimesaat MM, Boelke S, Fischer A, et al. Comprehensive postmortem analyses of intestinal microbiota changes and bacterial translocation in human flora associated mice. PLoS One. 2012;7:e40758.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Burcham ZM, Hood JA, Pechal JL, et al. Fluorescently labeled bacteria provide insight on post-mortem microbial transmigration. Forensic Sci Int. 2016;264:63–9.

    Article  CAS  PubMed  Google Scholar 

  65. Dix J, Graham M. Time of death, decomposition and identification: an atlas. Boca Raton: CRC press; 1999.

    Book  Google Scholar 

  66. Latil M, Rocheteau P, Châtre L, et al. Skeletal muscle stem cells adopt a dormant cell state post mortem and retain regenerative capacity. Nat Commun. 2012;3:903.

    Article  PubMed  Google Scholar 

  67. Mostafa EM, El-Elemi AH, El-Beblawy MA, Dawood AE. Adult sex identification using digital radiographs of the proximal epiphysis of the femur at Suez Canal University Hospital in Ismailia, Egypt. Egypt J Forensic Sci. 2012;2:81–8.

    Article  Google Scholar 

  68. Đurić M, Rakočević Z, Đonić D. The reliability of sex determination of skeletons from forensic context in the Balkans. Forensic Sci Int. 2005;147:159–64.

    Article  PubMed  Google Scholar 

  69. Campobasso CP, Introna F. The forensic entomologist in the context of the forensic pathologist’s role. Forensic Sci Int. 2001;120:132–9.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This review paper was supported by National Science Foundation HRD 1401075 and National Institute of Justice 2017-MU-MU-0042 grants.

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Authors and Affiliations

  1. Physical Sciences Department, Forensic Science Program, Alabama State University, 915 S. Jackson St., Hatch Hall Building Room 251, Montgomery, AL, 36104, USA

    Gulnaz T. Javan & Sheree J. Finley

  2. Faculty of Medicine and Life Sciences, Department of Forensic Medicine, University of Tampere, Tampere, Finland

    Sari Tuomisto

  3. Department of Biopharmaceutical Sciences, University of Illinois at Chicago, Chicago, IL, USA

    Ashley Hall

  4. Department of Entomology and Department of Osteopathic Medicine, Michigan State University, East Lansing, MI, USA

    M. Eric Benbow

  5. Department of Biological Sciences, Florida International University, Miami, FL, USA

    DeEtta Mills

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  1. Gulnaz T. Javan
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  2. Sheree J. Finley
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  5. M. Eric Benbow
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Correspondence to Gulnaz T. Javan.

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Javan, G.T., Finley, S.J., Tuomisto, S. et al. An interdisciplinary review of the thanatomicrobiome in human decomposition. Forensic Sci Med Pathol 15, 75–83 (2019). https://doi.org/10.1007/s12024-018-0061-0

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